Outline for HISTORY 100 at UMass
Outline for HISTORY 100 at UMass
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parlIII Integration Chapter 12 The Sense Organs Chapter 13 The Nervous System 1 Organization Spinal Cord and Peripheral Nerves Chapter 14 The Nervous System 11 The Brain Chapter 15 Endocrine Integration The Sense Organs PRECIS Vertebrates receive information about changes within their bodies and in the outside world through free nerve endings and a variety of specialized receptor cells located in sense organs The major sensory systems of vertebrates and some of their functional anatomical changes during evolution will be examined in this chapter OUTLINE Receptors Chemoreceptors Olfactory System The Vomeronasal Organ The Terminal Nerve Gustation Cutaneous Receptors Proprioceptors Lateral Line System Basic Organization of the Lateral Line System Electroreceptors The Ear Inner Ear Structure Equilibrium Hearing Mechanisms of Ch ondrichthyans and Teleosts Hearing Systems of Tetrapods The Ear of Sauropsids The Ear of Lissamphibians Evolution of the Mammalian Ear Photoreceptors Median Eyes The Structure and Function of ImageForming Eyes The Fibrous Tunic Vascular Tunic Choroid Iris and Ciliary Body Th e Retina The Origin and Development of the Eye Evolutionary Adaptations of the Eye The Eyes ofLampreys Chan driehthyans and Aetin opterygians The Eye of Terrestrial Vertebrates Thermoreceptors To avoid being eaten to find shelter food and matesiin short to survive in a changing worldivertebrates must detect changes in their external and internal environments and make appropriate behavioral and physiological responses A study of the sense organs and sensory systems used to do this can reveal much about the biology of a vertebrate The ability to detect and respond to change is a basic property of life and to a degree all living cells have it but as animals became more active and complex certain cells became specialized as receptors to monitor the environment for the benefit of the entire organism Most vertebrate receptors develop embryologically from the neural tube the neural crest or the neurogenic placodes Chapter 4 and connect to other cells of the nervous system Incoming sensory information is integrated by the nervous system and responses are generated in the forms of nerve impulses or hormones to activate the appropriate muscles glands and other effector organs Nervous and hormonal integration overlap in many ways but nervous integration deals with more rapid and discrete types of activity than does hormonal integration In this and the next two chapters we will examine receptors and the nervous system39 endocrine glands will be described in Chapter 15 In evaluating the functional anatomy of sensory organs it is insufficient to demonstrate that a particular type of receptor cell responds physiologically to a certain stimulus because a single type of cell may respond to a variety of imposed stimuli including pain temperature and pressure Rather sensory biologists seeking to understand the evolution and functional morphology of a sensory system must demonstrate that an animal actually uses specific types of stimuli to cue behavioral or physiological changes We will discuss a classic example of this concept later in the section on electroreception p 409 and Fig 1212 Receptors A receptive region of a nerve cell or neuron may be stimulated directly by environmental changes within or outside the body and in response generate a nerve impulse This is a common method of reception among invertebrate metazoans Vertebrates retain nerve endings of this type which are known as free nerve endings but vertebrates also have many specialized types of receptor cells and neurons Receptor cells act as transducers which are instruments that convert one form of energy into another They are specialized to detect a minute energy change in a specific environmental signal such as light pressure sound or taste and then initiate a nerve impulse in a sensory neuron Receptor cells have an electrical resting potential derived from an unequal distribution of ions across their plasma membrane The resting potential is maintained in phasic receptors until they are stimulated Upon stimulation of a phasic receptor cell ion channels in the plasma membrane open producing an ionic depolarization of the membrane so that the cell develops a receptor potential This response is graded39 that is the receptor potential is proportional to the magnitude of the stimulus A few receptors are tonic that is they are always active Stimulation of tonic receptors increases or decreases the receptor potential Only when the receptor potential attains a certain magnitude does it initiate a nerve impulse in the sensory neuron Nerve impulses never vary in magnitude with the magnitude of the receptor potential A nerve impulse is said to be all or none it either occurs or it does not occur The magnitude of sensory stimulation above the threshold level needed to initiate a nerve impulse is encoded by the frequency of nerve impulses and sometimes by their pattern The decoding and perception of particular sensations are functions not of the nerve impulse but of the specificity of the receptors and the connections of their neurons within the nervous system Vertebrates evolved receptor mechanisms that detect environmental changes important for their survival39 many physiochemical changes that are less critical go undetected Humans for example cannot sense small changes in electric fields but many aquatic vertebrates such as chondrichthyans can Some receptor types respond to more than one type of incoming stimulus e g certain cutaneous receptors of the skin can detect pressure which is a mechanical stimulus and temperature which is an electromagnetic stimulus It is convenient to classify the numerous receptors according to the major type of sensory signal to which they are sensitive Chemical receptors Olfactory cells smell Taste buds taste Mechanical temperature and electrical receptors Cutaneous receptors Free nerve endings pain temperature and other modalities Meissner s corpuscles touch and pressure Merkel s disks touch and pressure Pacinian corpuscles touch and pressure Ruffini endings touch and pressure Eim er s organs touch and pressure Sinus hairs 5 whiskers touch and pressure Proprioreceptors Tendon and joint receptors tension Muscle spindles degree and rate of contraction Lateral line ear and electroreceptors Hair cells vibrations and gravity Ampullary organ cells electric fields Tuberous organ cells electric fields Photoreceptors and specialized therm oreceptors Rod and cone cells visible electromagnetic radiation Pit organ cells infrared electromagnetic radiation This organization of receptor types is based on the primary sources of incoming stimuli chemical mechanical and electrical and electromagnetic It sometimes also is useful to group receptor types as we did with bones and muscles according to their locations within the body Using such a scheme we can recognize somatic receptors sometimes called exteroreceptors which are located in the outer wall of the body Visceral receptors which can be termed enteroreceptors lie deeper within the body Many free nerve endings and individual receptor cells are scattered through the skin and tissues of the body Others are aggregated and combined with cells that support and protect them amplify the environmental stimulus and help localize the source of the stimulus We call such aggregations sense organs In this abbreviated treatment we can examine and compare only a few of the many receptors and sense organs of vertebrates Chemoreceptors All animals detect many chemical changes in their external and internal environments Vertebrates receive chemosensory signals in four ways First internal chem oreceptors continuously monitor certain aspects of the internal environment Examples include the carotid and aortic bodies located on major arteries near the heart which detect changes in the oxygen and carbon dioxide content of the blood The pH of cerebrospinal fluid which decreases ie becomes acidic when carbon dioxide levels in the blood increase also is monitored by hydrogen ion receptors in the fourth ventricle of the brain The rates of breathing and blood circulation are reflexively adjusted by information provided by all these receptors Second many free nerve endings are present in serous and mucous membranes of the eyes mouth and nose and detect noxious chemical stimuli Lachrymotor agents ie chemicals that make you cry eg the odor of a freshly chopped onion or tear gas are perceived in part by such endings Third and fourth vertebrates have receptors that detect odors and food in the external environment We have olfactory receptors L alfaclus 5 smell from alfacere 5 to smell in our noses and gustatory receptors L gustatus 5 tasted from guslare 5 to taste on our tongues Although taste and smell have much in common we think of smell as chemical information carried in the air and taste as chemical information primarily from food or fluids in contact with parts of the mouth This distinction becomes blurred for many aquatic craniates the body surfaces nose and mouth of which are bathed in water In general olfactory receptors can detect a lower concentration of a substance than can gustatory ones so they can detect faint traces of distant substances Olfactory System Olfactory receptors are specialized neurons that detect chemical substances called odorants Olfactory neurons are essentially similar in all vertebrates and they develop embryonically from paired neurogenic placodes that invaginate to form a pair of nasal sacs see Chapter 4 for discussion of neurogenic placodes The cell body of the neuron which contains the cell s nucleus lies in the olfactory epithelium and sends its receptive process the dendrite to the surface Fig 121 Nonmotile cilia on the end of the dendrite which range in number from about 5 to 20 increase the cell s receptive surface several hundredifold A long process or axon extends from the cell body to the main olfactory bulb of the brain Bundled together these axons constitute the olfactory nerve cranial nerve 139 Chapter 13 By comparison with other sensory systems olfactory impulses have a particularly short and direct route to the brain Odorants in solution in the mucous sheet flowing across the olfactory epithelium bind with receptor molecules in the plasma membrane of the olfactory cilia and initiate receptor potentials Olfactory neurons are extraordinarily sensitive Dogs can detect a substance known as diacetal in concentrations as low as 17 3 10218 molar Vertebrates can detect a wide range of odors possibly as many as 10000 different odors in the case of humans but how the distinctions are made is not entirely clear The distinctive molecular configurations of odorant molecules allow them to bind with and activate specific receptor proteins in the plasma membrane of the cell The complex genetic control of the synthesis of receptor proteins makes possible the production of different receptor protein families that recognize major differences among odorants One family for example may recognize aromatic compounds such as benzene and its derivatives another family may recognize aliphatic compounds and so on Subtle variations in receptor proteins may enable the distinction of different benzene derivatives toluene xylene or phenol But it is still unlikely that there is a different receptor protein for each possible odorant Each olfactory cell can bind with one or a small group of structurally related odorants Perception of different odors probably depends on processing in the brain of the combination of information from stimulated olfactory neurons the intensity of stimulation and the synaptic pattern that their projections make within the central nervous system Perhaps an analogy is color vision in which the processing of information from only three types of photoreceptors red green and blue enables us to distinguish hundreds of hues Olfactory receptor cells show considerable sensory adaptation They are very sensitive to a new odor but their activity slows down or stops in the continued presence of the same odor Thus we notice an odor on first entering the kitchen but fail to detect it after a few minutes Olfactory cells are interspersed with and supported by sustentacular cells Fig 121 Mucus is secreted by the sustentacular cells and also by simple goblet cells Tetrapods also have large multicellular mucous glands in the olfactory epithelium Fig 121 Cells with motile cilia also occur in the olfactory epithelium of tetrapods these cilia clear mucus from the surface of the epithelium Basal cells in the epithelium can differentiate into new cells of any type to replace cells that are lost Vertebrates move water or air across the olfactory epithelium in different ways A lamprey has a single nostril on the top of the head that leads to the olfactory sac embryonically paired and to the hypophyseal sac Fig lZZA Respiratory movements of the pharynx vary the pressure on the hypophyseal sac so that water is alternately sucked into and forced out of the adjacent olfactory sac In contrast the paired olfactory sacs of most aquatic gnathostomes have distinct incurrent and excurrent external nostrils or nares on the surface of the head Fig lZZB Pleats inside the olfactory sacs increase their surface area Water is drawn into an incurrent naris by ciliary action or by pumping or in many cases by suction developed in the oral cavity The excurrent openings from olfactory sacs or nasal cavities of choanates1 are internal nostrils or choanae Gr choane 5 funnel that open in the roof of the mouth Fig 123 The nasal cavities of choanates are also part of the airways to and from the lungs The olfactory epithelium of choanates is restricted to the dorsal part of the nasal passage Fig 1241 and is ventilated by the respiratory movements In lissamphibians and basal sauropsids which do not ventilate their lungs as frequently as do birds and mammals these respiratory movements are supplemented by additional pumping movements of the floor of the buccopharyngeal cavity Chapter 18 The surface area of the olfactory epithelium is increased in amniotes by scrolls of bone collectively called the turbinates Fig 124B Turbinates are particularly well developed in mammals They bear the olfactory epithelium and greatly increase the olfactory surface area Their presence in early mammals such as TMarganucadan suggests that these animals had an acute olfactory sense that probably reflected a nocturnal mode of life see Focus 35 One of the turbinates lies at the front of the nasal cavity directly in line with the respiratory current It helps cleanse moisten and warm inspired air and it cools expired air As expired air cools water condenses and is reused to moisten inspired air Such a mechanism likely evolved in relation to the elevated ventilation rates and endothermy that characterized mammalian evolution The sense of smell provides most vertebrates with considerable information about their surroundings It helps them find food recognize members of their own species and avoid enemies It also aids in homing in some species For example young salmon become imprinted to the odors of the stream in which they hatched and years later olfactory clues help them return to the same stream to spawn Odor detection also is a part of a communication system based on the secretion into the external environment of species specific chemical messengers called pheromones Gr pherein 5 to bear 1 harmaein 5 to excite Pheromones have many advantages Most are small molecules that are easy to synthesize They may persist in the environment for hours or days diffuse around obstacles and are effective in the dark The amount of information one pheromone can convey is limited but some vertebrates secrete several pheromones with