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AMER. ZOOL., 17:431-441 (1977). Structural and Functional Organization of the Lateral Line System of Sharks ROBERT L. BOORD Department of Biological Sciences and Institute for Neuroscience and Behavior, University of Delaware, Newark, Delaware 19711 AND C. B. G. CAMPBELL Department of Anatomy, California College of Medicine, University of California, Irvine, California 92717 SYNOPSIS. The lateral line sense organs of sharks include ampullae of Lorenzini and neuromasts. Each of these two classes of receptors is highly specialized and therefore can be expected to biologically respond to one specific modality of stimulus of minimal threshold intensity. Current anatomical, electro-physiological and behavioral evidence indicates that the ampullae are organized to respond to very weak DC and low frequency AC electric fields that originate from external sources in the environment and that this information is used in the detection of prey. Neuromasts consist of canal receptors and pit organs and are mechanoreceptors that are sensitive to water movements caused by external sources as well as the animal's own swimming movements. There is no convincing experimental evidence of the behavioral role that neuromasts play in the life of sharks, but they can orient toward a source that causes water displacements and perhaps use the neuromast system in the coordination of locomotor activity. Ampullae and neuromasts are innervated by different components of the lateral line nerves that project to special terminal areas within the central nervous system. The dorsal root of the anterior lateral line nerve, which is believed to carry nerve fibers from the ampullae of Lorenzini exclusively, enters and terminates within the anterior lateral line lobe of the medulla. Neuromasts (canal and pit organs) are innervated by the ventral root of the anterior lateral line nerve and posterior lateral line nerve, which project to the posterior lateral line lobe (nucleus medialis) of the medulla and, in addition, distribute to the eminentia granularis of the cerebellum, superior and inferior lobes of the auricle, and to the spinal cord. There is no apparent overlap between those central terminal fields that receive fibers from electroreceptors and those that receive fibers from mechanoreceptors nor with the central terminal field of VIII"1 nerve neurons. This supports the contention that different functional classes of lateral line receptors are specialized to perform a particular function, but the central coordinating and integrating mechanisms are unknown. embryonically and morphologically to those receptors that are housed within the Lateral line sense organs are considered inner ear. Lateral line receptors do share components of the acousticolateralis sys- certain developmental (originate from tern of vertebrates because they are related epidermal thickenings called placodes) and superficial anatomical (the sensory cell '. ~ '. ~ \ ~ T \ is a hair cell) features with vestibular and ~ INTRODUCTION Experiments designed to elucidate the central pro- jections of lateral line nerves were conducted at the University of Delaware's Marine Studies Center at Lewes, Delaware. We gratefully acknowledge the invaluable assistance of Dr. Kent S. Price, Jr., Director ,. of the Marine Studies Center, for providing space, facilities and material. The original work was suPported by NIH Grants NS11272 and NS08209 to R.L.B. and C.B.G.C. respectively. . . _ _ . _ auditory sensory areas but differ in fundamental structure, stimulus modality to which they respond a n d the behavioral , in t h e Hfe o f t h e organjsrn. role t h . i r-i i i •• i i Among the Elasmobranchn, even the lateral line c o m p o n e n t of the acousticolateralis sensory system consists of dif- 431 432 ROBERT L. BOORD AND C. B. G. CAMPBELL ferent structural and functional types of receptors and, although these receptors are generally said to be supplied by a common lateral line nerve that has its roots within a common acousticolateralis area of the medulla, the peripheral innervation and central connections of each class of lateral line receptor differ. According to the terminology of Dijkgraaf (1963), the lateral line organs of sharks can be classified as ordinary or ampullary. Included in the former category are canal organs or neuromasts and pit organs or free neuromasts, which are distributed in specific patterns over the head, trunk and tail. Canal neuromasts are situated at regular intervals at the bottom of fluid.