JOURNAL OF MORPHOLOGY 237:213–236 (1998)
Morphology of the Brain and Sense Organs in the Snailfish
Paraliparis devriesi: Neural Convergence and Sensory
Compensation on the Antarctic Shelf
JOSEPH T. EASTMAN1* AND MICHAEL J. LANNOO2
of Biomedical Sciences, College of Osteopathic Medicine,
Ohio University, Athens, Ohio
2Muncie Center for Medical Education, Indiana University School of
Medicine, Ball State University, Muncie, Indiana
1Department
ABSTRACT The Antarctic snailfish Paraliparis devriesi (Liparidae) is an
epibenthic species, inhabiting depths of 500–650 m in McMurdo Sound.
Liparids are the most speciose fish family in the Antarctic Region. We
examine the gross morphology and histology of the sense organs and brain of
P. devriesi and provide a phyletic perspective by comparing this morphology to
that of four scorpaeniforms and of sympatric perciform notothenioids. The
brain has numerous derived features, including well-developed olfactory
lamellae with thick epithelia, large olfactory nerves and bulbs, and large
telencephalic lobes. The retina contains only rods and exhibits a high convergence ratio (82:1). Optic nerves are small and nonpleated. The tectum is
small. The corpus of the cerebellum is large, whereas the valvula is vestigial.
The rhombencephalon and bulbospinal junction are extended and feature
expanded vagal and spinal sensory lobes as well as hypertrophied dorsal
horns and funiculi in the rostral spinal cord. The lower lobes of the pectoral
fins have taste buds and expanded somatosensory innervation. Although the
cephalic lateral line and anterior lateral line nerve are well developed, the
trunk lateral line and posterior lateral line nerve are reduced. Near-field
mechanoreception by trunk neuromasts may have been compromised by the
watery, gelatinous subdermal extracellular matrix employed as a buoyancy
mechanism. The expanded somatosensory input to the pectoral fin may
compensate for the reduction in the trunk lateral line. The brains of P. devriesi
and sympatric notothenioids share well-developed olfactory systems, an enlarged preoptic-hypophyseal axis, and subependymal expansions. Although
the functional significance is unknown, the latter two features are correlated
with habitation of the deep subzero waters of the Antarctic shelf. J. Morphol.
237:213–236, 1998. r 1998 Wiley-Liss, Inc.
KEY WORDS: Liparidae; Paraliparis; Antarctic; brain; evolution
The current sample of fishes subjected to
neuroanatomical analysis is biased toward
laboratory-reared or easily obtainable freshwater species. For example, goldfish (Carassius auratus), European carp (Cyprinus carpio), zebrafish (Danio rerio), channel catfish
(Ictalurus punctatus), and centrarchid sunfishes have been frequently used as model
organisms in neuroanatomical studies (e.g.,
Northcutt and Davis, ’83; Davis and Northcutt, ’83). Brain morphology and the causes
of its variation remain unexplored in numerous higher level taxa (Butler and Hodos,
r 1998 WILEY-LISS, INC.
’96). Because of this bias, general conclusions about brain diversification and evolutionary trends within fishes must be consid-
Contract grant sponsor: NSF; Contract grant number: OPP
94-16870 (to JTE); Contract grant sponsor: NIH; Contract grant
number: NS30702-01 (to MJL).
This work was supported by internal funds from the Ohio
University College of Osteopathic Medicine and Ball State University.
*Correspondence to: Joseph T. Eastman, Dept. of Biomedical
Sciences, College of Osteopathic Medicine, Ohio University, Athens, OH 45701-2979. E-mail: [email protected]
214
J.T. EASTMAN AND M.J. LANNOO
ered provisional until sampling includes
phyletically and ecologically representative
species.