different meanings Pheromones frequently are used to warn conspecifics of danger For example injured minnows produce an alarm substance known as Schrecksla that induces others to flee Other pheromones indicate social status in a hierarchy are used to establish territories or signal sexual readiness For example female goldfish produce a hormone that promotes oocyte maturation Some of this hormone also is released as a pheromone into the environment which sexually arouses mature conspecific males and causes them to liberate sperm Sorensen et al 1987 Odors are less important for arboreal or flying vertebrates than for aquatic and terrestrial ones because olfactory trails do not always cross gaps from tree to tree Only a few birds including the nocturnal and ground dwelling kiwi of New Zealand39 vultures and other scavengers and certain marine birds such as fulmars have been thought to have a well developed sense of smell This sense is poorly developed in primates for they became arboreal animals early in their evolutionary history Only vestiges of olfactory organs remain in cetaceans which close their external nostrils under water The Vomeronasal Organ In most tetrapods the medioventral part of the olfactory epithelium forms a pair of vomeronasal organs or Jacobson s organ Fig 124 These organs are absent from most species of aquatic tetrapods including larval lissamphibians most turtles crocodilians and aquatic mammals2 Birds most bats and many primates including humans also lack them although vestiges sometimes appear during embryonic development The receptive neurons of the vomeronasal organ resemble olfactory ones except that the cilia are replaced by microvilli The axons of the vomeronasal neurons terminate in the accessory olfactory bulb of the brain which has different projections within the brain than does the main olfactory bulb The paired vom eronasal organs are not completely separated from the main olfactory chambers in lissamphibians tuataras and scleroglossans3 and odorants can enter the vom eronasal organ via either the external or internal nostrils In squamates the vomeronasal organs usually form a pair of distinct saclike structures that have their own entrances into the mouth Derived scleroglossans use them in combination with a forked tongue Fig 1241 Odorants adhere to the tongue as it is darted in and out of the mouth and the tips of the tongue are brought close to the palatal entrances of the vom eronasal organs Snakes use this mechanism to follow prey trails and in sexual recognition In mammals the vom eronasal organs are culdesacs that open into the front of the mouth through the nasopalatine duct the nasal cavity or both the nasal cavity and the mouth Fig 1243 Many mammals use the vomero nasal organ to detect pheromones important to the animal s social and sexual interactions Males of some species can determine whether a female is in heat by the pheromones she produces When next you walk the family dog you may notice it mouthing but not swallowing certain objects This activity known as the Flehmen response blocks the nostrils and the back of the oral cavity in order to more efficiently suck odorants into the vomeronasal organ Fig 124C The Terminal Nerve All living gnathostomes have a terminal nerve that usually is applied closely to the surface of the olfactory nerve4 It is tiny in most craniates but large in some species of marine mammals The distal ends of its neurons terminate in the rostral part of the nasal mucosa and their cell bodies are scattered along the nerve The functions of the terminal nerve are not entirely clear but in jawed fishes lissamphibians and mammals its fibers contain gonadotropinireleasing hormone GnRH This hormone which also is found in many brain cells notably those of the hypothalamus helps regulate reproduction Chapter 21 The presence of GnRH in the terminal nerve suggests that it may be part of a chem osensory system regulating some aspects of reproduction via the nasal detection of pheromones For example stimulation of the terminal nerve in male elasmobranchs can cause sperm to be released Gustation Taste is detected by barrelshaped clusters of 20 to 30 receptor and sustentacular cells of endodermal origin that are called taste buds Fig 1251 The surfaces of the taste cells bear microvilli that contain the molecules receptive to chemicals Taste buds open to the surface by pores Because taste buds are exposed and subject to wear mature cells have a life span of only a week or two undifferentiated cells within the buds continue to divide and transform into replacement cells The receptive cells are supplied by distinct sensory neurons that return to the brain in cranial nerves from the mouth and pharynx The facial nerve VII carries fibers from taste buds in the oral cavity the glossopharyngeal IX and vagal X nerves carry fibers from those in the pharynx Chapter 13 Taste buds traditionally are classified as visceral sensory organs because most are oriented to the interior of the visceral tube and appear to develop from endoderm Although taste buds are used prim arily to find and recognize food they also are important in sexual and other behavioral interactions in many species Taste buds do not respond to as low a concentration of substances as do olfactory cells and the substances must be in contact with the buds Taste buds also respond to a relatively narrower spectrum of chemical substances Areas of the hum an tongue are particularly sensitive to salt sour sweet and bitter substances but you do not need to be a gourmet to detect more than this As with olfactory cells different categories of taste buds likely are sensitive to a spectrum of substances The distinction among tastes probably results from the particular combination of taste buds that are activated and the pattern of their projection in the brain Our final perception of what we call flavor depends on a complex mixture of signals from not only the taste buds but also olfactory cells and tactile receptors It is not easy to sort out the contributions of each and the same is probably true for other vertebrates Taste buds are distributed throughout the oral cavity and pharynx in fishes and lissamphibians They also spread onto the skin in many fishes and aquatic lissamphibians They occur over the entire body surface in catfishes and minnows but are particularly abundant on the barbels around the mouth Fig lZSB Taste buds on the body surface have been thought to arise from endodermal cells that migrate onto the body surface during development5 They are supplied by the facial VII nerve In amniotes taste buds are limited to the oral cavity and pharynx Many sauropsids including birds have taste buds on the back of the tongue and palate Taste buds are more abundant in mammals Most are associated with papillae on the tongue but some are found on the palate pharynx and epiglottis Cutaneous Receptors Cutaneous receptors are used for sensing the surfaces of objects or other individuals For example many aquatic craniates receive considerable information about their aqueous environment from a special group of cutaneous mechanoreceptors known as the lateral line system which lies in or just beneath the skin This system is so intriguing and important that we devote to it a special section p 406 All vertebrates have branching free nerve endings in their dermis and these may penetrate the epidermis These free nerve endings are activated by vibrations touch injuries abrupt temperature changes and other external stimuli Their primary function is to alert the animal to cuts burns and other injuries that we perceive as painful Specialized cutaneous mechanoreceptors also are present In all cases a very slight mechanical deformation of some part of the plasma membrane of either a free neuron or a specialized receptor cell initiates the receptor potential Most cutaneous receptors are confined to the skin and are supplied by spinal nerves A few spread into the mouth and other mucosae such as the moist layer of cells covering the eyeball the cornea39 see p 426 These are supplied by branches of the trigeminal cranial nerve V which also supplies cutaneous receptors over the surface of the head All cutaneous receptors are regarded as somatic receptors Mammalian skin contains a bewildering array of touch and pressure receptors Some are nerve endings layered or laminated with connective tissue fibers Other nerve endings are not laminated but are typically associated with receptive cells Probably because they are protected from their surroundings laminated receptors adapt rapidly to changes in a stimulus and give a response when the stimulus begins or ends They do not respond to a continuing stimulus Endings that are not laminated adapt more slowly and remain active for the duration of the stimulus Those endings laminated or not that lie just beneath the epidermis detect stimuli in their immediate vicinity ie their receptive fields are small and well defined Examples shown in Figure 1261 are Merkel s disks not laminated and slowly adapting and Meissner s corpuscles laminated and rapidly adapting Receptors lying deeper in the dermis detect stimuli over a wider and less clearly defined area Examples are Ruf ni endings not laminated and slowly adapting and Pacinian corpuscles laminated and rapidly adapting Mammals also have neurons entwined around hair follicles so the hairs act as lever arms Slight movement of the hair tip is magnified at the hair follicle and initiates a nerve impulse The most specialized of these are the long vibrissae or whiskers on the snout of many mammals which are so sensitive that they can respond to air currents as well as to light touch because the base of the hair follicle is suspended within an expanded sinus of tissue uid that maximizes displacement of any hair movement Fig 1263 Cats rats and other nocturnal species use their vibrissae to provide information for moving about in the dark Eimer s organs are examples of highly specialized touch receptors More than 25000 Eimer s organs are present on the appendages of the nose of the starnosed mole Fig lZ6C this is fivefold as many touch receptors as are found in the human hand The overwhelming preponderance of one sensory system in this case touch often is correlated with reductions in another sensory system in this case moles have very reduced visual systems Such tradeoffs in the relative development of sensory systems are a common theme across vertebrate evolution Less is known about cutaneous mechanoreceptors of nonmammalian tetrapods Frogs snakes and some other species are extraordinarily sensitive to ground seismic vibrations and use this information to help detect the presence of predators or prey Seismic receptors have been found in the skin although the ear is the more typical route for acquiring such stimuli eg see the discussion of the ear of lissamphibians p 419 The lateral margins of the bill of ducks and other water fowl have organs such as Pacinian corpuscles that are used to detect food in muddy water Mechanoreceptors on or near the feather follicles may enable birds to detect an imminent stall and measure airspeed across wings Brown and Fedde 1993 Propriocepto rs Coordinated contraction and relaxation of locomotor and other muscles in the correct sequence and with the needed force and velocity require some sensory feedback from the muscles to centers in the spinal cord and brain that control their activities A category of mechanoreceptors known as proprioceptors L praprius 5 one s own 1 ceplus 5 taken from capere 5 to take which are located in muscles tendons and joints continuously provide this information although we are seldom aware of their activity Most proprioceptors are associated with somatic muscles so they are considered somatic receptors Tendon organs consist of groups of encapsulated collagen fibers that are entwined by sensory nerve endings Fig 1271 They detect tensions developed by the muscles and provide information on which muscles are active and the magnitude of the forces developed If forces become dangerously great then the sensory information reaching the central nervous system will initiate re exes that reduce the number of motor impulses going to the muscles Tetrapods cope with gravitational forces by continuously adjusting their posture Adjustments are made continuously in the degree and rate of muscle contractions as limb angles and the loads on the muscles change Tendon organs are more numerous in tetrapods than in nontetrapods and muscle spindles are present within the skeletal muscles of tetrapods Muscle spindles provide information by which the degree and rate of muscle contraction can be adjusted to meet the changing forces to which the muscles are subjected A muscle spindle is a small fusiform group of specialized muscle fibers inside a sheath Fig 1273 These fibers are called intrafusal fibers L 1sus 5 spindle because they lie within the sheath The surrounding normal muscle fibers are referred to as extrafusal Most of the intrafusal muscle fibers are known as nuclear bag bers because their nuclei are concentrated in the swollen equatorial region of the fibers The equatorial region lacks contractile myofibrils and is encircled by annulospiral endings of sensory neurons Other more slender intrafusal fibers known as nuclear chain bers receive branching sensory neuron ends nearer their poles Motor neurons also terminate near the polar ends of each type of intrafusal fiber As muscles stretch because of increasing loads on them the muscle spindles are passively stretched This is detected by the sensory endings on the nuclear chain fibers Sensory information returning to the spinal cord initiates nerve reflexes that increase the motor output to the extrafusal fibers in the stretched muscles The increase causes the extrafusal fibers to contract enough to compensate for their increased load If for example you stand flatfooted and bend your knees the gastrocnemius and soleus muscles on the back of the shin and the hamstring muscles on the back of the thigh are stretched If this were not compensated for by an increased contraction of these muscles you would fall During muscle contraction the polar regions of the nuclear bag fibers also are stimulated and contract If their rate of contraction matches the rate of contraction of the surrounding extrafusal fibers then tension will not develop in the nucleated noncontractile region of the nuclear bag fibers If the rate of contraction of the extrafusal fibers lags behind that of the nuclear bag fibers then the nuclear region of the nuclear bag fibers becomes stretched This is detected by the annulospiral neuron endings Sensory impulses returning to the spinal cord will initiate an increase in the rate of nerve impulses going to the extrafusal fibers until the rates of contraction of intrafusal and extrafusal fibers are again the same Lateral Line System The lateral line system is one of the most highly variable sensory systems of craniates In its basic form it consists of a series of mechanoreceptive organs in the skin organized as a series of lines It has been lost or modified in many groups and is the source for sense organs specialized to detect other modalities such as electric fields In our treatment we will discuss its basic structure and trace a few of its many evolutionary modifications Basic Organization of the Lateral Line System The lateral line system is present in living hagfishes lampreys chondrichthyans actinopterygians fishlike sarcopterygians and larval lissamphibians including paedomorphic species This somatic sensory system enables them to detect water disturbances The lateral line system generally is lost at metamorphosis in lissamphibians although several families of aquatic salam anders retain it as adults It is entirely absent in all living amniotes even those such as sea turtles or cetaceans that readapted to an