-filled canals and pit organs are located between specially modified scales, but both are similar in structure and exposed directly or indirectly to the external environment. Ampullary sense organs include the ampullae of Lorenzini which are situated on the walls of alveoli at the blind ends of jelly-filled canals that traverse the dermis and epidermis to open onto the surface by a small pore. Ampullae are restricted to the head. Lateral line organs are highly specialized and therefore can be expected to consistently respond in a biologically meaningful way to one specific modality of stimulus of minimal threshold intensity. Although responses can be elicited by a variety of stimuli, Murray (1974) points out that the true function of a sense organ can only be shown with certainty when certain requirements are met. These requirements are: (1) the structural features of the receptor must be compatible with the possible function, (2) the response to a particular natural stimulus must be shown to initiate or control behavioral or homeostatic responses of the animal, and (3) electrophysiology must provide a knowledge of the underlying mechanism. Another requirement must be added to this list; that is, if a receptor has a special function, the nerves that innervate it will have a special representation within the central nervous system. The purpose of this paper is to consider the structural and functional organization of the peripheral and central lateral line sensory system of sharks in the light of the above criteria. The literature on the peripheral system is vast but historical aspects will receive little attention because there is currently general agreement as to the specific functions of lateral line receptors. In the final analysis, regardless of the differential response of the peripheral receptor, behavioral activity depends upon information carried to the central nervous system in the form of nerve impulses and transferred via an intermediate nerve network to appropriate motor neurons; however, studies on central mechanisms are meagre. Finally no anatomical system can be understood or appreciated unless considered in the light of its evolutionary history which, although highly speculative, cannot be omitted. THE AMPULLARY SYSTEM This component of the lateral line sensory system consists, in sharks, of the ampullae of Lorenzini. Norris and Hughes (1920), in addition, describe some peculiar special tubular organs on the anterior wall of the spiracle that they interpret as modified ampullae but about which nothing is known; therefore, our discussion is restricted to the ampullae of Lorenzini. Anatomy These sense organs consist of jelly-filled canals that end blindly in subcutaneous tissue as ampullae. Each ampulla, in Mustelus canis, consists of 8-9 alveoli whose walls contain the sensory epithelium and which is innervated by a small fascicle of nerve fibers that enters at the centrum cap, loses its myelin and spreads out over each alveolus (Waltman, 1966). Although ampullae of Lorenzini can respond to thermal, mechanical, chemical and electrical stimuli, there is abundant evidence to indicate that they are biologically electroreceptors (Bullock, 1974; Kalmijn, 1971, 1974; Murray, 1974) and are highly specialized to passively detect very weak DC and low frequency AC electric fields originating from external animate or inanimate LATERAL LINE SYSTEM OF SHARKS J4 sources in the environment. They are not electric organs that actively emit electric discharges and then respond synchronously to these discharges as is the case among the electric fishes. Waltman (1964), shows that, in Raja, the anatomical features, at the ultrastructural level, of Lorenzinian ampullae are compatible with their exceptional electrical properties. Presumably his findings in the skate are applicable to sharks. He shows that the inner layer of the canal wall is composed of squamous epithelial cells joined together by tight junctions and desmosomes so that it must be impermeable to ions and therefore acts as an insulating layer. The sensory (alveolar) epithelium consists of a single layer of receptor cells and accessory cells. The receptor cells (Fig. IB) are pear-shaped, bear a single cilium and are joined at their necks with the pyramid-shaped accessory cells by tight junctions. No electrical leakage can occur between the superficial cell layer of the sensory epithelium so that it, like the canal epithelium, is insulated from the extracellular space. The high electrical resistance between the inside and outside of the canal wall, as compared to other epithelial tissues, the low electrical