Download Central Lateral Line and Auditory Pathways: A Phylogenetic

AMER. ZOOL., 24:765-774 (1984)
Central Lateral Line and Auditory Pathways:
A Phylogenetic Perspective1
ROBERT L. BOORD
School of Life and Health Sciences and Institute for Neuroscience, The University of Delaware,
Newark, Delaware 19716
AND
CATHERINE A. MCCORMICK
Department of Anatomy, Georgetown University Schools of Medicine and Dentistry,
Washington, D.C 20007
SYNOPSIS. The phylogenetic origins of the lateral line electrosensory, lateral line mechanosensory, and auditory components of the octavolateralis system are unknown but each
of these sensory modalities appears to have evolved early in vertebrate history. The
octavolateralis terminal field occupies a large area of the dorsolateral wall of the medulla
and among agnathids, cartilaginous fishes, non-teleost bony fishes and, with modifications,
urodeles, consists of a dorsal electrosensory nucleus, a medial mechanosensory nucleus
and a ventral octaval nuclear complex. This arrangement of medullary octavolateral
nuclei, which differs from that of non-electroreceptive and electroreceptive teleosts, is
considered the primitive plan and is retained in that phyletic line leading to tetrapods.
Separate and parallel pathways are known, in elasmobranchs and a few teleosts, to ascend
from each medullary lateral line center to the midbrain and presumably from midbrain
to telencephalic levels via thalamic relays. There is no evidence, with the loss of lateral
line senses among some amphibians and all amniotes, that the central neural pathways
and nuclei are retained and used to process information from other sensory modalities.
The anatomy of the central auditory system of fishes is unknown but is required for an
understanding of whether auditory nuclei and pathways are retained during the fishamphibian transition, or whether new ones arise, to process information from independently evolved peripheral receptors.
INTRODUCTION
groups (holosteans, most teleosts, and some
The octavolateralis system consists of a amphibians). The phylogenetic origin of
lateral line subsystem that includes an array octavolateralis subsystems from a common
ofmechanoreceptorsandelectroreceptors
ancestral source is unknown although
located in the skin, an octaval subsystem ostracoderms apparently possess lateral line
that comprises the mechanoreceptors of the c a n a l s > a n electroreceptive system, and an
membranous labyrinth or inner ear, and i n n e r e a r (Denison, 1966; Baird, 1974;
the sequences of neurons that carry infor- Thompson, 1977) and all octavolateralis
mation from the peripheral receptors of modalities appear established among
each subsystem to various levels of the Devonian gnathostomes (Orvig, 1971).
central nervous system. The octaval comHistorically, most studies of the evoluponent is universally present among ver- t i o n o f t h e octavolateralis system have
tebrates, while the lateral line mechano- involved the peripheral apparatus. Simireceptive component is found in all larval larities in the development and structure
and most adult anamniotes. The electro- o f t h e octaval and lateral line receptors
receptive component is likewise lacking in formed part of the basis for considering
amniotes, and, although widely distributed t h e s e receptors to belong to a common
among anamniotes, is absent in certain "acousticolaterahs" or octavolateralis system. Mechanoreceptors of the lateral line
canals were hypothesized to have given rise
' From the Symposium on Evolution of Neural Sys- t o t h e electroreceptors and inner ear sense
terns m the Vertebrates: Functional-Anatomical Approaches
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presented at the Annual Meeting of the American O r g a n S - T h e P 1 S C i n e e a r W a S considered to
Society of Zoologists, 27-30 December 1982, at be vestibular in function except among
Louisville, Kentucky.
those teleosts that possess gas bladders (i.e.,
765
766
R. L. BOORD AND C . A. McCORMICK
pressure transducers) coupled to the labyrinth (van Bergeijk, 1967). Inner ear auditory receptors were thought to be the last
peripheral octavolateralis component to
evolve, occurring during the rhipidistianamphibian transition with the appearance
of a middle ear transmission apparatus and
new receptors responsive to airborne
sound. The change from aquatic to terrestrial living was accompanied by the loss
of lateral line mechanoreceptors in many
amphibian species, and it was hypothesized
(Larsell, 1934) that the incoming fibers of
the newly evolved auditory receptors synapsed upon a portion of the medullary lateralis center, thus transforming this phylogenetically old area into an auditory
nucleus.