In our previous examination of an ecologically unique group, the perciform notothenioids from coastal Antarctic waters, we suggested that: (1) unlike other well-studied
lineages (Miller and Evans, ’65; Kotrschal
and Junger, ’88; Kotrschal and Palzenberger,
’92; Huber and Rylander, ’92), the overall
pattern of neuronal diversification among
families of the suborder is not tightly correlated with either phyletic position or ecological factors (Eastman and Lannoo, ’95), and
(2) both degree of subependymal expansions
and the size of nuclear regions that project
to the neurohypophysis are correlated with
the habitation of cold water (Lannoo and
Eastman, ’95). We did find several examples
of a phylogenetic effect on brain morphology
within some lower taxonomic units. At the
time of our work, however, the extent of and
relationships among notothenioid families
and subfamilies were not well established,
and this may have obscured the recognition
of higher level phylogenetic effects. More
completely resolved and reliable notothenioid cladograms are now available, and familial relationships have changed (Lecointre et
al., ’97; Ritchie et al., ’97). These developments should enhance future attempts to
interpret notothenioid brain morphology in
a phylogenetic context.
In the present report, we examine the
sense organs and brain morphology of an
Antarctic scorpaeniform, the liparid snailfish Paraliparis devriesi, an epibenthic species from depths of 500–650 m in McMurdo
Sound (Fig. 1). Using this species as a representative of Southern Ocean liparids, we
first compare its neural morphology to the
known neural morphology of four scorpaeniform species. We then use P. devriesi to probe
the generalizations we proposed concerning
the causes of neuronal divergence within the
sympatric but phyletically distinct notothenioids (Eastman and Lannoo, ’95; Lannoo
and Eastman, ’95). Sensory biology has been
particularly well studied in notothenioids
(Macdonald and Montgomery, ’91; Montgomery and Pankhurst, ’97; Montgomery and
Macdonald, ’98).
Unlike notothenioids, which like most perciforms are coastal fishes, Antarctic liparids
are a secondary deep-sea group (Andriashev,
’77) inhabiting the world’s largest living
space—the cold, dark ocean at depths greater
than 200 m (Haedrich, ’96). Although liparids are the major taxonomic element of
the Antarctic ichthyofauna at depths greater
than 500–600 m (Andriashev and Stein, ’98),
their central nervous systems have not been
Fig. 1. Views (A, lateral and B, ventral) of Paraliparis devriesi (SL 5 170 mm) showing overall morphology, eye size, and location of the nostril (arrow) and
cephalic lateral line pores. Neuromasts of the terminal
or suprabranchial pore of the temporal canal above the
gill slit are innervated by the posterior lateral line
nerve. Ventral most pectoral rays are separated as a
lobe; pelvic fins and disk are absent. From Andriashev
(’80), 30.7.
ANTARCTIC SNAILFISH BRAIN
studied. The purpose of the present study is
to examine the gross morphology and histology of the nervous and special sensory systems of Paraliparis devriesi. This population of P. devriesi has the most southerly
distribution of any known liparid, living in
water with an average temperature of
,21.9°C and experiencing a 4-month period
of winter darkness. Our work provides insight into the biology of a species typical of
the scores of other morphologically similar
epibenthic liparids that have successfully
colonized the shelf and upper slope of the
world ocean, especially in the Antarctic Region.
PHYLOGENY, DISTRIBUTION, AND ECOLOGY
OF THE LIPARIDAE
The Liparidae has a worldwide distribution with .200 species living from the intertidal zone to depths of 7,000 m (Stein and
Andriashev, ’90; Nelson, ’94; Andriashev and
Stein, ’98). Liparids are included in the actinopterygian order Scorpaeniformes, a predominantly marine group with .1,200 species (Nelson, ’94). The family is monophyletic,
but phyletic relationships among genera are
uncertain (Kido, ’88; Balushkin, ’96). There
is agreement that liparids have diversified
away from ancestral inshore benthic habitats to deeper water column niches. Paraliparis is a phyletically derived deep-water
genus exemplifying this trend (Andriashev
and Stein, ’98). Because liparids lack a swim
bladder, habitation of the water column has
involved reduction and loss of bone, replacement of bone by cartilage, and loss of the
pelvic fins or disk (Burke, ’30; Stein, ’78;
Andriashev, ’86; Kido, ’88). An additional
modification of density, conferring neutral
buoyancy on P. devriesi and probably many
other liparids, involves expansion of a watery, gelatinous subdermal extracellular matrix (Eastman et al., ’94; Jung et al., ’95).