resistance of the jelly in the canal, and the arrangement of the sensory epithelium in parallel and not in series with the canal wall provide the anatomical basis for the electroreceptive function. There is negligible attenuation of DC voltages along the canal and the potential difference across the sensory epithelium is virtually unchanged to that voltage applied at the tube end. The single cilium is considered unnecessary for electrical sensitivity and indicates a mechanical function (Szabo, 1972) but there are no stereocilia, as are typical of mechanoreceptors, and the cilium has an unusual axonemal pattern. Instead of the usual 9 + 2 arrangement (9 peripheral double-barreled tubules surrounding a central pair of single tubules), the arrangement is 8 + 1 in the body of the cilium and 9 + 0 at the base. Furthermore, there are no apparent root fibers or basal body associated with the cilium. Ampullary sensory epithelium is not 433 FIG. 1. Diagram of canal neuromast (A) and ampullary (B) sensory cells showing the differences in their innervation and apical surface. Abbreviations: aff, afferent nerve ending; C, cilium; eff, efferent nerve ending; K, kinocilium; St, stereocilia. (From Roberts and Ryan, 1971, and Waltman, 1966) covered by a cupula but is overlain by a corpuscular layer consisting of extracellular membrane fragments and membrane bound vesicles. Behavior Dogfishes can respond or are sensitive to weak electric fields in the water and it has been shown that the ampullae of Lorenzini mediate the electrical stimuli. Dogfishes (Scyliorhinus caniculus) respond to uniform square wave fields of 5 Hz with a voltage gradient of 0.1 ptV- cm"1, as evidenced by the eyelid reflex. Furthermore, small flatfish (and other teleosts) produce DC bioelectric fields of an average of 0.2 fiW• cm"1 at a distance of 10 cm, which can be detected by sharks and rays from distances greater than 10 cm (see Kalmijn, 1974). After determining that sharks are sensitive to electric fields, Kalmijn (1971) designed a series of experiments that yielded convincing evidence that their electroreceptive system is used in detecting prey. Sharks are able to find and devour concealed flatfish in the absence of chemical (olfactory), mechanical and visual stimuli. Feeding responses are abolished when the living flatfish are electrically shielded or replaced by pieces of dead fish. Moreover, when buried electrodes are 434 ROBERT L. BOORDAND C. B. G. CAMPBELL used to simulate the bioelectric fields of the and pit organs or free neuromasts that are flatfish, sharks shows the same feeding situated between pairs of modified scales. behavior toward the electric field pro- The main element of the former is the duced by the electrodes as they do toward lateral line canal that runs the length of the trunk and into the tail and is continuous living prey. rostrally into the head where the canals are arranged in complicated but constant patPhysiology terns. The distribution of pit organs varies Responses to a variety of stimuli, e.g., with the species, but they occur along the mechanical (pressure), thermal, chemical dorsolateral surface of the body dorsal to and electrical, can be recorded from single the lateral line or, in some species, both axons from the ampullae of Lorenzini by dorsal and ventral to the lateral line (Teselectrophysiological methods, but Murray ter and Kendall, 1967). Pit organs of the (1974) concludes that the most satisfactory head are confined, in Squalus acanthias and functional stimulus appears to be electri- Mustelus cards, to a pair in front of each cal. endolymphatic pore and a mandibular row There is a regular resting discharge back of the lower jaw (Norris and Hughes, from the ampullae (in Raja ocellata), i.e., 1920). nerve impulses are conducted along the axons that innervate the ampullae without Anatomy being stimulated. Indications are that this discharge is spontaneous because under Hair cells (Fig. 1A) of canal neuromasts maintained DC electrical stimulation, the are cylindrical and, unlike those of the initial increase in the action potential fre- ampullae, do not extend the entire width quency adapts, in a few minutes, back to of the sensory epithelium. Supporting cells the resting frequency. do reach the basement membrane and Murray (1967, 1974) showed that this in- extend between the hair cells which they crease in frequency occurs with cathodal envelop at their distal surfaces. Each hair stimulation of the ampullae (i.e., when the cell contains a single long kinocilium with cathode is placed at the canal opening and eleven tubules