In contrast to these ideas, recent anatomical and physiological studies strongly
indicate that each modality of the octavolateralis system is a separate system that
evolved independently and in parallel
within different vertebrate radiations. This
is to say that the central neural pathways
and centers which process information
from lateralis and octaval receptors were
established early in vertebrate history and
are basic parts of the vertebrate body plan.
Changes that have occurred through time
involve adaptive modifications of primitive
neural substrates to process inputs from
diverse kinds and numbers of peripheral
receptors, including the loss of certain
peripheral receptors and the concomitant
loss of central processing areas (e.g., the
loss of the lateral line system in amniotes).
A basic special somatic sensory pathway
involves a series of neuronal sequences from
the primary neuron to the telencephalon
via relay nuclei at each level of the neuraxis. In the auditory and lateral line systems medullary nuclei receive input from
peripheral receptors and give rise to
ascending lemnisci that terminate in the
midbrain (these medullary nuclei may also
project to the cerebellum and undoubtedly
to the reticular formation). Information is
relayed from the mesencephalon to the
telencephalon via thalamic centers. Such
thalamo-telencephalic projection systems,
contrary to previous belief, are now known
to exist among fishes (Schroeder and
Ebbesson, 1974; Luiten, 1981; Echteler and
Saidel, 1981) and are likely a general characteristic of the vertebrate brain.
The purpose of this discussion is to consider the main currently known features of
the central ascending neuronal pathways
of the mechanoreceptive, electroreceptive, and auditory components of the octavolateralis system and to present evidence
that they are primitive constituents of the
vertebrate central nervous system. The
vestibular component of the octaval subsystem does not form long ascending lemnisci but more localized connections
involved with postural reflexes and will be
considered only as required in discussing
the auditory component. Moreover, major
consideration will be given to the octavolateralis system among those vertebrates
within that phyletic lineage leading to tetrapods.
MEDULLARY LATERAL LINE AND OCTAVAL
PATTERNS IN FISHES
Each octavolateralis subsystem is associated with a specific set of cranial nerves
that terminate within a specialized part of
the octavolateralis area of the medulla (Fig.
1). The electroreceptors and mechanoreceptors of the lateral line system are innervated by the anterior and posterior lateral
line nerves. Among elasmobranches each
anterior lateral line nerve possesses a dorsal root which carries electroreceptive
information from the Lorenzinian ampullae and terminates within a dorsally positioned longitudinal column of cells and
neuropil called the dorsal nucleus. The
ventral root of the elasmobranch anterior
lateral line nerve and the posterior lateral
line nerve innervate mechanoreceptors
(canal neuromasts and free neuromasts or
pit organs) and terminate within another
dorsal cell and neuropil column called the
medial nucleus (Boord and Campbell, 1977;
Bodznick and Northcutt, 1980). The octaval or eighth cranial nerve innervates inner
ear sense organs and terminates within a
ventral column of cells and neuropil consisting of several nuclear subdivisions
(Boord and Roberts, 1980; Northcutt,
1980). This arrangement of the octavolateralis peripheral nerves and three central
EVOLUTION OF OCTAVOLATERALIS PATHWAYS
767
From lateral line
mechanoreceptors
From inner ear
receptors
FIG. 1. Diagram, lateral view, showing the central octavolateralis pathways as presently known in a cartilaginous fish. Abbreviations: AL, anterior lobe of the cerebellum; DON, dorsal (electrosensory) octavolateralis
nucleus; IL, inferior lobe of the hypothalamus; L, lateral nucleus of the lateral mesencephalic nuclear complex;
L Lem, lateral line lemniscus; LP, lateral posterior thalamic nucleus; MD, dorsomedial nucleus of the lateral
mesencephalic nuclear complex; MON, medial (mechanosensory) octavolateralis nucleus: nil, optic nerve;
PL, posterior lobe of the cerebellum; VON, ventral octaval nuclear complex.