aquatic mode of life The sense organs within the lateral line system are small clusters of mechanoreceptor and sustentacular cells called neuromasts Fig 1281 The individual receptor cells are termed hair cells because each bears a single long kinocilium that is followed by a cluster of 15 to 30 stereocilia of decreasing length Fig 1291 The kinocilium is a modified cilium containing the characteristic 9 l 2 pattern of microtubules The stereocilia lack microtubules and are modified microvilli The kinocilium and stereocilia project into an overlying gelatinous secretion the cupula During embryonic development the cells that will form the hair cells of the neuromasts develop from ectodermal placodes that are adjacent to the one that will give rise to the receptive cells of the inner ear Chapter 4 Gnathostom es generally have three lateral line placodes rostral to the otic placode and three caudal to it Figs 427 and 430 Some of the neuromasts lie on the skin surface39 others lie in grooves or canals still others lie in linearly arranged pits known as pit organs6 Most neuromasts are on the head Neuromasts located in the waterfilled skin canals or grooves open to the surface by pores Fig 128B The canals and grooves have a distinct pattern One canal known as the trunk canal extends along the flank from head to tail whereas several others ram ify on the head Fig 1210 Particularly noteworthy in the head of gnathostom es are the supraorbital infraorbital and preopercularmandibular canals Each canal in the trunk or head is accompanied by a nerve ramus that leads back to the brainstem Chapter 13 The patterns of the lateral line canals and their innervation across gnathostomes are remarkably conservative and useful for phylogenetic work Canal bones may develop surrounding the neuromasts of the lateral line canals and these are centers of ossification for many major bones found in the head of Osteichthyes Chapter 7 The hair cells of neuromasts are tonic mechanoreceptors that generate a constant base rate of nerve impulses bending the cupula alters the rate Neuromasts enable the animal to detect water movements in different directions because movements that bend the cupula toward the kinocilium increase the rate of nerve impulses that the cell generates whereas an opposite movement decreases the rate Efferent lateralis neurons that extend from the brain to many hair cells modulate their sensitivity and may suppress background noise caused for example by the animal s own movements The sensory neurons that carry impulses from the neurom asts to the medulla of the brain are known as afferent lateralis neurons Traditionally these neurons have been regarded as components of the facial VII vagal X and sometimes the glossopharyngeal IX cranial nerves but most neuroanatomists now believe that the lateralis neurons constitute six distinct lateralis nerves Chapter 13 The polarity of the neuromasts within a canal is not the same All of the kinocilia in one set of neuromasts may be located on the caudal edges of the hair cells those in another set may be rotated 1807 and be on the rostral edge This arrangement together with the pattern of distribution of the canals enables a fish to both detect water disturbances and determine their source Water flowing from head to tail may be the message of one set water owing from tail to head may be the message of the other set Many sorts of water disturbances can be detected currents the movements of nearby animals or of the fish itself disturbances caused when a fish approaches a rock or other stationary object and lowfrequency vibrations generated by a nearby sound source The lateral line system has aptly been defined as distant touch You can make some predictions about a gnathostome s sensory world by studying its lateral line system For instance placement of neuromasts in canals allows fish to better localize the source of an impinging pressure wave If for example all of the neuromasts were located at the body surface then they all would be deflected as the animal swims forward By placing them in canals however impinging pressure waves at right angles to the body surface can be detected If an animal has relatively large pores opening into its canals or if they lie in open grooves then it is often a relatively slow swimmer faster swimmers require greater shielding of the canal neuromasts and so have smaller pores Electroreceptors Water conducts electricity well and electroreceptors occur in many groups of aquatic craniates Most types of electroreceptors develop from placodal tissue adjacent to the tissue that forms typical lateral line mechanoreceptors Fig 4 30 and are supplied by lateralis neurons The similarities and differences between lateral line mechanoreceptors and typical ampullary electroreceptors are summarized in Table 121 Like the lateral line sense electroreception is an ancient sensory system of vertebrates Living hagfishes do not have any recognizable type of electroreceptors nor do they have any of the hindbrain nuclei associated with electroreception in other groups of craniates Also hagfishes appear unable to physiologically detect even strong electric fields In contrast lampreys are electroreceptive although their electroreceptors are confined to the epidermis and do not extend into the dermis as do the larger organs found in gnathostom es Thus we interpret electroreception as a synapomorphy of vertebrates The electroreceptors found in many living gnathostomes e g chondrichthyans basal actinopterygians coelacanths lungfishes and larval lissamphibians are called ampullary organs In chondrichthyans groups of ampullary organs often known as ampullae of Lorenzini in this group are clustered on the head adjacent to the lateral line canals Fig 121 11 and B Each ampullary organ consists of a subcutaneous tube that lies tangential to the skin s surface One end of the tube opens by a pore on the body surface and the other terminates in a slight enlargement the ampulla which contains modified hair cells Fig 121 lC Compared with typical hair cells the sensory cell of an ampullary organ has a single cilium and no microvilli eg compare Fig 1291 and B The entire tube of the ampullary organ is filled with a gelatinous mucopolysaccharide secretion so a cupula is absent The jelly has the properties of an electrical capacitor It has a low electrical resistance and readily holds and conducts current The rate of discharge of the tonic electroreceptive cells in the ampulla is altered by an electric current oriented parallel to the jellyfilled tubes The electrical resistance of the skin and tube s wall prevents electric currents from reaching the electroreceptive cells except through the jelly Impulses are sent to the brain on afferent lateralis neurons there appears not to be any efferent innervation of the sensory cells of an ampullary organ Fig 129B Until the middle of the 20th century no one suspected the electroreceptive role of ampullary organs Initially regarded as specialized mucous glands electrophysiological studies of ampullary organs conducted in the 1930s showed that they were exquisitely sensitive to different concentrations of salt water and temperature indeed the ampullae of Lorenzini of chondrichthyans are among the most sensitive known temperature receptors although we have no idea whether any chondrichthyan species uses them to detect temperature changes For a time the detection of these stimuli was regarded as their function even though it seemed doubtful that the acquisition of such information warranted so complex and elaborate a sensory network Then behavioral studies convincingly showed that chondrichthyans use ampullary organs for the passive electrolocation of prey organisms Fig 1212 A chondrichthyan can detect the weak electric currents generated inadvertently by the contraction of the cardiac and respiratory muscles of prey organisms buried in the sand even when its other senses have been blocked The known lower limit of detection is a gradient of 0001 mVcm Sophisticated neurophysiological systems allow an elasm obranch to distinguish external electric fields signals from selfgenerated electric fields noise created by their own muscles see Montgomery and Bodznick 1999 Different chondrichthyans have different arrangements of the ampullary organs For example the size and distribution of the ampullae of Lorenzini in skates correlate with differences in their feeding strategies The discovery of their electroreceptive role ruled out the old idea that ampullary organs were capable only of temperature or salinity detection Even though they are sensitive to these stimuli one cannot assume that this is the information that the animal typically uses them to gather This story shows the importance of investigating not only what a sensory receptor can detect but also what an animal does with the sensory information Many organisms including sharks can orient themselves in magnetic fields and some use this ability in navigation and migration Ampullary organs of chondrichthyans are sensitive enough to detect the minute voltage gradient induced by swimming in the earth s magnetic field and in some species the use of this sense for navigation has been demonstrated experimentally Kalmijn 1978 1988 Electroreception based on ampullary organs was lost in the ancestor of neopterygians Fig 1213 This loss eliminated not only the ampullary organs them selves but also their central connections within the brainstem Chapter 13 Such an evolutionary loss has puzzled neuroanatomists and behaviorists and no compelling adaptive explanation exists for the absence of electroreception in groups such as bowfins gars and early teleosts Electroreception was independently lost in frogs and the lineage that led to amniotes Fig 1213 This evolutionary loss is more easily understood because air does not conduct electricity Some of the most intriguing examples of convergent derivation of a sensory system are provided by the multiple re evolution of electroreception which has occurred at least twice in teleosts ie in the clade including catfishes and South American knifefishes Gymnotidae and independently in the clade including elephant snout fishes Mormyridae and some allies and once in amniotes monotreme mammals eg the platypus7 Receptive cells of teleostean electroreceptors lack kinocilia on their apical surfaces Fig 129C This together with differences in the way that these organs respond physiologically to electric fields gives us great confidence that they are not homologous to the typical ampullary electroreceptors found in chondrichthyans In the case of the platypus electro receptors are modified skin glands innervated by the trigeminal V cranial nerve Catfishes have a single type of electroreceptor that has been termed an ampullary organ because it too is shaped like an ampule or flask8 Like the electroreceptors of chondrichthyans catfish electroreceptors are sensitive to lowfrequency ie DC electric fields Other electroreceptive teleosts have similar ampullary organs as well as a second type of electroreceptor known as a tuberous organ Tuberous organs are specialized for detecting rapidly changing ie high frequency electric fields and so can be referred to as phasic electroreceptors Many species of teleosts with tuberous organs also generate highfrequency electric pulses and fields using muscles modified into electrogenic organs Chapter 10 they can then detect the pulses that they generate using their tuberous organs Among extant fishes this capability occurs in the knifefishes of South America and in the elephant snout fishes of Africa and a few related groups Studies on gymnotids and mormyrids show that they engage in active electrolocation detecting nearby objects in the turbid waters in which they live by the distortions they produce in their own electric fields They also use electric pulses in electrocommunication Electrocommunication is important in species and sex recognition in territoriality and probably in other social interactions Among many other interesting variants of ampullary electroreceptors is the rostral organ of coelacanths Fig 121 1D This large organ situated in the snout opens to the outside by three large pores on each side of the head39 it is anatomically different from typical ampullary electroreceptors and its function was unknown for many years Neuroanatomical and behavioral evidence now confirm that it is electrosensory The Ear For more than 100 years comparative anatomists have noted the many similarities between the ear and the lateral line system The receptor cells of both systems are hair cells that are stimulated when liquids or other materials move across their surface and bend their cilia The two systems develop from adjacent neurogenic placodes Chapter 4 Neurons from cranial nerve VIII9 which carry sensory information from the ear terminate in the medulla of the brain adjacent to the terminations of lateralis fibers which carry information from the lateral line organs and electroreceptors there are three lateral line nerves anterior to the entry of cranial nerve VIII and three such nerves posterior to its entry39 see Chapter 13 Because of these similarities most investigators regard the lateral line ampullary electroreceptive system and ear as components of the octavolateralis system The lateral line part of this system detects water disturbances around aquatic vertebrates and the ampullary electroreceptors detect electric fields The part of the ear containing hair cells is invaginated beneath the skin and thus is isolated from external aquatic disturbances It has instead become specialized to detect internal liquid disturbances caused by changes in the orientation and movement of the body balance and acceleration and by any external sound waves that are able to reach it All vertebrates have an inner ear embedded in the otic capsule of the skull and this is where the receptive hair cells are located Living tetrapods also have middle and external ears that are specializations for receiving airborne sound waves and transmitting them to the inner ear Inner Ear Structure The inner ear develops embryonically in all vertebrates as an invagination of the ectodermal otic placode to form an otic vesicle Fig 1214 also Chapter 4 The vesicle gradually differentiates into a series of membranous sacs and ducts that are filled with a lymphlike uid called endolymph The entire complex is known as the membranous labyrinth blue in Fig 1215 It lies within a system of parallel canals and chambers in the cartilage or bone of the otic capsule of the skull These spaces are known as the osseous labyrinth The space between the membranous labyrinth and the osseous labyrinth is crisscrossed by strands of connective tissue and filled with a liquid called perilymph green in Fig 1215 Many adult anamniotes have an endolymphatic duct that opens onto the surface of the head In other vertebrates it either is lost or forms a small deeply seated endolymphatic sac In gnathostomes each membranous labyrinth has three semicircular ducts that connect with a chamber known as the utriculus L utriculus 5 small bag These ducts are sometimes called canals but technically the term semicircular canal applies to the spaces in the osseous labyrinth in which the semicircular ducts lie In gnathostom es two of the semicircular ducts lie in the vertical plane perpendicular to each other39 the third lies in the horizontal plane at right angles to the other two A swelling termed an ampulla not homologous with the ampulla associated with the electroreceptive organs is located at one end of each duct The semicircular ducts are remarkably similar in most gnathostomes Fig 1216 In contrast lampreys lack the horizontal duct Fig 1216A and hagfishes have only a single semicircular duct although its orientation allows it to detect the same motions as a lamprey Gnathostomes exhibit greater