in the typical 9 + 2 arthe anode elsewhere on the fish). This is rangement (9 peripheral doublets suropposite to other lateral line receptors rounding a central pair of simple tubules) where it is the anode that excites. The DC and as many as 30 stereocilia, all of similar current threshold for the response is as height (3-4 fim). The outer tubules of the low as 1 /iV/cm along the tube; equally kinocilium participate in the formation of effective is low frequency AC current a basal body. The entire sensory (from 0-80 impulses per second). The im- epithelium is covered by an acellular portant point is that sharks and rays are gelatinous cupula which attaches to the sensitive to electrical stimuli from DC up to kinocilium and stereocilia and likely 8 Hz as determined by both behavioral and reaches the roof of the canal. At least in electrophysiological methods. Moreover, Scyliorhinus caniculus, the position of the the responses to electrical stimuli are un- kinocilium is variable and only occasionally doubtedly mediated by the ampullae of faces opposite directions in adjacent hair Lorenzini which are sensitive to extremely cells (Roberts and Ryan, 1971). Furthermore, the stereocilia do not increase in low stimulus values. height stepwise fashion toward the kinocilium. These conditions are unlike THE ORDINARY SYSTEM those found in the neuromasts of teleosts (Flock, 1967). This component of the lateral line sysRoberts and Ryan (1971) describe, in tem consists of sensory areas or neuromasts located in a series of fluid- Scyliorhinus caniculus, a second sensory cell filled canals that communicate at inter- intermingled among the hair cells. Second vals, with the surrounding water via pores, sensory cells are more abundant than hair 435 LATERAL LINE SYSTEM OF SHARKS cells, lack stereocilia and contain a single short cilium (kinocilium) located in a shallow pit in the cell surface and containing variable axonemal patterns. They contain many long thin microvilli with no apparent internal electron dense structure nor any regular relationship with the cilium. The function of these second sensory cells is unknown. They are innervated by afferent nerve fibers (no efferents) and may represent a stage in the development of hair cells or serve functionally as secretory cells. Behavior There are no behavioral experiments on sharks that offer conclusive evidence of the biological role of the ordinary lateral line system of sense organs, but there can be little doubt that neuromasts are sensitive to water movements. Fibers that innervate ordinary lateral line receptors discharge vigorously, unlike those that innervate ampullary receptors, when the neuromasts of free swimming sharks are stimulated by water disturbances (Kalmijn, 1974). It is reasonable to suppose that sharks can and do respond to water movements caused by other animals and inanimate objects, at least at short distances. By short distances is meant the near field which is that distance from a vibrating sphere where a combination of water displacements and pressure waves, both simultaneously produced by the source, coexist (Harris and van Bergeijk, 1962). The far field consists of only pressure waves and exists beyond that point where the amplitudes of pressure waves and displacements are equal. The best evidence is that neuromasts are probably most sensitive to water displacements which is the case among bony fishes (Harris and van Bergeijk, 1962; Suckling and Suckling, 1964). Banner (1967) shows, in lemon sharks, that it is displacement rather than pressure emanating from a sound source that causes a behavioral response (closing of jaws and brief cessation of respiration). However, it was not determined whether it was lateral line or labyrinthine receptors responding to the stimulus. Sharks can respond behaviorally to sound sources in both the near and far field and are capable of orienting toward a sound source in the far field (Wisby et at, 1964), but there is no convincing evidence as to what receptors are involved. It is unlikely, although there is no experimental proof, that the ordinary lateral line system responds to pressure waves and acts as a hearing organ. Even if the neuromasts respond to water displacement caused by sound in the near field, it is improbable that the central nervous system processes this information as hearing in the strict sense. TABLE 1. Some structural and functional features of the lateral line system of sharks. Sense Organ Distribution Receptor Innervation Peripheral termination Central termination Function Stimulus Role ampullae of Lorenzini