Liparids are best represented in polar waters and probably originated and radiated in
the North Pacific Region with subsequent
dispersal southward along the western coast
of the Americas (Andriashev, ’86, ’91). Liparids are one of the few fish families having
both boreal and austral centers of species
diversity (Stein et al., ’91). In the 200–2,000
m-deep waters of the Antarctic Region, liparids underwent a radiation complementing the shallow water radiation of perciform
notothenioids (Andriashev and Stein, ’98).
The 64 known Antarctic liparids, mostly
215
members of the genera Paraliparis and Careproctus (Andriashev and Stein, ’98), represent 31% of the 208 species of benthic fishes
from the continental shelf and upper slope of
the Antarctic Region. With the description of
these new species subsequent to the publication of recent works on Antarctic fishes (Gon
and Heemstra, ’90; Eastman, ’93), the Liparidae has surpassed the endemic Nototheniidae as the most speciose fish family in the
Antarctic Region.
MATERIALS AND METHODS
Collection of specimens
Fieldwork and fixation of specimens and
tissues were conducted at the U.S. McMurdo
Station (77° 518 S, 166° 408 E) on Ross Island
in the southwestern Ross Sea. We captured
Paraliparis devriesi (Andriashev, ’80) in the
Erebus Basin of McMurdo Sound during November 1978, 1991, 1992, and 1994. The
collection site (77° 478 2134 S, 166° 098 5400
E-GPS coordinates) was ,22 km from McMurdo Station. Paraliparis were taken in
large, conical wiremesh bottom traps fished
at a depth of 635 m through holes drilled in
the annual sea ice. The traps were baited
with chopped fish, left on the bottom for 3–5
days, and retrieved with an oceanographic
winch. The bait attracted numerous scavenging amphipods and P. devriesi. We obtained
27 specimens that we used in studying various aspects of the biology of P. devriesi (Eastman et al., ’94; Jung et al., ’95). We used 12
of these specimens for the present study of
brain and sense organ morphology. Both
males and females were included in the sample, and all were adults averaging 179 mm
TL (63 mm SEM) and 64.9 gm (63.79 gm
SEM).
Microscopy
We obtained brains for gross morphology
and histology from specimens that had been
fixed by immersion in 10% formalin and
stored in 70% ethanol. Brains were dehydrated in alcohol, cleared in Hemo-De, and
embedded in paraffin according to standard
procedures. We cut 10–12 µm thick transverse and longitudinal sections that were
stained with 0.1% aqueous cresyl violet acetate. Other paraffin sections were stained
with Bodian’s Protargol or with hematoxylin
and phloxine. We stained the entire olfactory sac with cresyl violet acetate and then
destained with acid alcohol. The resulting
metachromasia facilitated the camera lu-
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J.T. EASTMAN AND M.J. LANNOO
cida illustrations of the innervation pattern
of the lamellae.
For light microscopy, we prepared samples
of eye, olfactory apparatus, skin of the lips,
oral and branchial cavities, pectoral fin, and
trunk. These were fixed in Bouin’s solution,
embedded in paraffin, sectioned at 7 µm,
and stained using a variety of methods
(Luna, ’68; Humason, ’79). We used Mayer’s
hematoxylin and phloxine for general tissue
structure, periodic acid-Schiff-Alcian blue
(PAS-AB) at pH 2.5 and 1.0 for nonsulfated
and sulfated glycosaminoglycans, Gomori’s
aldehyde fuchsin for elastic fibers and Gomori’s trichrome and Mallory’s phosphotungstic
acid hematoxylin for connective tissue. Bodian’s Protargol (Clarke, ’81) was effective in
staining neurons in the olfactory epithelium
when slides were incubated for 24 h at 50°C.
We used an ocular reticle in a compound
microscope to obtain cell counts for calculating a convergence ratio in the central retina.
We counted the number of nuclei in a field
100 µm in length in each of three different
Bodian-stained sections from one individual.
The convergence ratio (number of visual
cells:number of ganglion cells) was expressed
as the average of these counts.
We viewed and photographed sections using either a Nikon SMZ-U dissecting microscope or a Jenalumar compound microscope.
Cell sizes were measured using an ocular
micrometer. Photographs were taken using
Kodak T-Max 100 black-and-white film. Terminology for brain areas follows Nieuwenhuys (’82), Northcutt and Davis (’83), Davis
and Northcutt (’83) as followed by Eastman
and Lannoo (’95), and from Wullimann et al.