nuclear columns occurs in representatives
of Agnatha (petromyzontids), Chondrichthyes (elasmobranchs and holocephalans),
Dipnoi (lungfishes), Crossopterygii (coelacanths), Polypteriformes (bichirs and reedfish), and Chondrostei (sturgeons and paddlefish), although the neuroanatomical
connections have not been experimentally
confirmed in all cases. It is considered the
primitive evolutionary pattern since it
occurs in these early vertebrate radiations
and can be used as a valuable diagnostic
feature for comparative anatomical considerations (McCormick, 1982). Specifically,
the presence of the dorsal root of the anterior lateral line nerve and the dorsal nucleus
in a given species strongly suggests that it
is electroreceptive. This suggestion has
been confirmed physiologically in petromyzontids, polypteriforms, and dipnoans
(Bodznick and Northcutt, 1981; Bullock et
ai, 1983). Conversely, arthrodires (placoderms) are believed to have possessed
ampullae of the Lorenzinian type (i.e., electroreceptors); therefore, it is likely that a
dorsal anterior lateral line nerve root and
a dorsal nucleus were present in these close
relatives of the cartilaginous fishes.
Electroreception appears to have evolved
early in vertebrate history in a population
ancestral to petromyzontids and cartilaginous fishes. Although retained in many
vertebrate lines, including those leading to
land vertebrates, it was lost in the later
groups of actinopterygians (e.g., all living
holosteans and most teleosts). The organization of the octavolateralis area of the
medulla in these non-electroreceptive
species differs from the primitive plan in
that all lack the dorsal nucleus although
the mechanosensory medial nucleus is
retained. The electroreceptive sense has
apparently evolved independently at least
twice in teleosts—in the Osteoglossomorpha (mormyrids and the African notopterids) and in the Euteleosti (silurids and
gymnotids). Electroreceptive teleosts comprise about 1 % of all known teleost species.
The peripheral receptors and central circuitry of the various teleost electrosensory
systems differ from the non-teleost electrosensory system and cannot be considered homologous (Boord and Northcutt,
1982; McCormick, 1982).
The medullary nuclei of the lateralis system of fishes are therefore organized into
three different patterns as shown by nonteleost electroreceptive groups, non-electroreceptive groups, and electroreceptive
teleosts (Fig. 2). The eighth nerve nuclei
of fishes are also organized into three patterns, but the phylogenetic distribution of
these patterns does not parallel those of
the lateral line system. In all cases, the
R. L. BOORD AND C. A . McCORMICK
A
A
B.C A A A!B*
/
\
B:O
o
\ CAUDATA
FIG. 2. Patterns of variation of the primary lateral line areas of the medulla. The letters and symbols across
the top indicate the presence or absence of various conditions with respect to the major lateral line centers
as follows: A, lateral line area consists of the dorsal nucleus and the medial nucleus. A*, dorsal nucleus and
medial nucleus present at least in larval stages. B, lateral line area consists of the medial nucleus. B*, medial
nucleus present at least in larval stages. C, lateral line area consists of the medial nucleus and the newly evolved
electrosensory lateral line lobe. 0, lateral line subsystem absent.
eighth nerve nuclei form a column of cells possess, like tetrapods, separate auditory
and neuropil generally ventral to that of and vestibular centers which are the tarthe lateral line nuclei. The pattern in lam- gets of distinct auditory and vestibular
preys, unlike that in any other vertebrate, nerves. However, the central terminations
is characterized by three aggregates of large of inner ear receptors in fish may not folcells (anterior, intermediate, and posterior low this pattern because these receptors
octavomotor nuclei) that are included may be functionally heterogeneous, i.e., the
within a small-celled ventral nucleus (Lar- same receptor may serve both auditory and
sell, 1967; Northcutt, 1979). It is uncertain gravistatic functions. Moreover, in differwhether agnathans possess inner ear audi- ent species offish different endorgans may
tory receptors in addition to their vestibu- serve as the principal auditory receptor
Iar endorgans.