head modified hair cell (cilium; no stereocilia) anterior lateral line nerve (dorsal root) afferent anterior lateral line lobe passive electroreception DC and low frequency electric fields electrolocation neuromasts head, trunk, tail hair cell (kinocilium; stereocilia) anterior lateral line nerve (ventral root); posterior lateral line nerve; nerve IX afferent and efferent posterior lateral line lobe, eminentia granularis and auricle of cerebellum mechanoreception water movements (displacements) orientation; coordination of swimming movements 436 ROBERT L. BOORD AND C. B. G. CAMPBELL Physiology Neuromasts, like ampullary organs, are spontaneously active and discharge in a non-swimming dogfish at 15-20 impulses/ sec (Roberts, 1972). They are sensitive to external water displacements as well as to the shark's own swimming movements and perhaps the former stimulus causes displacement of the cupula that covers free neuromasts and the latter stimulus results in displacement of the fluid that causes shearing displacement of the cupula of the canal neuromasts. No experiments have apparently been designed to distinguish between the roles of these two ordinary types of neuromast organs. Roberts (1972) shows that the responses of canal neuromasts are bidirectional, i.e., a particularlar receptor discharges when the tail moves in one direction and is inhibited when the tail moves in the opposite direction due to the to and fro movements of the fluid within the canal. Moreover, the discharges occur in bursts that are synchronous with the frequency of the locomotory movements of the shark. It is probable that lateral line neuromasts are capable of playing a role in the coordination of swimming or proprioception, but the mechanism is unknown. If this is true, there is no satisfactory explanation because fishes are known to swim normally after the lateral line nerve has been transected and the neuromasts therefore denervated. RECEPTOR CELL INNERVATION The hair cells of neuromast organs are innervated by afferent and efferent fibers; those of ampullary organs only by afferent fibers (Figs. 1A and IB). The synapse at the base of ampullary receptor cells, in Raja, consists of synaptic vesicles aligned on either side of a ribbon-shaped presynaptic bar (inside the receptor cell) but with few vesicles within the nerve terminal (Waltman, 1966). This type of synapse is interpreted as afferent and the receptor cell is therefore presynaptic relative to the nerve ending. The afferent synapse of the hair cells of canal neuromasts in the dogfish lacks a presynaptic bar, although clusters of vesicles occur inside the cell (Roberts and Ryan, 1971). A second type of synapse occurs at the base of canal neuromast hair cells and is considered efferent because of the abundance of vesicles inside the nerve terminal and subsynaptic cisternae inside the receptor cell (the hair cell, in this case, is subsynaptic because efferent neurons conduct impulses from the central nervous sytem). The second sensory cells of canal neuromasts are innervated by afferent fibers, but whether they possess efferent terminals is uncertain (Roberts and Ryan, 1971). No ultrastructural studies of the hair cells of pit organs and their innervation are available. Minute displacements of the cupula of canal neuromasts and consequently the stereocilia toward the kinocilium result in an electrical excitability of the apical hair cell membrane (a depolarization) which is conducted across the receptor cell. This electronic conductance triggers, by some little known mechanism, the release of an unidentified neurotransmitter that evokes a response in the form of a nerve impulse that is carried to the central nervous system by afferent nerve fibers. Evidence that the release of the transmitter is controlled and triggered by electrical activity is indicated in the receptor cells of the ampullae where the effective stimulus is electrical and is presumably amplified across the receptor cell. Stimulation of the efferent neurons, which are not spontaneously active, can suppress or completely inhibit spontaneous activity in the afferent fibers from the trunk neuromasts in the dogfish, Scyliorhinus caniculus (Russell and Roberts, 1972). Natural stimulation of neuromast organs by directing water jets at the lateral line canal evokes no activity in the efferent fibers; however, efferent activity does occur in response to stimuli (chemical, tactile) that cause the shark to move but not to stimuli (visual) that do not cause the shark to move (Roberts and Russell, 1972). These authors therefore conclude that