(’96). Terminology for the spino-occipital and
spinal nerves is based on Parenti and Song
(’96).
RESULTS
Initial examination of gross brain morphology (Fig. 2) of Paraliparis devriesi revealed
several distinctive features including an
elongate brain, large olfactory nerves,
stalked telencephalic lobes, small optic
nerves and tectum, small diencephalic inferior lobes, a large pituitary and saccus vasculosus, a large corpus cerebellum, and an
extended rhombencephalon with evidence of
extensive sensory input. To interpret this
morphology we conducted a histological examination of both the sense organs and the
brain.
Sensory systems
Olfactory apparatus
The nasal cavities have a single pore-like
narial opening (Fig. 1A) and a well-developed accessory nasal sac venterolateral to
the main cavity (Fig. 3). The oval olfactory
rosette is arranged as a series of 11–12 primary lamellae originating from a central
raphe (Figs. 3, 4A). There are no secondary
lamellae. The posteriormost three or four
lamellae share a common stem. This pattern, type G in the classification of Yamamoto (’82), is typical of scorpaeniforms and a
variety of other teleosts. There is no sexual
dimorphism in the size of the olfactory apparatus and associated brain regions as in
some midwater and bathypelagic fishes
(Marshall, ’79).
The pseudostratified columnar olfactory
epithelium is composed of 7–9 cell layers.
Our sample measured 100 µm (Fig. 4C),
exceptionally thick for teleosts (Yamamoto,
’82). The epithelium thins to ,25 µm near
the tips of the lamellae. This epithelium
consists of three cell types: basal, sustentacular, and olfactory sensory. Silver staining
identified the sensory cells as bipolar neurons possessing thin (1–2 µm) apical dendrites ,30 µm long (Fig. 4C–E). Cilia are
evident, but we could not determine whether
these were associated with the distal end of
dendrites or with nonsensory columnar epithelial cells. The nuclei of sensory neurons
were difficult to distinguish from those of
the numerous sustentacular cells, but were
occasionally evident because of their characteristic large nucleus with a single dark
nucleolus. Nonsensory and sensory areas of
the epithelium could not be distinguished as
the neurons are distributed along the sides
of the lamellae and in the trough between
adjacent lamellae. In the lamina propria
beneath the basal lamina, axons of the sensory neurons form fascicles of the olfactory
nerve. The pattern of branching of the fascicles of the olfactory nerve into the lamina
propria of the lamellae is illustrated in Figure 3.
Vision
The eyes (Fig. 1A) are unremarkable in
external morphology and size (four times in
head length), but on dissection the optic
nerve (275 µm diameter) and extrinsic eye
muscles were extremely small. The pupil is
spherical. Accessory vascular structures such
as a choroid rete are absent. The central
ANTARCTIC SNAILFISH BRAIN
217
Fig. 2. Brain of Paraliparis devriesi (TL 5 180 mm)
in (A) dorsal, (B) left lateral, and (C) ventral views.
35.7. AC, anterior commissure; CC, crista cerebellaris
of the rhombencephalon; CCb, corpus division of the
cerebellum; EG, eminentia granularis division of the
cerebellum; Ha, habenula; IL, inferior lobe of diencephalon; LLant, anterior lateral line nerve; LLpost, posterior
lateral line nerve; OB, olfactory bulb; nP, preoptic
nucleus; Pit, pituitary gland; SN1, first spinal nerve;
SN2, second spinal nerve; SON, spino-occipital nerve;
Sps, spinal sensory nucleus; SV, saccus vasculosus; Tec,
tectum of the mesencephalon; Tel; telencephalon; I, olfactory nerve; II, optic nerve; III, oculomotor nerve; IV,
trochlear nerve; V, trigeminal nerve; VI, abducens nerve;
VII, facial nerve; VIII, auditory/vestibular nerve; IX,
glossopharyngeal nerve; X, vagus nerve; Xs, visceral
sensory division of the vagus nerve.
retina is thin, measuring 150–175 µm. The
visual cell layer consists of a single type of
photoreceptor (Fig. 4F,G). Using the criteria
of Nicol (’89, p. 88), we identified these as
rods. They possess elongate myoids and long
(63–75 µm), thin cylindrical outer segments.