(Blaxter et al., 1981; Corwin, 1981; Platt
Four eighth nerve nuclei (anterior, mag- and Popper, 1981).
nocellular, descending, and posterior)
occur among chondrichthyans, sarcopter- MEDULLARY LATERAL LINE AND OCTAVAL
ygians, and non-teleost actinopterygians,
PATTERNS IN AMPHIBIANS
and a fifth nucleus (tangential) is recognized in teleosts. Although fishes are
All amphibians possess a lateral line subbelieved to possess inner ear auditory system, at least during larval stages, and an
receptors a separate and specialized med- octaval subsystem. The lateral line subsysullary acoustic nucleus has not been con- tem contains mechanoreceptors and some
clusively identified. In mormyrids each species also possess an electric sense. The
inner ear receptor projects to parts of sev- central organization of electroreceptive and
eral octaval nuclei but the saccule, which mechanoreceptive medullary centers is
is concerned with hearing, also projects to similar to that of primitive electroreceptive
a separate and discrete area of the octaval non-teleostean fishes (Fig. 2). Larsell (1967)
complex (Bell, 1981a). This suggests that reported three anterior lateral line nerve
mormyrids, and perhaps other fish, may roots in larval and aquatic adult urodeles,
EVOLUTION OF OCTAVOLATERALIS PATHWAYS
and the dorsal root apparently carries electroreceptive input from ampullary organs
to a dorsal neuropil region called the dorsal island of Kingsbury (Fritzsch, 1981). It
is therefore likely, as Larsell suggested
(1967), that the dorsal island of Kingsbury
and the dorsal nucleus of primitive electroreceptive fishes are homologous. Ventrally positioned nerve fascicles from lateral line mechanoreceptors terminate
ventral to the electroreceptive area in urodeles, presumably in the medial nucleus,
and the octaval nerve terminates in a column of cells separate from the medial
nucleus (Fritzsch, 1981).
According to Larsell (1967), anuran larvae possess a dorsal island of Kingsbury but
adults, including aquatic species such as
Xenopus, lack this structure and thus are
presumably non-electroreceptive. Lateral
line mechanoreceptive fibers in Xenopus
terminate in the medial nucleus (Boord
and Eiswerth, 1972). At least some larval
apodans possess electroreceptors as well as
mechanoreceptors (Hetherington and
Wake, 1979) but the areas of termination
of these receptors are unknown.
Larsell hypothesized that the amphibian
medial nucleus was transformed into an
auditory, or cochlear, nucleus with the loss
of the lateral line mechanoreceptive system. However, in the premetamorpnic
bullfrog, a mechanoreceptive lateral line
nucleus is situated medial to the octaval
nucleus but disappears during metamorphosis with the loss of the lateral line and
does not contribute to or transform into
an octaval nucleus (Jacoby and Rubinson,
1983). It thus appears that the lateral line
mechanosensory nucleus is lost with the
loss of the peripheral system and has no
counterpart (homologue) in amniotes.
Three nuclei are generally considered to
form the column of cells receiving eighth
nerve input in amphibians, a dorsal (acoustic) nucleus, a ventral nucleus and a caudal
nucleus. In Xenopus, the eighth nerve projects to these nuclei but not to the medial
(lateral line) nucleus. The octaval cell column is the only medullary component of
the octavolateralis area in most adult
anurans. In Rana, the dorsal (acoustic)
nucleus receives input from the newly
769
evolved inner ear auditory receptors
(amphibian papilla and basilar papilla),
while the other otic receptors (semicircular
canals, utriculus, sacculus and lagena) project to the ventral and caudal nuclei (Gregory, 1972).
