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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
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is a hair cell) features with vestibular and
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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
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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. The cranial,
nervous system. How and where informaoccipital, and anterior spinal nerves of the dogfish,
tion received at the periphery is processed
Squalus acanlhias. J. Comp. Neur. 31:293-402.
and integrated with information from Roberts, B. L. 1972. Activity of lateral-line sense
other sensory modalities requires a knowlorgans in swimming dogfish. J. Exp. Biol. 56:105118.
edge of central neural pathways and conRoberts, B. L. and I. J. Russell. 1972. The activity of
nections which are largely unknown.
lateral-line efferent neurones in stationary and
swimming dogfish. J. Exp. Biol. 57:435-448.
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