The visual cell layer is 50–57% of the retinal
thickness, a percentage closer to that seen in
deep-sea fishes than in diurnal coastal fishes
(Locket, ’75). There are few bipolar and ganglion cells (Fig. 4G) and the convergence
ratio (number of visual cells:number of ganglion cells) is 82:1. The retinal pigment epithelium is thin and compact suggesting limited retinomotor movement.
Taste buds
We conducted a histological survey of the
skin of the oral cavity and trunk to document the location of taste buds. There are a
few taste buds on the upper lip and in the
skin over the gill arches and a moderate
number of buds on the lower lip. The only
taste buds not associated with the oral cavity
are located on the long, separated rays of the
lower lobe of the pectoral fin (Figs. 1B, 4B).
Lateral line system
The cephalic lateral line system of Paraliparis is well developed (Fig. 1) and docu-
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J.T. EASTMAN AND M.J. LANNOO
Fig. 3. Olfactory sac and lamellae of Paraliparis
devriesi. A: Dorsolateral view of right olfactory sac showing arrangement of typical 12 lamellae and the darkly
stippled accessory nasal sac extending ventrally from
the lateral aspect of the floor of the sac. Part of the roof of
the sac has been removed. 310. B: Dorsal view of the
branching pattern of distal olfactory nerve into bases of
olfactory lamellae. Nerves and lamellae were differentiated by gross staining with cresyl violet acetate. 332.
ANTARCTIC SNAILFISH BRAIN
mented in Burke (’30), Andriashev (’86), and
Stein and Andriashev (’90). The trunk lateral line system is reduced to a single suprabranchial pore above the gill slit (Burke,
’30). Balushkin (’96, p. 284) suggests that
this is actually a large superficial neuromast
of the trunk lateral line. This pore is supplied by the posterior lateral line nerve,
which is smaller in size than the anterior
lateral line nerve.
Somatosensation
In Paraliparis devriesi, free nerve endings
have been observed in the gelatinous subdermal extracellular matrix (Eastman et al.,
’94). In general, the somatosensory system
of fishes is not well known (Atema et al., ’88).
The thickest nerve fibers identified from the
skin of fishes have a diameter of no more
than 1 µm. Free nerve endings in the skin
are thought to mediate touch, temperature,
and proprioceptive sensations (Harder, ’75;
Whitear, ’71, ’86a,b).
Gross description of brain and
cranial nerves
The following description is based on a
specimen designated PDE 15 (170 mm TL;
weight 52.0 g). The brain length was 11,000
µm overall (rostral olfactory bulb to the obex)
and 9,800 µm from the rostral telencephalon
to the obex. Measurements are given below
(see Histology).
Dorsal view
The telencephalon appears ‘‘stalked’’ by
the unique morphology of elongated preoptic
peduncles and a foreshortened tectum (Fig.
2A). The telencephalic lobes (Tel) are large,
extending more laterally than the tectal lobes
(Tec). The preoptic peduncles (nP) have pronounced lobes on their dorsomedial surfaces. The pineal gland (P) is large. The
corpus cerebellum (CCb) is large, is especially wide, and is the largest structure visible on the dorsal surface. The crista cerebellares (CC) are pronounced. The fourth
ventricle is wide rostrally but tapers down
quickly as vagal sensory lobes (Xs) fill the
floor caudally. The obex is obscured by a
large dorsal decussation of the spinal sensory nucleus (Sps). More caudally and bilaterally, Sps nuclei are unusually large and
form prominent bulges (Fig. 2A,B). Along
the dorsal spinal cord to at least the level of
the second spinal nerve, Sps nuclei are
prominent and together form a pronounced
dorsal midline slit.
219
Lateral view
In lateral view (Fig. 2B) the telencephalic
lobes (Tel) form the largest structures. The
pituitary (Pit) is large, as is the saccus vasculosus (SV). The optic nerves (II) cross, with
the right optic nerve, destined for the left
eye, located dorsally. The tectum (Tec) is
relatively small, about the size of the inferior lobes (IL). The corpus cerebellum (CCb)
is the most dorsal structure in this brain but
forms a low, flat lobe compared to its appearance in most other fishes. The lobe of the
corpus is smooth, without externally visible
bends or lobules. The crista cerebellares (CC)
form large prominences rostrally but not
caudally. A gap forms in the dorsal profile of
the medulla from the caudal cristae to the
dorsal prominence of Sps.