HIGHER ORDER AUDITORY AND
LATERAL LINE PATHWAYS
Auditory and lateral line modalities are
presumably represented at all levels of the
brain but anatomical data on the ascending
pathways and connections are available to
a limited extent for only a few species. In
amniotes, first order medullary acoustic
nuclei and a second order cell group, the
superior olivary complex, give rise to
ascending lemnisci that largely terminate
in a midbrain auditory center. This midbrain area projects to an acoustic area
within the dorsal thalamus which in turn
relays this information to pallial and, in
some cases, striatal areas of the telencephalon. The nuclei which comprise the
central auditory pathways are considered
homologous among the three vertebrate
amniote classes. The frog is the only anamniote in which auditory pathways to the
telencephalic level are known (Northcutt,
1980). Electroreceptive and mechanoreceptive lateral line pathways to mesencephalic levels are known among elasmobranchs and some teleosts (Knudsen, 1977;
Bell, 19816; Carr et ai, 1981; Braford,
1982; Finger, 1982; Maler et ai, 1982) and
there is some information concerning these
pathways beyond the midbrain (Braford
and McCormick, 1979; Finger, 1980: Carr
et ai, 1981; Boord and Northcutt, 1982:
Finger and Bullock, 1982; Schweitzer,
1982).
Boord and Northcutt (1982) show in the
clearnose skate that efferents from the
electroreceptive dorsal nucleus and
mechanoreceptive medial nucleus form
separate channels en route to the torus
semicircularis of the midbrain, where they
terminate within separate nuclei of a lateral mesencephalic nuclear complex (Fig.
1). This complex includes lateral, dorsomedial, and ventromedial subdivisions; the
lateral and dorsomedial subdivisions are
electrosensory and mechanosensory,
770
R. L. BOORD AND C. A. McCORMICK
respectively. The ventromedial subdivision, on the basis of deoxyglucose metabolism and physiological evidence (Bullock
and Corwin, 1979; Corwin and Northcutt,
1982), is presumed to be auditory but the
ascending projections from medullary
octaval nuclei have not yet been studied.
In the teleost Cyprinus, however, the auditory division of the torus semicircularis
receives a bilateral projection from the
anterior octaval nucleus. A diencephalic
nucleus which presumably receives input
from this toral area has been studied electrophysiologically (Echteler, 1981, 1982).
An elasmobranch homologue of the auditory portion of the midbrain of other
anamniotes and of amniotes remains to be
discovered. The elasmobranch mechanosensory dorsomedial nucleus is considered
homologous to the mechanosensory portion of the torus semicircularis of bony
fishes, but the lateral nucleus of elasmobranchs is not homologous to the toral
electrosensory zone of electroreceptive
teleosts because electroreception was
apparently re-evolved independently in
teleosts (Boord and Northcutt, 1982).
The thalamus of elasmobranchs, like its
counterpart in tetrapods, relays a variety
of sensory inputs to the telencephalon
(Schroeder and Ebbesson, 1974; Luiten,
1981). Electrosensory, acoustic, and visual
responses have been recorded from
restricted loci within telencephalic regions
of sharks and rays (Platt et ai, 1974; Bullock and Corwin, 1979). The main target
for ascending electrosensory (and visual)
input in skates is a subdivision of the medial
pallium but the deep layers of the dorsal
pallium (the central nucleus) cannot be
excluded. The source of electrosensory
input to these pallia appears to be the lateral posterior thalamic nucleus (Bodznick
and Northcutt, 1984) which receives an
input from the electrosensory lateral mesencephalic nucleus. Lateral line mechanosensory pathways to the telencephalon have
not been demonstrated in sharks or skates
but in a teleost (catfish, Ictalurus) Finger
(1980) shows that a ventral thalamic zone
relays mechanosensory information to a
central pallial nucleus of the telencephalon.