variation in the rest of the membranous labyrinth For example cartilaginous fishes have a utriculus that is divided into two parts In all gnathostomes the utriculus connects ventrally with a larger sac called the sacculus L sacculus 5 small sac from which a caudoventral evagination of some type arises Fig 1216 In most groups of gnathostomes the caudoventral evagination of the sacculus forms a small lagena L lagena 5 flask and in some diapsids and mammals the lagena develops into a longer duct The lagena becomes greatly elongated in therians and coils to form the cochlear duct Gr kachlias 5 snail The name cochlear duct also is given to the elongate lagena of birds Several types of haircell groups are located within the membranous labyrinth A patch of sensory hair cells termed a crista L crista 5 crest occurs in the ampulla of each semicircular duct Another called the crista neglecta because it was long overlooked is found in the utriculus Fig 1215 Larger patches of hair cells termed maculae L macula 5 spot occur in the utriculus and sacculus of all vertebrates and in the lagena of many Maculae often appear as small white spots because each is overlain by small calcareous crystals termed statoconia which are secreted into a gelatinous membrane The statoconia are loosely organized in cartilaginous fishes and mixed with sand grains that enter through the endolymphatic duct Some of the mineral particles are magnetic10 Statoconia are consolidated into larger otoliths Gr 015 ear 1 lilhas 5 stone in many osteichthyans Because they are so heavily mineralized otoliths are denser than the rest of the fish Different groups of teleosts have evolved large otoliths in different chambers within the membranous labyrinth but typically either the saccular or utricular otolith is enlarged for use in sound detection Teleostean otoliths often have distinctive shapes in different species Otoliths of some species grow by the accretion of layers of calcareous crystals and the number of layers can be counted for use as an indication of the fish s age Sensory papillae are patches of hair cells and their associated sustentacular cells that occur only in the sacculus lagena or cochlear duct of tetrapods The cilia of their hair cells impinge on an overlying tectorial membrane L rectum 5 roof Movement between the cilia and the membrane activates the receptor cells Equilibrium Hair cells within the ampullae utriculus and sacculus of all vertebrates detect changes in position and movement and so provide information that helps an animal maintain its position in space or its equilibrium Additional information about position and movement com es from sight proprioceptors and in tetrapods tactile and pressure receptors in the feet The pull of gravity on the statoconia or otoliths particularly the large one in the sacculus registers static equilibrium that is the present orientation of the body in space If the animal rolls to one side or pitches forward then the changed pull of gravity on the statoconia or otoliths in the sacculus and utriculus creates shear forces on the cilia of the hair cells and alters their rate of discharge Because hair cells in the maculae of the sacculus and utriculus have different polarities they can detect displacements in different directions Stops starts and other changes in linear acceleration also affect the statoconia or otoliths because their inertia causes their movements to lag behind those of the body as a whole Angular accelerations or turning movements of the head are detected by the cristae in the semicircular ducts If for example a vertebrate turns to the left or to the right then the crista in the ampulla of the horizontal duct moves at the same rate as the body but movement of the endolymph in the narrow duct lags slightly and as a result bends the cupula overlying the crista which nearly blocks one entrance into the duct Similarly turning movements in the vertical plane will affect some combination of the vertical ducts Presumably the large diameter of the two vertical ducts in the ear of a lamprey enables them to detect some horizontal movements of the head but clearly the gnathostome condition of a dedicated horizontal duct is a better design Healing Mechanisms of Chondrichthyans and Teleosts To us hearing is the detection of airborne pressure waves but to a teleost fish and to many other aquatic gnathostom es it is the detection of water disturbances generated by sound sources under water or at the water s surface Sound waves generated by a vibrating object spread much more rapidly through a dense medium such as water than through air Sound travels at 1500 ms in water compared with 330 ms in air Sound waves have two components 1 lowfrequency particle motion or displacement waves which are somewhat analogous to the ripples produced when a pebble is dropped into the water and 2 higher frequency pressure waves which result from the alternate compression and rarefaction of molecules in the water The amplitude of the displacement waves decays very rapidly proportional to the square of the distance from the sound source regardless of the sounds frequency In contrast the amplitude of a sound pressure wave decays more slowly linearly with distance in a frequencydependent manner ie lowfrequency sounds travel much farther than do high frequency ones For example certain very lowfrequency sounds generated by instruments in New Zealand can be detected in California having crossed the entire Pacific Ocean basin Because of differences in their decay rates the displacement wave component of sound predominates close to the sound source that is in the near eld whereas the pressure wave component is more important at a distance from the sound source that is in the farfield Because hair cells are stimulated by the displacement of their stereocilia a displacement wave directly affects the hair cells that it can reach For example lateral line organs are well suited to detect and localize the source of lowfrequency water particle displacements in the nearfield Maximum sensitivity for such lateralline detection is for sounds with frequencies of 50 Hz to 150 Hz Displacement waves may also directly reach the inner ears of chondrichthyans by passing through the skin and jellyfilled parietal fossa in the chondrocranium and affecting the crista neglecta which lies in part of the utriculus Skates and galeomorph sharks can hear very well using this system Teleosts use their otoliths for detecting nearfield displacement waves When a displacement wave impinges on the body the movements of the dense otoliths lag slightly behind the movements of the rest of the body which creates a relative movement between the otolith and the hair cells on which it rests causing the hair cells to bend Such displacement of the body relative to its otoliths is a way to detect nearfield sounds Mechanisms whereby teleosts detect higher frequency farfield pressure wave components are complex Because the density of a teleost is similar to that of water sound pressure waves easily pass through and move the body at nearly the same amplitude and frequency as they move the water In this sense a teleost s body is transparent to sound For a sound pressure wave to be detected the waves must induce a movement over certain hair cells that differs from that of the rest of the body Neurophysiological evidence suggests that for many teleosts the macula in the sacculus is more sensitive to far field pressure waves than are other parts of the inner ear A potentially better mechanism is to use a gasfilled space in the body such as the swim bladder as a hydrophone see Chapter 18 for more on swim bladders Sound pressure waves passing through the body cannot compress the liquid in the tissues but they can compress the air in the swim bladder The changing pressure in the swim bladder vibrates its walls at the same frequency as the impinging sound wave Carps minnows and other ostariophysans have a particularly elegant system The swim bladder vibrations are transferred to the inner ear by paired sets of small bones the Weberian ossicles which are derived from ribs Fig 1217 These ossicles extend from the anterior end of the swim bladder to a perilymphatic sac that lies beside the sacculus The system is analogous to the tympanic membrane and auditory ossicles of mammals p 420 and Chapter 22 Ostariophysans have very low auditory thresholds ie they can detect very faint sounds and can detect some of the highest frequencies 5000 Hz of any teleosts They are most sensitive to frequencies between 200 Hz and 600 Hz Fig 1218 In contrast tunas and allies that do not have a swim bladder have far less sensitive ears Fig 1218 Many other groups of teleosts independently evolved swim bladderiear connections Considerable evidence indicates that teleosts like tetrapods can detect the direction from which a sound came Tetrapods detect direction by differences in the time and intensity of the arrival of the pressure waves at the two ears but it is unlikely that teleosts can do so because pressure waves travel so fast in water and the distance between the two inner ears is so small Therefore directional discrimination in fishes probably depends on differences in the polarity of groups of hair cells in the macula The underwater world can be a relatively silent place to a human diver whose ears are adapted to detect airborne sound waves But what do chondrichthyans or teleosts hear Many sorts of noises are detected with underwater listening instruments Waves surf and currents all generate sounds as do rapid changes in the direction or velocity of swimming animals Animals feeding on coral shellfish and other coarse material make noises Many teleosts also produce sounds at will by gnashing their teeth or rubbing spines or certain pectoral bones together Others have muscles that pluck on the swim bladder as one might pluck a bass fiddle or they drum on the body wall overlying the swim bladder with their pectoral fins Some species use sounds to call mates startle predators or warn conspecifics of danger Some of the sounds produced by teleosts are very loud A chorus of marine catfish can generate a noise of 20 decibelsiequivalent to a subway train 10 m away Clearly sound can be an important sensory modality for teleosts Hearing Systems of Tetrapods Although a teleost with a swim bladder and a swim bladderiear transmission system has no difficulty in receiving sound pressure waves this is not necessarily true for a tetrapod Lowfrequency sound waves 1000 Hz of sufficient intensity may travel through the ground as well as air and can cause a slight displacement of superficial skull bones that can be detected as sound Caecilians terrestrial salamanders some squamates and all snakes detect lowfrequency waves in this way The most important sounds for a tetrapod however are higher in frequency and so travel only as sound pressure waves in air a medium that is far less dense than water The force of an airborne sound pressure wave must be amplified considerably to enter the denser liquids of the inner ear to produce a displacement wave that can move certain hair cells relative to overlying structures Terrestrial vertebrates that detect higherfrequency sound waves have a thin tympanic membrane also called a tympanum or eardrum on or near the surface of the head The term external ear may be applied to a tympanum the term also may refer to accessory structures such as the ear pinna that help to direct sounds to the tympanum An airfilled middle ear or tympanic cavity lies on the inside of the tympanic membrane and connects to the pharynx by way of the auditory tube also known as the Eustachian tube Figs 1219 and 1220 The tympanic cavity and auditory tube equalize the air pressure on the two sides of the tympanic membrane which enables the membrane to respond quickly to highfrequency sounds The tympanic cavity and auditory tube of an amniote develop from the first embryonic pharyngeal pouch so they are homologous to the first gill pouch or spiracle of a fish We are uncertain whether this homology strictly applies to the middle ear cavity and auditory tube of lissamphibians which show certain peculiarities in their development 1 1 The conversion of a sound pressure wave in air to a displacement wave in the perilymph and endolymph of the inner ear is made by the response of the tympanic membrane or certain skull bones when a membrane is absent Three other structures are essential Figs 1219 and 1220 1 At least one auditory ossicle known as the columella in lissamphibians and sauropsids or stapes in mammals must be present the lateral end of which connects either to a tympanic membrane or to superficial skull bones on which airborne sound waves impinge The medial end of the columella or stapes bears a foot plate that fits into an opening known as the oval window on the lateral surface of the otic capsule The columella or stapes is homologous to the hyomandibular of fishes Chapter 7 The large size of the tympanic membrane relative to the size of the foot plate forms a pressureamplification mechanism All the energy impinging on the large tympanum is concentrated on the small foot plate The resulting increase in energy per unit of area on the foot plate enables the highfrequency aerial vibrations to overcome the inertia or impedance of the liquid in the perilymphatic duct and set up displacement waves in it The internal and middle ears often are described as an impedancematching device 2 At least one specialized perilymphatic duct must be present The perilymphatic duct receives displacement waves from the foot plate and carries them past a receptive part of the membranous labyrinth to some point where they can be dissipated The perilymphatic duct may be expanded to form a perilymphatic cistern adjacent to the oval window The dissipation point is either inside the cranial cavity eg Fig 12193 or at the round window that opens into the middle ear cavity eg 12l9C 3 Finally within the membranous labyrinth at least one sensory area must be specialized to receive the displacement waves from the perilymphatic duct Tetrapods have one or more unique groups of hair cells known as papillae which are specialized to receive these waves A papilla consists of hair cells overlain by a tectorial membrane rather than by otoliths Many differences in the location of the papilla or papillae exist among tetrapods Different groups of tetrapods detect airborne sound waves in different ways utilizing some structures that are homologous and some that are not This suggests considerable independent evolution of auditory mechanisms in tetrapods Such a pattern of multiple evolutionary origins of auditory specialization parallels that already noted for teleost fishes In particular a tympanic membrane was not present in the earliest tetrapods and perhaps its absence in caecilians and salamanders is a retention of this plesiomorphic condition An ear utilizing a tympanic membrane evolved independently at least three times in tetrapods l in the lineage that leads to anurans frogs 2 in the line of evolution to turtles and diapsids and 3 in the late synapsid lineage that gave rise to mammals The Ear of Sauropsids We begin with the ear of sauropsids12 in which the tympanic membrane usually is located at the bottom of a recess the external acoustic meatus Fig 12l9A The tympanum is described as postquadrate in position because it lies just caudal to the quadrate bone which usually partly encases the tympanum and middle ear cavity The columella crosses the tympanic cavity and transfers displacement waves from the tympanum through the oval window to a perilymphatic cistern Fig 12 193 A perilymphatic duct extends from the cistern across the lagena which contains the receptive basilar papilla to the perilymphatic sac where the waves are dissipated This sac may lie beside the round window which opens back into the tympanic