Ventral view
The most prominent features of the ventral brain (Fig. 2C) are the pituitary (Pit)
and the saccus vasculosus (SV). Both are
relatively large, each about size of the visible portion of the relatively small inferior
lobes (IL).
Cranial and spinal nerves
The cranial nerves exhibit several unusual features (Fig. 2). The olfactory nerve
(CN I) is hypertrophied, the optic nerve (CN
II) is reduced. CNs III, IV, V, VI, VII, VIII,
IX, and X are normal size. The anterior
lateral line nerve (LL, ant) is larger than the
posterior lateral line nerve (LL, post) and is
the second largest cranial nerve (diameter),
after the olfactory nerve (I).
The spino-occipital nerve consists of two
dorsal and three ventral roots (Fig. 2B). As
verified by dissection, this nerve and the
first and second spinal nerves provide sensory and motor innervation of the pectoral
fin. Distal to the spino-occipital ganglion, an
anterior branch of the spino-occipital nerve
joins with the pectoral branch to the ramus
lateralis accessorius (Freihofer, ’63), which
provides taste fibers to the pectoral fin. This
pattern of union is identical to that in Liparis florae (Freihofer, ’63, p. 183).
Histology
Parasagittal sections
The following descriptions were made using a series of parasagittal sections from a
specimen designated PDE 21 (168 mm TL;
weight 57.3 g). A second specimen, PDE 16,
was also examined (167 mm TL; weight 38.3
220
J.T. EASTMAN AND M.J. LANNOO
Figure 4
ANTARCTIC SNAILFISH BRAIN
221
Fig. 5. Parasagittal section of the brain of Paraliparis devriesi taken from near the midline. x11 CCb,
corpus division of the cerebellum; OB, olfactory bulb;
ON, optic nerve; nP, preoptic nucleus; P, pineal gland;
Pit, pituitary gland; Sps, spinal sensory nucleus; SV,
saccus vasculosus; Tec, tectum of the mesencephalon;
Tel; telencephalon; Xs, visceral sensory division of the
vagus nerve.
g). Of the four parasagittal sections chosen
from PDE 21 for detailed examination, the
most lateral section was in a plane near the
lateral edge of the pituitary. The second section chosen was halfway between the first
section and the midline. The third section
was halfway between the previous section
and the midline. This off-midline section is
illustrated (Figure 5). The fourth section
chosen was near the midline. In these sections the total length from the tip of the
telencephalon to the spinal cord is between
9,000 µm (lateral) and 10,800 µm (medial).
Olfactory Bulb (OB). The olfactory bulb
is ,2,000 µm long (rostrocaudally) and sessile, located at the rostrocaudal edge of the
telencephalon. Histologically, this nucleus is
laminated with the usual four layers present (internal cellular layer [ICL], superficial
olfactory fiber layer [SOL], external cellular
layer [ECL], and glomerular layer [GL]) (Fig.
5). The internal cellular layer consists of
spherical cells uniformly sized (7–9 µm).
Telencephalon (Tel). The bilateral lobes
of the telencephalon are relatively large
(length ,2,000 µm, depth ,1,400 µm). The
telencephalon is positioned at the end of a
preoptic peduncle and is therefore located a
distance (750–1,100 µm) from the tectum.
The telencephalic hemispheres are shallow
(,1,000 µm) and ellipsoid, with rostral and
caudal regions being shallower than the central region. Within the telencephalon, neuronal cell soma tend to be sparse, but neurons
are dense in the transition between the dorsal and ventral divisions and in the rostral
portion of the ventral division. The neurons
are primarily spherical, ranging in size from
7–10 µm. There is no obvious cellular hypertrophy within the telencephalic nuclei.
Pineal (P). The pineal organ is large
(,300 µm long 3 300 µm high) and positioned caudal to an elaboration of the tela
choroidea, which is ,300 µm long and 200
Fig. 4. Histological sections of sense organs of Paraliparis devriesi. A: Primary lamella of olfactory rosette
showing thick olfactory epithelium, transition to nonolfactory epithelium (arrowheads) and lamina propria
forming core of lamella. Hematoxylin and phloxine. 353.