the lateral line efferent system acts neither as a feedback regulatory system LATERAL LINE SYSTEM OF SHARKS 437 nor exerts a tonic effect on the hair cells as believed to be the case in the auditory system. They suggest, since vigorous muscle activity and swimming movements of the shark are accompanied by efferent activity, that the function of the efferent system operates in a protective manner to prevent the sense organs from being over-stimulated. This implies an insensitivity or decrease in sensitivity during movement of the shark and the neuromasts are fully responsive after movement stops. THE LATERAL LINE NERVES Canal and free neuromasts and ampullary receptors of the head are innervated by the anterior lateral line nerve; canal neuromasts and pit organs of the trunk and tail and the pit organs located in front of the endolymphatic pores are innervated by the posterior lateral line nerve. Special somatic sensory components of the glossopharyngeal nerve are said to supply only neuromasts of the anterior portion of the main lateral line canal. Anterior and posterior lateral line nerves are generally considered branches of branchiomeric cranial nerves VII and X respectively; however, they neither innervate structures of visceral origin nor distribute with the rami of those branchial nerves with which they are closely associated. They are separate nerves with their own ganglia and are composed only of afferent and presumably efferent neurons that innervate lateral line sense organs. The anterior lateral line nerve consists of superficial ophthalmic, buccal, otic and external mandibular branches (Fig. 2). Proximal to its ganglion, each branch divides and enters the medulla as a dorsal root and a ventral root (Fig. 3). A certain proportion of nerve fibers in each branch apparently differentially innervate electroreceptors and mechanoreceptors. Furthermore, McCready and Boord (1976) present circumstantial evidence that those fibers carried by the dorsal root innervate ampullae of Lorenzini and those that innervate canal and pit organs are carried by the ventral root. FIG. 2. The lateral line nerves of the smooth dogfish Mustelus canis as seen in a dorsolateral view of the brain stem. The anterior lateral line nerve (NLLa) consists of superficial ophthalmic (os), buccal (b), otic (o) and external mandibular branches. The external mandibular branch is included with the VIIth cranial nerve as the hyomandibular trunk (h). Some lateral line neurons also occur in the glossopharyngeal nerve (IX). Other abbreviations: ALL, anterior lateral line lobe; Aur, auricle of cerebellum; Gb, ganglion of buccal branch of NLLa; Gos, ganglion of superficial ophthalmic branch of NLLa; Gg, geniculate ganglion; God, ganglion of dorsal root of otic branch of NLLa; NLLp, posterior lateral line nerve; Rod, dorsal root of dorsal ramusof NLLa; Rosd, dorsal root of superficial ophthalmic branch of NLLa; Rosv, ventral root of superficial ophthalmic branch of NLLa; Rov, ventral root of otic ramus of NLLa; VIII, statoacoustic nerve; Vm, mandibular ramus of trigeminal nerve; Vmx, maxillary ramus of trigeminal nerve; Vop, deep ophthalmic ramus of trigeminal nerve; Vos, superficial ophthalmic ramus of trigeminal nerve; X, vagus nerve. The posterior lateral line nerve, proximal to its ganglion that is closely associated with the vagal ganglion, is a broad flat nerve that courses anteriorly from the vagal roots to enter the medulla as a single root just dorsal to the glossopharyngeal root (Figs. 2 and 3). LATERAL LINE CENTRAL PATHWAYS Acousticolateralis area The first order neurons that comprise the lateral line nerves project, along with 438 ROBERT L. BOORDAND C. B. G. CAMPBELL the statoacoustic nerve, to an area of the medulla called the acousticolateralis area, although there is no experimental evidence to indicate common terminal fields of lateral line and statoacoustic nerve fibers. The acousticolateralis area includes three nuclear groups; namely, nucleus dorsalis or anterior lateral line lobe, nucleus medialis or posterior lateral line lobe, and nucleus ventralis (Ariens Kappers et al., 1936). In the revised nomenclature of Smeets and Nieuwenhuys (1976) nucleus ventralis and nucleus medialis are equivalent to nucleus vestibularis magnocellularis and nucleus intermedius areae octavolateralis respectively. The medial nucleus occupies the dorsolateral portion of the medulla and extends from a nuclear center called the eminentia granularis, which caps its rostral extremity, to the vicinity of the bulbospinal junction. The dorsal nucleus occupies a large protrusion