cavity but it often lies in the cranial cavity This ear is very sensitive and can respond to highfrequency sounds Some squamates can detect sound waves with a frequency as high as 10 kHz The ear of birds is similar The main differences are that the lagena forms an elongated cochlear duct and the basilar papilla forms an equally long organ of Corti13Fig 12l9C Songbirds can detect frequencies as high as 21 kHz Many squam ates including all snakes lack a tympanum an absence that is regarded as a secondary condition Instead the columella connects with the quadrate bone Fig 12l9D Such animals detect chiefly ground vibrations but their ears also are sensitive to lowfrequency airborne vibrations It is probable that the tympanic membrane was secondarily lost in these species as an adaptation to a burrowing mode of life Those squamates that lack it are for the most part burrowers all amphisbaenians live beneath ground and we believe that snakes passed through a burrowing phase early in their evolution most species now live above ground but basal snakes still burrow The Ear of Lissamphibians Frogs have a large tympanum located high up on the head surface dorsal to the quadrate bone14 Fig lZZOA The columella of a frog connects to the tympanum and continues across the tympanic cavity to the oval window in the otic capsule This is referred to as a frog s tympanic ear system to distinguish it from a second auditory system the opercularis system that also is present in lissamphibians Lissamphibians have an additional auditory ossicle known as the operculum that also lies in the oval window and fits into a notch on the caudal surface of the footplate of the columella The operculum develops embryonically from a part of the wall of the otic capsule15 The opercularis muscle extends from the operculum to the suprascapular element of the pectoral girdle thereby coupling the inner ear to the girdle leg and ground The opercularis muscle is homologous to the levator scapulae muscle Chapter 10 The perilymphatic cistern lies just inside the oval window and continues past the sacculus to a perilymphatic sac that extends into the cranial cavity Two sensory papillae are present in the ear of frogs a basilar papilla near the entrance to the lagena and a more dorsally located amphibian papilla which is uniquely found in lissamphibians Fig 1216C Larval salamanders have a columella that connects to superficial skull bones Fig 12203 but this is either lost or reduced later in development so that adult salamanders have only the opercular system Fig 1220C Lissamphibians are secretive creatures that are sensitive to lowfrequency seismic vibrations that can alert them to potential danger Early in the 20th century Kingsbury and Reed 1909 proposed that the opercularis system detected ground vibrations of this type Hetherington Jaslow and Lombard 1986 corroborated this hypothesis and found that the opercularis is a tonic muscle that is tense and rigid exactly what would be expected if it was part of a vibrationdetecting system Lowfrequency vibrations of this type are detected by the amphibian papilla The tympanic ear system of frogs is adapted to receive much higher sound frequencies such as their mating calls These are detected by the basilar papilla Salamanders do not have mating calls and not surprisingly they lack the tympanic system including the basilar papilla Evolution of the Mammalian Ear Mammals have a third type of tympanic ear An external flap the auricle or pinna helps funnel sound waves down the external acoustic meatus to the tympanic membrane Fig 1221 The human auricle is neither very large nor important but the auricle of many mammals is large and can be moved and directed toward a sound source A large auricle amplifies sound waves because the waves it gathers are concentrated on the relatively smaller tympanic membrane Three auditory ossicles the malleus incus and stapes extend from the tympanic membrane across the middle ear cavity Fig lZZZA The oval window of a mammal is technically known as the fenestra vestibuli The ossicles derive their names from their shapes L malleus 5 hammer L incus 5 anvil L stapes 5 stirrup As we have seen Chapter 7 the malleus evolved from the quadrate bone39 the incus from the articular bone and the stapes from the hyomandibular The quadrate and articular bones bear the jaw joint in nonmammalian vertebrates As in other vertebrates with tympanic ears amplification of a sound wave derives from the large size of the tympanic membrane relative to the foot plate of the stapes The three auditory ossicles of mammals form a lever system that further increases this amplification about one and a half times but as in any lever system the increase in force at one end of the system is accompanied by a reduction in the extent of movement at that end In humans the total force on the foot plate of the stapes is 22 times that on the tympanic membrane but the extent of movement of the foot plate is only about one third that of the membrane Two small muscles the tensor tympani and stapedius attach to the malleus and stapes respectively Because the malleus derives from the mandibular arch the tensor tympani is a mandibular arch muscle and is innervated by the trigem inal V nerve The stapes is a hyoid arch derivative and the stapedius muscle is innervated by the facial VII nerve Tension in these muscles dampens oscillations of the ossicles and so protects delicate inner ear structures from excessive movements caused by loud noises including the sounds that the animal itself may make such as the ultrasonic sounds of bats and cetaceans see below which are emitted at very high energy levels The hypothesis that the mammalian ear with its three ossicles evolved from a tympanic ear similar to that seen in living sauropsids in which there is only a single ossicle presents some serious problems How could the articular and quadrate when they became redundant as jaw joint bones move into the middle ear without disrupting its function What would be the advantage of adding them to an effective ear These problems vanish if as we now believe mammals evolved from ancestral amniotes that did not have tympanic ears e g animals similar to tcaptorhinids and early synapsids such as tsphenacodonts These animals had a large columella that was connected to the quadrate In these forms there was no modification of the quadrate as there is in extant sauropsids that would accommodate a tympanic membrane and middle ear behind it Presumably tcaptorhinids and early synapsids detected ground vibrations and lowfrequency airborne vibrations through the skull including the lower jaw Vibrations detected by the lower jaw would have been transmitted via the articular quadrate and columella to the inner ear As the postdentary bones of the jaw and the columella became smaller and lighter Chapter 7 they became more efficient in transmitting sound Such improved sound transmission may have been another factor in addition to feeding mechanics in the evolution of changes in jaw mechanisms More derived synapsids had an unusual ange the re ected lamina that extended ventrally and caudally from the angular bone Figs 729 and 730 Many investigators believe that the re ected lamina of the angular held a socalled mandibular tympanic membrane that lay adjacent to an airfilled space Such a space would have further increased the efficiency of the articular quadrate and columella in sound transmission With the final shift of the jaw joint to the dentary and squamosal bone in early mammals the articular quadrate and columella now modified into the tiny stirruplike stapes became dedicated auditory ossicles If we are correct in thinking that early mammals such as tMarganucadan occupied an insectivorous nocturnal niche then we may hypothesize that the ability to detect high frequency sounds may have been advantageous So rather than trying awkwardly to fit the articular and quadrate into an already functional ear we now believe that these bones together with the colum ella were soundtransmitting bones throughout the early history of tetrapods and especially in the line of evolution to mammals Changes in jaw mechanics made it possible for these bones to become dedicated and highly efficient auditory ossicles The lagena and perilymphatic duct found in ancestral terrestrial vertebrates are elongated in mammals to form the snail like cochlea16 Figs 1216F and 1222A The cochlea spirals around a core of bone the modiolus that contains the cochlear branch of cranial nerve VIII which is called the vestibulocochlear nerve in mammals Fig 1222D The cochlea becomes progressively narrow as it approaches its apex Its spiral ranges from a onequarter turn in the platypus to four turns in the guinea pig The human cochlea makes three and a half turns The presence in early fossil mammals of spaces in the otic capsule for an elongated and partly coiled cochlea is evidence that these mammals had a keen sense of hearing The lagena itself forms the cochlear duct that contains the elongated basilar papilla known as the organ of Corti Fig 12223 and C The hair cells of the organ of Corti rest on the basilar membrane and their cilia impinge on an overlying tectorial membrane Displacement waves are received from the stapes at the fenestra vestibuli by a part of the perilymphatic duct called the scala vestibuli This duct passes along one side of the cochlear duct and returns on the other as the scala tympani The scala vestibuli and scala tympani connect at the apex of the modiolus by a small opening known as the helicotrema Displacement waves are released through the scala tympani back into the tympanic cavity at the round window or fenestra cochleae When displacement waves cross the cochlear duct from the scala vestibuli to the scala tympani they cause slight movements of the basilar membrane Shear forces develop between the hair cells and the tectorial membrane activating the hair cells which in turn initiate nerve impulses Because the dimensions and other properties of the cochlea and basilar membrane change from base to apex traveling waves of different frequencies cause a maximum displacement of the membrane at different levels High frequencies are detected near the base of the cochlea39 low ones register near its apex Most mammals can detect frequencies as high as 20 kHz Bats particularly microchiropterans have evolved a very sensitive auditory system that enables them to avoid obstacles in the dark and to find their insect prey by sending out highfrequency sounds and listening to the echoes Sounds with a frequency greater than 20 kHz are referred to as ultrasonic because they are higher than most mammals can detect A large ossified larynx allows a high tension to be developed on the vocal cords and as a result sounds with frequencies as high as 150 kHz can be generated The ultrasonic sounds are emitted through the mouth in some species of bats and through the nose in others Because these high frequencies have very short wavelengths they have a very high resolution and such bats can discriminate between objects that are very close together The ultrasonic sounds are emitted as pulses lasting 1 ms to 4 ms Pulses can be repeated up to 100 times per second as a bat hones in on an insect Frequencies drop about an octave during the course of each pulse Different species of bats listen to different aspects of the echoes 1 time lag in echo return 2 decrease in loudness between the emitted sound and its echo and 3 differences in frequency between the emitted sound and its echo which are sensed as a beat note Considerable independent evolution of these systems has occurred among bats Cetaceans have evolved an underwater sonar system that also is based on emitting highfrequency sounds and listening to the re ected echoes Considerable modification of the ear originally sensitive to airborne sounds has occurred so that underwater sounds can be detected Many cetaceans also have evolved communication systems based on lowfrequency songs about 20 Hz that can travel hundreds and perhaps thousands of kilometers Photoreceptors The ability to detect changes in light is important for nearly all metazoans because their periods of feeding and reproduction and many other aspects of their physiology and behavior are closely attuned to the diurnal cycle and to seasonal changes in day length The additional ability to detect the source of light can provide information on the approach of predators location of shelter and so forth For those animals with groups of photoreceptive cells numerous enough to discriminate between different light intensities and different wavelengths and a neuronal circuitry capable of processing these data light can provide much information about the world The informational content of a visual imageiits location size shape and movementican be much greater than that provided by most other senses To receive light an animal must have photoreceptive cells containing a visual pigment that absorbs quanta of light energy which initiates chemical changes that generate nerve impulses The light energy most valuable to vertebrates falls between wavelengths of 380 nm violet and 760 nm red Shorter wavelengths extending into the ultraviolet quickly are absorbed by water and so are of no value to aquatic animals Light with such short wavelengths also contains so much energy per quantum that it is potentially destructive to tissues in terrestrial vertebrates The integum ent protects deeper tissues from this ultraviolet radiation In contrast infrared and longer wavelengths contain too little energy to be biologically useful in most cases although some vertebrates have special receptors that detect infrared radiation as heat see section on infrared receptors known as thermoreceptors p 433 The body surface of most metazoans including many vertebrates can detect changes in light although specific light sensitive cells have not always been identified Zimmerman and Heatwolfe 1990 Imageforming eyes are limited to animals that move about a great deal in wellilluminated environments many arthropods cephalopods and all but a few vertebrates Median Eyes For many vertebrates the detection of light and the physiological adjustments to changes in light levels and day length are mediated by photoreceptors different from those that form images In addition to imageform ing lateral eyes anamniotes and many diapsids have one or two lightreceptive median eyes on top of the head These develop as does the retina of image forming eyes as embryonic outgrowths from the diencephalic region of the brain An adult lamprey has a nonpigmented spot of skin on the top of its head beneath which lies a pineal eye Fig 1223A A second organ known as the parietal eye lies deep to the pineal eye Fig 1223A A slight rightileft asymmetry exists in the position of these eyes Each is a hollow sphere of cells The deep cells in both spheres are photoreceptive and partly shielded by pigment Sensory neurons extend from them to the brain Experiments on ammocoete larvae of the lamprey show that the median eye complex generates a low level of neuronal activity in dim light that is correlated with the larva s nocturnal activity Strong light inhibits neuronal activity and the larva rests during the day Beyond this the median eye complex of lampreys is a neuroendocrine transducer that translates light signals into chemical messages In the absence of light the median eye complex produces an enzyme that converts the neurotransmitter serotonin into a hormone melatonin The melatonin is released into the circulation and causes the pigment in the melanophores of the skin to concentrate and thus the animal blanches in the dark Light inhibits the formation or activity of this enzyme pigment becomes dispersed and the animal is dark during the day Experiments also show that the median eye complex is essential for metamorphosis and influences