The organization of the higher order
auditory pathways of frogs and amniotes is
similar. Portions of the anuran midbrain
torus semicircularis receive an acoustic
input from the medullary dorsal acoustic
nucleus and superior olive. This portion of
the torus projects to a central thalamic
nucleus and auditory information is then
relayed, via the lateral forebrain bundle,
to the ipsilateral striatum and possibly the
medial pallium (Neary, 1974; Kicliter and
Northcutt, 1975; Kicliter, 1979).
CONCLUDING REMARKS
Changes that have occurred during the
evolution of the octavolateralis system in
that phyletic line leading to the amniota
involve the loss of the lateral line mechanoreceptors and electroreceptors and the
appearance of specialized auditory receptors within the inner ear. There is no evidence that the central lateral line centers
and pathways are retained among the
amniotes. However, the otolithic labyrinthine receptors (maculae of the utricle, saccule, and lagena) and macula neglecta of
cartilaginous and bony fishes are retained
in amphibians and amniotes. One or more
of these endorgans has an auditory function among fishes but audition is primarily
subserved by the newly evolved auditory
papillae in amphibians, reptiles, birds and
mammals. A goal of comparative anatomy
is to understand how primitive or earlier
derived central neural pathways have been
altered to accomodate changes in the sensory periphery. How is the variability in
the auditory periphery of fishes and
amphibians reflected in the organization
of the central auditory pathways? While
auditory homologies are reasonably wellestablished among the amniotes, they are
unknown among fishes and between fishes
and amphibians. A piscine primary medullary auditory center has not been
described although the central projections
from individual labyrinthine sense organs
are known for a few fishes; namely a mormyrid (Bell, 1981 a), a cichlid (Meredith and
Butler, 1982), and an elasmobranch (Barry,
1983). It is particularly difficult to delineate auditory projections of fishes because
EVOLUTION OF OCTAVOLATERALIS PATHWAYS
inner ear maculae may function as both
auditory and vestibular receptors (Corwin,
1981; Platt and Popper, 1981). Moreover,
the same receptor may serve a different
role in different fishes. It is believed that
the sacculus and lagena are auditory among
most bony fishes although there are exceptions, e.g., the utricular macula is auditory
in clupeids (Blaxter et al., 1981). The macula neglecta and saccular macula are the
auditory receptors of cartilaginous fishes
(Corwin, 1981) while the lagenar macula
plays a lesser or perhaps no role in audition.
Medullary auditory centers must exist
because the evidence is overwhelming that
fishes have an auditory sense and therefore
the central course and connections of neurons carrying auditory information can be
expected to differ from vestibular neurons.
One anatomical approach that can be used
to identify auditory centers at the level of
the medulla of fishes is to determine the
higher order connections of each of the
primary octaval nuclei. For example, if one
of the octaval nuclei is shown to have second order connections identical or similar
to those of the amphibian dorsal (acoustic)
nucleus, it could be considered either
homologous to the dorsal acoustic nucleus,
or a case of independent evolution of a
similar pathway. Although the auditory
pathways of fishes are currently unknown,
at least three hypotheses can be considered
in comparing the octaval nuclei of fishes
with those of amphibians.
1. The primary auditory nuclei in fish
are homologous to those in amphibians.
This is a possibility even though the auditory endorgans are not identical among
fishes and some of the auditory endorgans
in amphibians have no counterparts in
fishes. This hypothesis can fit a condition
in which one or more of the labyrinthine
sense organs of fishes function solely as an
auditory receptor and project to a primary
acoustic nucleus homologous to the
amphibian dorsal (acoustic) nucleus. The
particular endorgan which functions as an
auditory receptor is irrelevant and may vary
among fishes. In those species such as the
Ostariophysii where the saccular and
lagenar maculae serve as auditory recep-
771
tors (Fay and Popper, 1980), neurons from
these maculae would terminate within a
specialized primary auditory area (which
may include parts of one or more of the
octaval nuclei), whereas fibers from vestibular receptors would have a separate
terminal field. Among those species in
which the utricular macula is auditory,
utricular fibers would terminate within the
same auditory area that receives saccular
and lagenar fibers in other fishes. Regardless of changes at the peripheral level, central structures are conservative and would
receive auditory information over neurons
from different otic endorgans of fishes.