that overhangs the IVth ventricle and extends from the caudal cerebellum to a level just rostral to the vagal lobe. Both dorsal FIG. 3. Diagram, lateral view of the brain stem of the smooth dogfish Mustelus cants, showing the positional relationships of the superficial roots of the dorsal (RLLad) and ventral (RLLav) roots of the anterior lateral line nerve, posterior lateral line nerve (NLLp), glossopharyngeal nerve (IX), facial nerve (VII), statoacoustic nerve (VIII), motor division of the trigeminal nerve (RVm), and sensory division of the trigeminal nerve (RVs). ALL, anterior lateral line lobe. and ventral nuclei are covered by a cerebellar crest (crista cerebellaris) which is continuous with the molecular layer of the cerebellum and is underlain by a layer of Purkinje-like cells whose dendrites radiate into dorsal and ventral nuclei. Lateral line projections Lateral line nerve fibers, like all primary sensory neurons, enter the central nervous system and bifurcate into ascending and descending branches. The course and termination of first order neurons of anterior and posterior lateral line nerves of the smooth dogfish, as determined by silver impregnation methods for depicting degenerating axons and their terminations, are shown in Figure 4. The posterior lateral line nerve enters the brain stem and adopts a rostromedial and rostrodorsal projectory to reach the dorsolateral portion of nucleus medialis, where it divides into ascending and descending roots. The ascending root extends rostrally ventral to the crista cerebellaris giving off collaterals or whole fibers that terminate about the cells of nucleus medialis and possibly the dendrites of the Purkinje-like cells and terminates massively in the eminentia granularis. At the level of the eminentia, some ascending root fibers diverge into two bundles that course caudodorsally to enter the two leaves of the auricle of the cerebellum. The descending root migrates medially as it passes through the medulla so that at the level of the bulbospinal junction it occupies a position near the midline. The number of axons in the descending tract diminishes as it descends, indicating that fibers terminate about the cells of the medial nucleus and only a few fibers are traceable into the uppermost cervical spinal cord. The anterior lateral line nerve enters the brain stem as a dorsal root and a ventral root. The dorsal root enters the anterior lateral line lobe (nucleus dorsalis) and bifurcates to form ascending and descending bundles that extend throughout the medial portion of this lobe. Fibers terminate about the cells that lie among the LATERAL LINE SYSTEM OF SHARKS ascending and descending tracts. There is no evidence of terminal degeneration within the crista cerebellaris or the Purkinje-like cells that lie adjacent to the crista. Furthermore, the distribution of fibers of the dorsal root appears confined exclusively to nucleus dorsalis. Preliminary studies indicate that the axons of the ventral root of the anterior lateral line nerve distribute with those of the posterior lateral line nerve. One difference is that the level of bifurcation of the ventral root of the anterior lateral line nerve and its ascending bundle occupy a more medial position within nucleus medialis but the exact pathways and connections are unproved. Lateral line pathways beyond the level of the first order neuron are uncertain. The chief secondary tract is the acousticolateral lemniscus which is believed to originate from nuclei dorsalis and medialis, crosses the raphe and ascends to midbrain levels. Some of the axons of this lemniscus are said to terminate in the tectum; others in the isthmic nuclei and a nucleus in the ventral part of the midbrain called the medial tegmental nucleus. The latter nucleus is considered a homologue of the torus semicircularis of other nonmammalian vertebrates and the inferior colliculus of mammals but this is uncertain. Nucleus isthmi is a continuation of the acousticolateralis area of the medulla and is said 439 to be connected with both the tectum and tegmentum and therefore a correlation center for acousticolateral and optic impulses. There is no evidence of lateral line pathways to the diencephalon or telencephalon. EVOLUTIONARY ASPECTS The lateral line sensory system possibly has its evolutionary origin in the primitive pore canal system that exists among the ostracoderms as well as early acanthodians, crossopterygians and lungfishes (Denison, 1966). The pore canal system, in certain ostracoderms, consists of larger long straight lateral line canals that open