the development of sexual maturity in lampreys All of this indicates that the median eye complex has a role in the daily and seasonal rhythms of lampreys but the nature of its involvement is not well understood Although not universally present the median eye complex is an ancient and widespread feature of vertebrates A foram en for it occurs in the skull of many early fossil craniates such as Tosteostracans Tplacoderms early cartilaginous and bony fishes as well as early tetrapods Extant species do not always have a foramen for it but a reduced pineal organ called the epiphysis is present in chondrichthyans and most actinopterygians Tadpoles and frogs have a small frontal organ which represents the parietal eye Fig 12233 Sphenadan and many squamates have a welldeveloped parietal eye complete with cornealike and lenslike structures and a reduced pineal organ beneath the skull roof Fig 1223C The parietal eye monitors the level of solar radiation and affects the anim al s orientation to the sun and its movements into the sun or shade The complex is represented in birds and mammals by an endocrine pineal gland the activities of which also are affected by light even though it is located deeply below the skull roof Fig 1223D and Chapter 15 The Structure and Function of Im ageF0 rming Eyes Except for a few species that live in dark habitatsisome deepsea fishes and many cavedwelling or burrowing vertebrates the eyes of which have been secondarily reducediall vertebrates have a pair of imageforming eyes The eyes are essentially little biological cameras They usually are located on the side of the head in such a position that little overlap exists in the left and right visual fields The eyes are directed more rostrally in some birds and many mammals so that the two visual fields overlap to a greater extent A high degree of overlap of the visual fields provides depth perception or stereoscopic vision in many mammals Many important structures are found in the orbit around each eyeball Extrinsic ocular muscles Fig 101 I attach to the eyeball and control its movements Eyes must be directed at objects in the visual field despite movements of the body and head and the movements of the two eyeballs usually are synchronized very precisely Tear glands and movable eyelids moisten and protect the surface of the eyes in tetrapods p 431 Although the eye varies greatly in adaptive details among vertebrates its basic structure is the same in all The hum an eye is representative of the design typical for a tetrapod Figs 1224 to 1227 lts wall consists of three layers of tissue an outer supportive brous tunic a middle nutritive vascular tunic and an inner retina containing the photoreceptive cells Part of the fibrous tunic is modified as a cornea which allows light to enter and which in tetrapods plays a significant role in bending the light to focus on the retina Parts of the vascular tunic and retina are modified to form the iris which controls the amount of light entering the eye and the ciliary body which supports and focuses the lens A watery aqueous humor fills the spaces in the eye in front of the lens and a more gelatinous vitreous body L vitreus 5 glassy lies behind the lens As light passes through the different parts of the eye it is bent or refracted toward the optic axis and casts an inverted image on the retina The Fibrous Tunic The fibrous tunic is a dense connective tissue that forms the essential supportive framework for the eyeball Most of it is opaque and white and is known as the sclera Gr skleras 5 hard This is the white of our eyes The fibrous tunic also forms the cornea L cameus 5 horny at the front of the eye The cornea is avascular and otherwise modified to facilitate the passage of light A delicate epithelial layer known as the conjunctiva covers the surface of the cornea turns onto the inner surface of the eyelids if they are present and is continuous with the surface layers of the skin A ring of cartilage or sclerotic bones develop in the sclera of many vertebrates Usually the sclerotic bones are located at the level of the lens where they support and strengthen the point of origin of lens muscles They also help maintain eyeball shape especially in some birds and other species that have nonspherical eyeballs Vascular Tunic Choroid Iris and Ciliar39y Body The next layer the vascular tunic is richly supplied with blood vessels and also contains some pigment This layer called the choroid Gr cha aeides 5 like a membrane in the posterior part of the eyeball helps nourish the underlying retina Choroid folds sometimes extend into the vitreous body They form the falciform process in some teleosts the papillary cone in some squamates and the pecten in birds Fig 1228A C and D The pecten is sometimes elaborate and may contain as many as 30 folds The function of these choroid folds is not entirely clear but if the pecten is destroyed then the oxygen content within the eye decreases greatly Some investigators also postulate that by casting a shadow on the retina these choroid processes help the animal detect the movement of an image across the retina Pigment in the choroid and in the adjacent pigmented layer of the retina prevents a scattering of light and a blurring of the image It is advantageous that as much light as possible reaches the photoreceptors of the retina in vertebrates that are active in dim light such as many chondrichthyans actinopterygians crocodilians and mammals Many of these animals have a tapetum lucidum L Iapele 5 carpet I lucidus 5 shining behind part of the retina39 it reflects light that has passed through the photoreceptors back onto them The photoreceptor cells thus are stimulated adequately but the tradeoff is some blurring of the image The tapetum may be located in the choroid or in the adjacent part of the retina The re ective layer can be composed of specially arranged collagen fibers extracellular plates of guanine or intracellular purine crystals The eyeshine of nocturnal animals caught in a ashlight or headlights is light that has been reflected by the tapetum The vascular tunic and accompanying nonnervous retinal tissue continue beside the lens and turn in front of it to form the iris Gr ms 5 rainbow Muscle fibers within the iris regulate the size of its opening called the pupil and hence the amount of light passing through the lens Fig 1224 These iris muscles of retinal origin come from ectoderrn and usually are smooth muscle fibers Both circularly arranged sphincter and radially arranged dilator muscle fibers are present in the iris of most vertebrates The diameter of the pupil is under autonomic control meaning that it opens and closes in response to signals from the sympathetic and parasympathetic neurons that innervate it Chapter 13 The pupil usually is a round opening but its shape is slitlike in many vertebrates such as cats and gekkonids which are active under a wide range of ambient light levels The halves of the iris on either side of the slit can be drawn far apart like curtains in dim light and almost completely closed in bright light to protect the very sensitive retina The bunching up of contracting tissues around a circular pupil prevents it from being closed as completely The vascular tunic and associated nonnervous retinal tissue adjacent to the lens form the ciliary body Delicate zonule bers extend from it to the lens which they help hold in place Fig l225 Smooth muscle fibers of retinal origin in the ciliary body focus the lens in different ways in different groups of vertebrates Ciliary processes of the ciliary body also secrete the lymphlike aqueous humor into the eye s posterior chamber the space between the lens and the iris Fig l225 From here the aqueous humor flows into the anterior chamber located between the iris and the cornea Fig l225 blue arrow It finally drains into the bloodstream through the venous sinus of the sclera which encircles the eye at the junction of the iris and cornea The aqueous humor nourishes the avascular cornea and lens and creates intraocular pressure that helps maintain the shape of the eye The Retina The retina is the third tissue layer of the eyeball Its most peripheral portion and its pigment layer become associated with the choroid ciliary body and iris as we have seen Its photoreceptive layer and nervous portion are limited to the posterior part of the eyeball and consist of multiple layers of cells Fig l226A Because of the way the eye evolved and develops embryonically p 429 light must pass through all of the neuron layers of the retina and through the bases of the rods and cones to reach the photoreceptive layer The rod and cone cells lie deep in the retina next to the pigment layer In many nonmammalian vertebrates processes of the pigment cells extend around the receptive regions of the rod and cone cells Pigment migrates into the processes during bright illumination thereby partly shielding the cells and withdraws when light levels fall Four neuronal layers lie between the rod and cone cells and the vitreous body These neural layers are an outer plexiform layer composed of horizontal cells a bipolar cell layer an inner plexiform layer formed by amacrine cells and a ganglion cell layer next to the vitreous body Axons of the ganglion cells course along the surface of the retina and turn inward at the optic disk to form cranial nerve H the optic nerve Fig 1224 Because no photoreceptors are present in the optic disk this is a blind spot The outer segment of a photoreceptive cell is considered to be a modified cilium because it is connected to the rest of the cell by a narrow ciliumlike stalk Fig l226B The stalk contains the characteristic nine peripheral microtubules but lacks the central two Membranes within the outer segments of the rods and cones contain photoreceptive pigments that absorb light energy and convert it into chemical energy This in turn changes the cell s membrane potential and affects the amount of neurotransmitter released by the cell Chapter 13 Photoreceptive pigments in vertebrate eyes consist of a protein known as an opsin which is combined with an aldehyde of vitamin A1 or A2 called retinene The proteins vary in different pigments and determine the spectrum of light energy that is absorbed The pigment in the rods known as rhodopsin or porphyropsin in some species or in some life stages of some species that metamorphose from aquatic to terrestrial environments such as certain lissamphibians absorbs light over a wide spectral range but the range varies with the species Cones contain pigments known as iodopsins with more restricted bands of spectral absorption Multiple pigments sometimes in one cell but more often in different cells are a prerequisite for color vision Mammals with color vision have three types of cones each having an absorption maximum in a different part of the spectrum 450 nm blue 525 nm green and 550 nm red Retinal photopigments that are sensitive to ultraviolet light as well as to color have been found in many vertebrates especially teleosts and birds Studies indicate that many of these animals can detect ultraviolet light but the adaptive significance of this is not clear Jacobs 1992 Rods are insensitive to different colors but they are very sensitive to light and have a very high degree of intraretinal convergence ie a great many rods synapse with a few bipolar cells and these synapse with still fewer ganglion cells The human retina contains approximately 120 million rods and 5 million cones but there are only about 1 million axons of ganglion cells that form the optic nerve39 therefore a small amount of light falling on many rods in the same convergent pathway can summate via bipolar cells to generate nerve impulses in the ganglion cells The tradeoff however is a decrease in resolution or visual acuity because a distinction cannot be made between spots of light falling on the same convergent pathway Rods can function in dim light but they cannot distinguish colors and rod vision is slightly blurred Cones distinguish colors but require brighter illumination They have far less convergence and so form much sharper images The eyes of hum ans and many other vertebrates contain both rods and cones but these receptors are not uniformly distributed A small central area of the retina has a high concentration of cells with little convergence and the fovea within it contains only cones This is the region of highest visual acuity and we adjust our eyes so that images fall here when we wish to discriminate fine points of light The retina is relatively thin in the fovea so its photoreceptors lie in a little pit The pit may itself act as a diverging lens and further enhance visual acuity The number of cones decreases rapidly from the fovea toward the periphery of the retina whereas the number of rods increases to a maximum about 20 from the fovea Many additional types of interconnections occur within the retina The retinal regions from which ganglion cells receive signals partly overlap Horizontal connections among rods cones and bipolar neurons are made by the horizontal cells in the outer plexiform layer Horizontal interconnections among bipolar and ganglion cells are made by the am acrine cells of the inner plexiform layer Some of these interconnections inhibit and others facilitate the transmission of impulses The significance of these arrangements is not entirely clear but some sharpen image boundaries and facilitate the detection of motion Still it is clear that much signal processing occurs in the retinainot unexpectedly because the retina is a part of the brain The Origin and Development of the Eye How did an organ as complex as the eye evolve Why does light pass through so many cell layers before reaching the photoreceptors Both phylogenetic and developmental clues can be found For example an amphioxus has ciliated photoreceptive cells in the lining layer of the lumen known as the ependymal layer of its central nervous system Most lie on the floor or lateral walls of the lumen and they are particularly numerous anteriorly Although shielded by a pigment spot from light stimuli coming from beneath the animal they can be activated by light from above because light easily passes through the thin integument and body wall These photoreceptive cells probably are homologous to the vertebrate rods and cones because the rods and cones also develop embryonically from ciliated ependymal epithelial cells that lie in the lining of the neural tube As the ancestors of vertebrates became larger and more active animals we may hypothesize that it was advantageous to concentrate photoreceptive cells near the anterior end of the body in the lumen of part of the evolving brain An evagination of this region would bring these cells closer to the body surface The advantage of having the photoreceptive part of the brain nearer the body surface would be enhanced were adjacent tissues modified to transmit light The cornea and lens may have evolved in this way This scenario is hypothetical but an essentially similar sequence of events occurs during the embryonic development of the vertebrate eye also see Chapter 4 The eye initially develops as a single median evagination17 of the diencephalon that soon bifurcates to form the paired optic vesicles Fig 1227 As each optic vesicle grows toward the body surface its proximal part narrows as the optic stalk and its distal part invaginates to form a twolayered optic cup The choroid ssure lies on the ventral surface of the stalk and carries blood vessels for the eye The outer layer of the optic cup becomes the pigment layer of the retina whereas the inner layer differentiates into the photoreceptive cells and neuronal layers of the retina The outer photoreceptive segments of the rod and cone cells develop from cilia of the ependymal epithelium lining the optic cup Because of the way the optic cup develops these cilia are directed