Fibers from the newly evolved auditory
endorgans of amphibians would project to
this same auditory area. The auditory
nucleus of fishes would be homologous to
that of amphibians, and these nuclei would
have similar or identical central connections. This hypothesis could also fit a situation in which some or all of the otolithic
endorgans have both auditory and vestibular functions. The neurons from these
receptors would segregate centrally and
terminate within separate auditory and
vestibular nuclei.
2. The entire octaval cell column of
fishes is a field homologue of the amphibian acoustic and vestibular nuclei; individual octaval nuclei are not comparable
between fishes and amphibians. If the inner
ear maculae of fishes have dual functions,
this could be reflected centrally by the dual
function of the octaval nuclei; there would
be no specialized auditory and vestibular
nuclei in fishes. The amphibian dorsal
nucleus would arise by a reorganization of
the octaval column of fishes. If this is the
case, the efferent projections of each primary octaval nucleus of fishes would be
expected to be similar to both auditory and
vestibular secondary pathways of amphibians.
3. The auditory nuclei in fish are nonhomologous to the dorsal (acoustic) nucleus
of amphibians. According to this view, the
independently evolved auditory receptors
of amphibians would be paralleled by the
appearance of new central auditory pathways. If the labyrinthine endorgans common to fish and amphibians are hypothe-
772
R. L. BOORD AND C. A. McCORMICK
sized to be conservative in their central
connections, then the appearance of new
auditory endorgans in amphibians with
projections separate from those of other
labyrinthine endorgans implies that the
amphibian dorsal (acoustic) nucleus has no
direct counterpart in fishes. It is interesting
to note that in Rana some of the cells of
the ventral and caudal nuclei project to the
mesencephalic torus semicircularis in parallel with the pathway from the dorsal
nucleus (Wilczynski, 1981). If eighth nerve
input to these cells originates from the saccular macula, which is both an auditory and
vestibular receptor (Moffat and Capranica,
1976), this could represent a second
ascending auditory pathway. If the saccular macula offishesalso projects to the torus
semicircularis via a primary octaval nucleus,
it could be concluded that this pathway is
homologous to the saccular pathway of
frogs and not to the pathway from the auditory amphibian and basilar papillae.
A major stumbling block in our understanding of the changes in the central
auditory pathways that occurred during the
fish-amphibian transition is that the octaval
column of amphibians cannot be easily
derived from that of fishes. It is noteworthy that the extant amphibians are believed
to be far removed from the stem amphibians and the organization of their octaval
nuclei may be the result of a series of subsequent specializations. In addition, not
only is there no one-to-one correspondence between the primary octaval nuclei
of fish and amphibians, but these nuclei in
amphibians and reptiles are also not readily
comparable. In light of Lombard's (1980)
suggestion that certain peripheral auditory
structures of the middle ear have evolved
independently in amphibians and reptiles,
it might also be suggested that the differences in organization of the octaval nuclei
in amphibians and reptiles reflect the possibly independent evolution of auditory
endorgans. Clearly, careful studies of the
projections of the individual labyrinthine
endorgans and of the higher order octaval
pathways in fishes, amphibians, and reptiles will provide important clues to the resolution of these questions.
ACKNOWLEDGMENTS
Some of the information contained in
this report was obtained from experiments
supported by PHS grant NS11272 to Robert L. Boord and NSF grant BNS 81-18843
to Catherine A. McCormick.
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