extensively onto the surface by grooves and an interconnected network of smaller mesh canals that open intermittently onto the surface by small pores. Both possessed receptors that could respond to water displacements. It is reasonable to speculate that the generalized pore canal system that primitively covered the entire body became topographically restricted and gave rise to the free neuromasts of the lateral line system. The lateral line grooves could conceivably have become deeper and have been covered by skin to give rise to canal neuromasts (and inner ear). Neither is it difficult to morphologically conceptualize the transformation of mechanoreceptors into electroreceptors. The loss of mechanical sensitivity and the development of an electrical sensitivity need only involve the outer face of the receptor cell. Deformation of the outer cell membrane of the neuromast receptor results in an electronic transduction process that is presumably similar in both mechanoreceptors and electroreceptors (see Bennett, 1971). All sharks, including fresh water species, possess passive electroreceptors, but among Elasmobranchs electric organs also occur, e.g. Torpedenids and Rajids. It can FIG. 4. Diagram, lateral view, showing the pathways of first order neurons of posterior lateral line nerve be assumed that primitive elasmobranchs, (NLLp) and dorsal (NLLad) and ventral (NLLav) whose ancestry is not documented in the roots of the anterior lateral line nerve in the smooth fossil record, possessed a passive elecdogfish, Mustelus cants. Other abbreviations: ALL, trosensory system. During the evolution of anterior lateral line lobe; aur, auricle of cerebellum; em, eminentia granularis; PLL, posterior lateral line the elasmobranchs, electric organs were added independently, as has occurred in lobe. 440 ROBERT L. BOORD AND C. B. G. CAMPBELL diverse fish groups evolutionary lineages. with different CONCLUDING REMARKS lower vertebrates, Handbook of sensory physiology, Vol. III/3, pp. 1-12. Springer-Verlag, New York. Denison, R. H. 1966. The origin of the lateral-line sensory system. Amer. Zool. 6:369-370. Dijkgraaf, S. 1963. The functioning and significance of the lateral line organs. Biol. Rev. 38:51-106. Flock, A. 1967. Ultrastructure and function in the lateral line organs. In P. Cahn (ed.), Lateral line detectors, pp. 163-197. Indiana University Press, Bloomington, Indiana. Harris, G. G. and W. A. van Bergeijk. 1962. Evidence that the lateral-line organ responds to near-field displacements of sound sources in water. J. Acoust. Soc. Am. 34:1831-1841. Kalmijn, A. J. 1974. The detection of electric fields from inanimate and animate sources other than electric organs. In A. Fessard (ed.), Electroreceptors The lateral line system of sense organs is anatomically a special somatic sensory system; therefore it consists of special receptors that are innervated by special functional components of cranial nerves that project to special functional centers within the central nervous system. Lateral line sense organs in sharks include passive electroreceptive ampullary receptors and and other specialized receptors in lower vertebrates, mechanoreceptive canal and free Handbook of sensory physiology, Vol. III/3, pp. 147neuromasts. Each functional class of re200. Springer-Verlag, New York. ceptor responds to incredibly low levels of A. J. 1971. The electric sense of sharks and the appropriate stimulus and fulfills the Kalmijn, rays. J. Exp. Biol. 55:371-383. criteria for sense organs as outlined in the McCready, P. J. and R. L. Boord. 1976. The topography of the superficial roots and ganglia of the introduction. anterior lateral line nerve of the smooth dogfish, Although it can be shown that ampullary Mustelus canis. J. Morph. 150:527-538. organs and neuromasts respond to other Murray, R. W. 1974. The ampullae of Lorenzini. In than electrical and mechanical stimuli, it is A. Fessard (ed.), Electroreceptors and other specialized receptors in lower vertebrates, Handbook of sensory reasonable to assume that lateral line rephysiology, Vol. III/3, pp. 125-146. Springer-Verlag, ceptors are biologically highly selective. New York. Even if there were no selective response at Murray, R. W. 1967. The function of the ampullae of the peripheral level, the differential proLorenzini of elasmobranchs. In P. Cahn (ed.), Lateral line detectors, pp. 277-293. Indiana University jections of the primary neurons indicate Press, Bloomington, Indiana. differential neural coding by the central Norris, H. W. and S. P. Hughes. 1920. 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