toward the lumen After the lumen has narrowed later in development the receptive segments of the rods and cones lie next to the pigment layer of the retina and light must pass through the nervous layers of the retina to reach them The optic cup induces the overlying surface ectoderm first to thicken as a lens placode and then to invaginate and form a lens vesicle that differentiates into the lens Adjacent mesenchyme encapsulates the lens and optic cup to form the fibrous and vascular tunics Tissue from the ectodermal optic cup contributes to the iris and ciliary body and forms their muscles Embryonic blood vessels that cross the vitreous body to supply the developing lens atrophy after birth otherwise they would cast shadows on the retina Evolutionary Adaptations of the Eye Eyes and their neuronal projections offer one of the best anatomical predictors of vertebrate behavior and function so it is important to consider ways in which the eyes have become modified in different groups The Eyes of Lampreys Chondrichthyans and Actinopterygians Lampreys chondrichthyans and actinopterygians live in aquatic environments and water continuously bathes and cleanses the corneal surface so that tear glands are unnecessary and never evolved Most species lack movable eyelids but a few have stationary skin folds above and below the eye In some chondrichthyans a nictitating membrane is present in the medial corner of each eye see Fig 1230A It closes to protect the eye during close contact with prey Many species of teleosts particularly those that swim at high speeds such as mackerels Scombridae have fared the eyes into the surface of the head using clear adipose eyelids Fig 12303 Adipose eyelids help to maintain streamlining of the head by limiting the drag that would be induced were the eye to project out from the heads surface Light levels change more slowly in most aquatic environments than on land and the pupillary response of lampreys chondrichthyans and actinopterygians is correspondingly slower than that of tetrapods Dilator fibers are absent in the iris of many species so that the pupil slowly expands when the sphincter muscles relax Because the refractive index of water is close to that of the cornea light waves pass through the cornea of a lamprey chondrichthyan or actinopterygian without being substantially bent or refracted The lens therefore is the primary refractive structure in the eye and it must be thickinearly sphericalito provide adequate refraction Fig 1228A The spherical lens is composed of modified layers of epithelial cells Successive layers have different curvatures and slightly different optical properties so that light is gradually refracted toward the optic axis as it passes through them This avoids the image distortion due to spherical aberration that would occur were the lens a homogeneous sphere Differences in the shapes of the lens of a teleost and a mammal and their relationship to vision under water are shown in Figure 1229A7D A teleost s eye cannot focus properly in air because of the additional refraction that occurs when light passes from the air through the cornea At the opposite extreme a terrestrial mammal s eye cannot focus properly under water because refraction by the cornea is decreased which explains why humans need the air space created by a diving mask in front of their eyes to enable them to focus on objects under water Foureyed fishes in the genus Anableps provide a particularly clear example of the differences between an eye designed to work in water and an eye designed to work in air Fig 1229E and F The eye has two pupilsione directed above the water s surface and the other below Light passing from the air through the dorsal part of the cornea is refracted and passes through the thin axis of the lens to focus on the ventral part of the retina Light passes from the water through the ventral part of the cornea is refracted by the thicker part of the lens and is focused on the dorsal part of the retina Thus a single lens with optical axes of two different lengths is able to focus light from both air and water Lampreys chondrichthyans and actinopterygians tend to be nearsighted because the lens is close to the cornea and far from the retina To focus sharply on a distant object muscles move the lens closer to the retina A lamprey accommodates to 5 focuses on a more distant object by contracting a corneal muscle that pulls the cornea inward and pushes the lens back Lenstoretina distance in an aquatic animal is analogous to lenstofilm distance in a camera To focus on a near object the lenstofilm distance is increased by moving the lens away from the film to focus on a distant object this distance is decreased Appropriately for a large predator the eyes of a shark at rest are focused on somewhat more distant objects To see a nearer object an ectodermal protractor lentis muscle pulls the lens away from the retina The eye of an actinopterygian has a small retractor lentis muscle Fig 1228A of ectodermal origin that attaches to the lens and pulls it toward the retina In all three of these cases intraocular pressures restore the lens to its resting position when the focusing muscle relaxes Light intensity is low in many bodies of water and long wavelengths of light especially reds and oranges are readily absorbed Correlated with this the retina of many chondrichthyans and actinopterygians consists prim arily of rods The maximum sensitivity for pigments in the photoreceptive cells of teleosts living in marine coastal and fresh water is in the greenyellow range corresponding to the wavelengths of the maximum available light Only blue light penetrates far into the water and species living in deep oceanic waters have a photoreceptive pigment that absorbs maximally in the blue part of the spectrum Only those species living in brightly illuminated habitats such as coral reefs or clear freshwater lakes have many cones As would be expected many chondrichthyans and actinopterygians have a tapetum lucidum that reflects light back onto the retina The Eye of Terrestrial Vertebrates Because they are not constantly bathed in water the eyes of terrestrial vertebrates must be protected and kept moist in other ways A tetrapod s eye usually has one or more eyelids that can move across its surface and protect and cleanse it The eye of lissamphibians has a stationary upper eyelid but a movable and transparent lower one Fig 12283 Lissamphibians also can retract the eyeball deeper into the orbit using the retractor bulbi muscle so that the eyelids completely close over it In amniotes both upper and lower lids are movable and a third transparent eyelid the nictitating membrane L niclare 5 to wink is usually present 18 The nictitating membrane normally is retracted into the median corner where upper and lower lids come together but it can be flicked across the surface of the cornea In humans it is reduced to a vestigial semilunar fold Eyelashes are associated with the eyelids of mammals Tetrapods also have evolved lacrimal harderian or other tear glands the secretions of which flow across the cornea or are spread across it by the movement of the eyelids Fig 1230 The tears of mammals drain into a lacrimal duct that opens into the nasal cavity Modified sebaceous glands known as tarsal glands open on the edges of the eyelids Fig 1230C their waxy secretions help prevent the tears from owing onto the face Because its index of refraction is much greater than that of air the cornea of a terrestrial vertebrate s eye refracts incoming light and plays an essential role in focusing light on the retina Because of the cornea s role in refraction a tetrapod s lens performs less refraction than does the lens of a teleost eye and it is both thinner along the optic axis and less curved eg Figs 1229A and C For example in lissamphibians the lens changes during metamorphosis from a spherical shape in the aquatic larva to a more oval shape in the adult Fig 1228B The lens is even thinner in amniotes Fig 1228C and D Distant vision is important for most terrestrial vertebrates and the lens is positioned relatively close to the retina so that distant objects are in focus when the eye is at rest Different groups of tetrapods have different methods of accommodation Lissamphibians accommodate for a close object by contracting the protractor lentis muscle Fig 1228B which pulls the lens away from the retina and toward the cornea In contrast amniotes have elastic lenses and accommodate for near objects by changing lens shape39 changing lens shape is analogous to changing lenses on a camera Except in snakes the lens of diapsids is encircled by an annular pad that lies adjacent to the ciliary body Fig 1228C During accommodation for close objects a sphincterlike muscle within the ciliary body exerts a force on the annular pad causing the lens to bulge its refractive power to increase and the image to be brought into focus We think that the eyes of snakes partially degenerated during a period when their ancestors lived as burrowing animals and then reevolved as snakes readapted to live on the ground surface Unlike other squam ates snakes lack ciliary muscles and accommodate for distant objects by the contraction of iris muscles that push the lens deeper into the eyeball Flying birds have a keen sense of sight and can quickly adjust to changes in light levels and distance A bird s eye is extraordinarily large and is strengthened by a ring of sclerotic bones also known as scleral ossicles Fig 1229D The eyes of some hawks and owls are larger in absolute size than ours despite their relatively much smaller body size A bird s iris muscles are striated rather than smooth and respond rapidly to changes in levels of light 19 Birds retain the annular pad mechanism for accommodation but their ciliary muscles also act in other ways One set of muscles pulls the lens forward into a narrowing ring of sclerotic bones so that the lens bulges another set pulls on the cornea to slightly change its curvature The sclerotic bones provide a firm point of origin for these muscles In a mammalian eye at rest intraocular pressure tends to push the wall of the eyeball peripherally and this force is transferred to the elastic lens by the ciliary body and zonule fibers Fig 1224 The lens is under tension and somewhat attened so that distant objects are in focus on the retina When tension is released the lens bulges slightly and nearer objects come into focus The lens is restored to its resting shape by the relaxation of ciliary muscles and the action of intraocular pressure Because levels of illumination can be much higher on land than in water terrestrial vertebrates frequently have many cones and correspondingly high visual acuity and many tetrapods have color vision Most species of lissamphibians which are secretive and shadedwelling creatures have few cones in their retinas but some have color vision Cones are abundant in the retinas of squamates and birds and most species have high visual acuity and welldeveloped color vision Diurnal and predacious hawks have exceptionally keen sight Their eyes are directed forward so that the two visual fields overlap to a large extent but not completely Two foveaeia central one on the optic axis and one placed more laterallygcontain as many as a million cones per square millimeter Images of objects that are straight ahead of a hawk fall on the central fovea of each eye and concurrent images of objects to either side fall on the lateral foveae In contrast to the diurnal birds early mammals were nocturnal creatures with few cones but many rods and many mammals do not have color vision Color vision evolved independently in primates and a few other primarily diurnal groups of mammals Thermoreceptors Vertebrates can detect thermal changes in their environment Such an ability is critical for thermal regulation in endothermic birds and mammals but the mechanism for detecting environmental temperature changes is not well understood Neurophysiologists have demonstrated small areas of mammalian skin that are sensitive to heat or cold and certain cells in the mammalian hypothalamus respond to changes in blood temperature Some investigators propose that specific encapsulated nerve endings in the skin are dedicated hot or cold receptors Others believe that temperature changes are detected by the combination and pattern of stimulation of encapsulated and free neuron endings Specialized infrared detectors are present in some groups of snakes In boa constrictors and pythons the infrared receptors are in a series of shallow pits on the scales bordering the mouths Independently the rattlesnakes and other pit vipers evolved a pair of deep pit organs hence the name pit viper on the face between the eyes and nostrils Fig 123120 Highly branched free neuron endings with many mitochondria lie in a delicate membrane within the pit These pits are sensitive to slight differences in infrared radiation between the warmblooded prey of the snake and the prey s surroundings If the pits are not obstructed a rattlesnake can strike at a bird or mouse with incredible accuracy even in the dark SUMNIARY 1 Free nerve endings receptor cells and aggregations of receptor cells called sense organs provide vertebrates with essential information about changes in their internal and external environments 2 The sense of smell or olfaction is detected by olfactory neurons These cells are located in the nasal cavities and their processes to the brain constitute the olfactory nerve Vertebrates differ in the ways that they move water or air across these cells 3 Most terrestrial vertebrates have a distinct group of olfactory cells that form vom eronasal organs Jacobson s organs Often pheromones and other odors of importance in the animal s social interactions are detected by this mechanism The terminal nerve also may be part of a system for detecting pheromones dealing with reproduction 4 Gustatory receptors are taste buds of endoderm al or ectodermal origin that are usually located within the oral cavity and pharynx They are supplied by the facial glossopharyngeal and vagus nerves Taste buds may be distributed widely over the body surface in some species of teleosts 5 The skin of vertebrates contains many free neuron endings that are stimulated by injuries In addition mammals have specialized touch and pressure receptors in the skin 6 Proprioceptors include tendon organs and muscle spindles They monitor the force the degree and the rate of contraction of skeletal muscles They provide information by which these factors are adjusted during muscle contraction 7 The lateral line system of anamniotes includ ing larval lissamphibians consists of linearly arranged neurom asts usually located within canals in the skin They provide information on water currents the animal s own movements and lowfrequency vibrations Lateralis fibers return to the brain in as many as six lateral line nerves which usually are associated closely with the facial glossopharyngeal and vagus nerves Chapter 13 8 The electroreceptors found in chondrichthyans and many osteichthyans are modified parts of the lateral line system These fishes can sense the electric activity of the muscles of other animals as they search for prey39 some others also generate and receive electric pulses in electrolocation and electrocommunication systems 9 The inner ear is closely related to the lateral line system It consists of a membranous labyrinth that is surrounded by perilymph and lodged in an osseous labyrinth in the otic capsule The mechanoreceptive hair cells of the inner ear lie within the membranous labyrinth 10 Certain groups of hair cells within the membranous labyrinth detect the movements and orientation of an animal in space equilibrium and others detect sound waves 11 A sound source in water generates lowfrequency particle displacement waves and higher frequency pressure waves Many fishes detect low frequencies primarily by the lateral line39 they detect higher frequencies by the sacculus Ostariophysans use the swim bladder and their specialized set of Weberian ossicles as a hydrophone for detecting high frequency pressure waves 12 Lowfrequency sound waves can be detected by tetrapods through superficial skull bones but a tympanic membrane beside an airfilled middle ear cavity is needed to convert pressure waves above 1000 Hz into displacement waves Movements of the tympanic membrane are transmitted by one or more auditory ossicles across the middle ear to the inner ear Here they set up waves in a special perilymphatic channel that carries them to the receptive cells 13 A tympanic membrane probably has evolved independently in at least three lines of tetrapods frogs sauropsids and a subgroup of synapsids that includes the mammals 14 A frog s ear has a tympanic membrane which connects to the columella and an operculum which connects via the opercularis muscle to the pectoral girdle and front leg The tympanic membrane detects highfrequency mating calls the opercular system detects lowfrequency environmental noises and seismic vibrations Adult salamanders have only the opercular system 15 Most sauropsids have an ear with a tympanic membrane and a single auditory ossicle which is the columella Amphisbaenians and snakes have secondarily lost the tympanic membrane and in these forms the colum ella abuts on the quadrate bone 16 Mammals have a tyrnpanic membrane and three auditory ossicles the malleus incus and stapes The malleus and incus bore the jaw joint in early synapsids with the malleus being homologous to the articular and the incus homologous to the quadrate 17 In mammals the lagena has become the cochlear duct of the inner ear and perilymphatic channels known as the scala tympani and scala vestibuli form the rest of the cochlea 18 Most early fishes amphibians and sauropsids had a median eye complex consisting of a pineal eye a parietal eye or both This complex is retained in many extant groups The median eye monitors ambient light and appears to initiate physiological adjustments to light levels The complex is represented in birds and mammals by the pineal gland 19 The imageforming eyes of vertebrates are essentially similar in all species and consist of three layers of tissue The fibrous tunic forms the cornea and sclera39 the vascular tunic forms the choroid ciliary body and iris and the retina is the deepest layer 20 Light is received by rod and cone cells Rods function in dim light but they cannot distinguish color and rod vision is slightly blurred Cones distinguish colors but require brighter illum ination They form much sharper images 21 Light does not travel far in water Most lampreys chondrichthyans and actinopterygians tend to be nearsighted with a spherical lens located close to the cornea They focus on more distant objects by contracting a muscle that retracts the lens toward the retina Sharks are farsighted and accommodate to close objects by moving the lens toward the cornea 22 The surface of a tetrapod s eyeball is 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the arnpullae of Lorenzini in selected skates Journal ofMorphology 1892257247 Retzius G 188171884 Das Gehororgan der Wirbelthiere Morphologischhistologische Studien 2 volumes Stockholm Samson amp Wallin Smith W J 1977 The Behavior of Communicating An Ethological Approach Cambridge Harvard University Press Sorensen P W Hara T J and Stacey N E 1987 Extreme olfactory sensitivity of gold sh to a steroidal pheromone Joumal of Comparative Physiology 160 3057314 Stem P and Marx J editors 1999 Making sense ofscents Science 2867077728 Studnicka F K 1905 Die Parietalorgane In Oppel A editor Lehrbuch der vergleichenden mikroskopischen Anatomie der Wirbeltiere part 5 Jena Gustav Fischer Szabo T 1974 Peripheral and central components in e1ectroreception In Fessard A editor Handbook of SensoryPhysiology volume 3 part 3 pp 1358 Amsterdam E1sevier Tavolga W N Popper A N and Fay R C 1981 Hearing and Sound Communication in Fishes New York SpringerVerlag van Bergeijk W A 1967 The evolution of vertebrate hearing In Neff W editor Contributions to Sensory Physiology New York Academic Press Wa1dvoge1 J A 1990 The bird s eye view American Scientist 783427353 Walker W F Jr 1981 Dissection ofthe Frog 2nd edition San Francisco W H Freeman amp Company Wa11s G L 1942 The Vertebrate Eye and ItsAdaptiveRadiation Bloom eld Hill Mich Cranbrook Institute of Science Webster D B Fay R R and Popper A N editors 1992 The EvolutionaryBiology ofHearing New York SpringerVerlag Wever E G 1985 TheAmphibian Ear Princeton Princeton University Press Wever E G 1978 TheReptilian Ear Its Stmcture and Function Princeton Princeton University Press Wurtman R J Axelrod J and Kelley D E 1968 The Pineal New York Academic Press Zimmerman K and Heatwolfe H 1990 Cutaneous photoreception A new sensory mechanism for reptiles Copeia 199086062 1Choanata is the group that includes tetrapods as Well as fossil taxa such as TOsteolepiformes and TElpistostegidae see Chapter 3 and Figure 315 in particular 2Exceptions include adult lissarnphibians that are aquatic including Xenopus and Necturus which have vomeronasal systems 3Scleroglossa includes several groups such as gekkos skinks varanids amphisbaenids and snakes Chapter 3 and Fig 323 in particular 4The terminal nerve is known as cranial nerve 0 Chapter 13 6These are not homologous to the thermoreceptive organs ofpit vipers see p 433 7Some neurobiologists suspect that certain shorebirds also are electroreceptive with putative receptors on the bill 8This is a deeply embedded but very unfortunate term in the literature because it suggests that the arnpullary organs of cat shes are homologous to the arnpullary organs of chondrichthyans again We stress that the condition in catfishes appears to have evolved independently 9VIII is commonly called the statuacuustjc nerve or octaval nerve it also is known as the vestibulocochlear nerve in mammals Chapter 13 10It Was proposed that these magnetic particles enabled chondrichthyans to detect the earth s magnetic field but others believe that this is not true Hanson et al 1990 11The cochlear nuclei of frogs do not appear to be homologous to the cochlear nuclei of amniotes which is evidence that the central connections of these sensory systems also evolved independently 12See Fig 320 for Sauropsida which includes the living turtles and diapsids 13The organ of Corti of a bird convergently resembles the organ of Corti of a mammal Both terms are unfortunately embedded in the literature ie one should be changed 14Many Paleozoic amphibians had an otic notch in a similar position that may have held a tympanic membrane 15The operculum of lissarnphibians is not homologous to the operculum of osteichthyans or chimeras Which are gill coverings 16Based on phylogeny the cochlea of birds is thought to have been derived independently of the cochlea of mammals 17Thus cyclopia an anomalous condition in Which a single median imageforming eye is present is actually the default developmental condition and Will result if bifurcation of the median evagination fails to occur 18The nictitating membrane of arnniotes is not homologous to the nictitating membrane of sharks 19This is also true in a few squarnates 20These infrareddetecting pit organs of pit vipers are not homologous to the pit organs of the lateral line system FIGURE 12 1 A portion of the human olfactory epithelium After Williams et al FIGURE 122 Olfactory organs of shes A Olfactory organ of a lamprey B Olfactory organ of an eel After Kleerekaper FIGURE 123 Evolution of nasal passages and the choana TOsteolepiforms and tetrapods have a choana Which is a connection of the nasal passages to the oral cavity FIGURE 124 Vomeronasal organ A Generalized snake or varanid scleroglossans With forked tongues B Mammal C Ungulate A After Bellairs B after Hillenius C after Smith FIGURE 125 Gustatory organs A Human taste bud B The distribution of taste buds on the surface of a cat sh Each dot represents 100 taste buds Taste buds are too numerous on the barbels to show as individual dots A After Williams et al B after Atema5Recent evidence based on experimental embryological studies of axolotls suggests that taste buds also can arise from ectoderm This finding agrees with the observation that many taste buds on the mammalian tongue occur in areas of epithelium that develop from ectoderm More experimental evidence on the development of taste buds is needed FIGURE 126 Cutaneous receptors A General sensory receptors of mammalian skin as seen in a vertical section B Sinus hair Whisker C Starnose mole Camifvlura The nose of this insectivore has 22 eshy appendages surrounding the nostrils Each appendage has hundreds of specialized touch receptors known as Eimer s organs See text for more information A after Williams et al FIGURE 127 Proprioreceptors A Tendon organ B A muscle spindle After Williams et al FIGURE 128 Neuromast and lateral line canal of a representative teleost A A neuromast B A vertical section through the skin and lateral line canal FIGURE 129 Neuromast arnpullary organ and tuberous organ A Hair cell of a canal neuromast organ typical of chondrichthyans and many other gnathostomes Note the presence of cilia a kinocilium and microvilli the series of stereocilia on its apical surface This cell is a mechanoreceptor and is fundamentally similar to hair cells found in the inner ear of craniates B Sensory cell of an arnpullary organ typical of chondrichthyans and other gnathostomes but not teleosts Note the single kinociliurn and absence of stereocilia This cell is an electroreceptor C Sensory cell of an ampullary organ of a teleost such as a cat sh that has secondarily evolved electroreception Note the absence of a kinociliurn and the presence of stereocilia on its apical surface A and B Modified from Board and Campbell C modified from Narthcutt FIGURE 1210 The distribution of lateral line canals on the head of the bow n Amia After Jarvik TABLE 12 1 Comparison of Chondrichthyan Neuromasts and Electroreceptors Characteristics Distribution of receptors Receptor cell specializations Innervation Peripheral termination Central termination Fun ction Stimulus Role Neuromasts Head trunk and tail Hair cell kinocilium and series of stereocilia Anterodorsal anteroventral and otic lateral line nerves via ventral roots Middle supratemporal and posterior lateral line nerves via ventral roots Afferent and efferent Posterior lateral line lobe Mechanoreception Water movements particle motion Orientation and coordination of swimming movements Modi ed om Boord and Campbell 1977 FIGURE 12 11 Electroreceptors Head Modified hair cell cilium no stereocilia Anterodorsal anteroventral and otic lateral line nerves via dorsal roots Afferent only Anterior lateral line lobe Passive electroreception DC and lowfrequency AC Electrolocation Electroreceptive organs of sharks and coelacanths A Ventral view showing the distribution of the lateral line and ampullary organs on the head of a shark B Dorsal view of the lateral line and ampullary organs on the head of a shark C Anatomy of an individual ampullary organ D The rostral organ of Latimeria A and B After Daniels C after Szaba D a er Bemis and Hetheringtan FIGURE 12 12 Experiments on electroreception by sharks A A live at sh lying buried in the sand draws an attack by the shark B A live at sh in an agar box transparent to electric elds through which a current of water is owing draws an attack directly on itself C The shark attacks downstream of a dead sh in the agar box where the water stream surfaces D A live at sh in the agar box covered by a sheet of plastic which acts as an electrical insulator and chemical barrier fails to draw an attack E Two electrodes buried in the sand draw attacks F The shark preferentially attacks an active electrode instead of chopped bits of food A er K ulmijn FIGURE 12 13 Cladogram of electroreception Ampullary electroreception was independently lost in neopterygians the group of actinopterygian shes that includes gars bow ns and teleosts frogs and amniotes Electroreception reevolved at least twice in teleosts and at least once in amniotes FIGURE 1214 Three stages in the development of the inner ear A Otic placode stage B Otic pit stage C Otic vesicle stage AfterArey FIGURE 12 15 Inner ear of a typical gnathostome Blue indicates structures lledwith endolymph Green spaces are lled with perilymph A er Kingsley FIGURE 12 16 Lateral views of the labyrinth of representative vertebrates A A lamprey B A teleost C A frog D A turtle E A bird F A mammal A and C A er Retzius FIGURE 12 17 A dorsal vieW of the Weberian apparatus of an ostariophysan After Popper FIGURE 12 18 Audiograrns comparing hearing sensitivity of two teleosts a tuna and a gold sh Which is an ostariophysan The ear of an ostariophysan is far more sensitive to sound and also can detect a broader range of sound frequencies After Fay and Popper FIGURE 1219 Ears of squamates and birds A A surface view of the ear of a squamate B A transverse section through the ear of a squamate C The auditory part of the ear of a bird D The highly modi ed middle ear of a snake B After Portmann C after Romer and Parsons FIGURE 1220 Lissarnphibian ears A The ear of an adult bullfrog in surface view below and dissected above B The auditory mechanisms of a larval salamander C The auditory mechanisms of an adult salamander A Modified from Walker and Homberger B and C after Kingsbury and Reed FIGURE 1221 Face of a giant leafnosed bat Rhinolophidae Hipposideros commersom39 to show enlarged pinna used in ultrasonic hearing After Vaughan et al FIGURE 1222 The mammalian ear based on the human ear A A transverse section through the ear B A diagram of an uncoiled cochlea C A transverse section through the cochlea D Schematic diagram of innervation of a mammalian ear A Modified from Walker and Homberger B and C after Dorit et al D after F awcett FIGURE 1223 The median eye complex of representative vertebrates A Larnprey B Frog C Lepidosaur D Mammal After Studnicka FIGURE 1224 A mammalian eye FIGURE 1225 Detailed structure of the front of a mammalian eye After F awcett FIGURE 1226 Retinal structure A The layers of the eyeball and the connections among cells Within the retina B An enlargement of the junction between the outer and the inner segment of arod A After Dowling and Boycott B After Giese FIGURE 1227 The development of the eye A Optic vesicle stage B Optic cup stage C Lens vesicle stage After Arey FIGURE 1228 The eyeballs of representative vertebrates A A teleost B A frog C A lizard D An owl A er Walls FIGURE 1229 Eyes adapted for aquatic versus terrestrial vision A The eye of a typical teleost in water B The eye of a typical teleost in air C The eye of a typical mammal in air D The eye of a typical mammal in water E The foureyed sh Anubleps lives at the water surface and has an eye specialized to see both above and below water F Detail of the eye of Anableps note the barrelshaped lens Light passing into the eye from the air above the sh passes through the short axis of the lens and focuses on the ventral portion of the retina Light passing into the eye from the water beneath the sh passes through the long axis of the lens and is focused on the dorsal portion of the retina FIGURE 1230 Eyelids and accessory structures A The stationary upper and lower eyelids and nictitating membrane of the eye in a shark B The adipose eyelid of a mackerel is composed of clear tissue It allows the head to be streamlined without limiting the eld of view T he top view is a lateral view and the lower gure is a schematic section through the eye and adipose eyelid C The lacrimal apparatus of a mammal A er Partmann FIGURE 1231 A section through the pit organ of a rattlesnake A er Gamaw and Harris
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