B: Taste bud in skin of lower lobe of pectoral fin. Hematoxylin and phloxine. 3510. C: Olfactory epithelium and
olfactory neurons (arrowheads). Bodian’s Protargol.
3510. D and E: High magnifications of olfactory neurons demonstrated by silver staining of neurofibrils.
Although the dendrite and cell body of these bipolar
neurons are apparent, the axon does not stain. Bodian’s
Protargol. 31,635. F and G: Low and high magnifications of retina showing photoreceptor layer consisting
exclusively of rods with long outer segments. Hematoxylin and phloxine. 3260 and 3510. 1, retinal pigment
epithelium; 2, outer segments of rods; 3, inner segments
of rods; 4, external nuclear layer; 5, internal nuclear
layer; 6, ganglion cell layer.
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J.T. EASTMAN AND M.J. LANNOO
µm high. Pinealocytes are spherical, uniform in size, small (5 µm), and cluster peripherally.
Preoptic Region (nP). At the preoptic peduncle, the forebrain bundles appear as rostrocaudally directed fibers. Optic nerve fibers run from rostral ventral to caudal dorsal
and form the rostral surface of this exposed
diencephalic region. Laterally, the preoptic
region is thick (500 µm deep) and composed
of an area sparsely populated by cells. Medially, the dorsal portion of the central half of
the preoptic peduncle is composed of large
(30–40 µm) preoptic nucleus pars gigantocellularis (nPg) neurons. These neurons exhibit substantial preservation artifacts and
were undoubtedly larger in life. This nPg
cell cluster is interrupted in two areas by
fiber bundles running rostrodorsally to caudoventrally. One bundle is positioned rostroventrally, the other caudodorsally. Ventrally
adjacent to the nPg cell cluster is a thin
layer of small (10 µm), preoptic nucleus pars
parvocellularis (nPp) neurons. Ventral to this
region is a thicker layer of smaller (7–9 µm)
nPp neurons.
Medially, the total length (,600 µm) of
the preoptic peduncle is composed of neurons (Fig. 5). The rostral portion of this
region is composed of nPp neurons. The caudal portion is composed of larger (12–20 µm)
nPm (preoptic nucleus pars magnocellularis) neurons. The dorsal portion of this
caudal region contains a small number of
nPg neurons.
Pituitary (Pit). The pituitary is large
(1,100 µm long, 500 µm deep), about as large
as the inferior lobes. The caudal edge of the
pituitary is positioned near the rostral edge
of the saccus vasculosus. Cells within the
pituitary are small (3–6 µm), spherical, similar in size to both the adenohypophysis and
neurohypophysis, and cluster along the surface of this organ. Cells (epithelial) of the
adenohypophysis are most numerous.
Inferior Lobes (IL). The inferior lobes are
relatively small (length ,1,300 µm) and shallow (between 500 and 900 µm). Within each
lobe, three ventricular lumina are present,
consisting of portions of the lateral recess
and a diverticulum of the caudal recess.
Saccus Vasculosus (SV). The saccus vasculosus is relatively large (1,300 µm long,
800 µm deep) and equals in area the inferior
lobes. The saccus contains coronet cells that
are medium size (6–8 µm in diameter).
Tectum (Tec). The tectum is small (length
,1,500 µm long, 600 µm high). The laminae
described by Northcutt (’83) and Butler (’92)
for other teleosts (from central to peripheral
the periventricular gray zone, deep white
zone, central zone, and superficial white and
gray zone) are present. Cells within the periventricular gray zone are medium size (7–10
µm), dense, and spherical. Within the remaining migrated laminae, cells are sparse,
medium size, and either spherical or fusiform shaped.
Torus Semicircularis (TS). The torus
semicircularis is moderately sized (length
,800 µm). The cells of this midbrain relay
nucleus are spherical and medium size (7–10
µm), similar in size to tectal cells.
Cerebellum. The valvula cerebellum
(VCb) is extremely small (,200 µm long and
250 µm deep). The valvula is represented by
a small dorsal upturning, which consists of a
continuation of the molecular layer of the
corpus, and a small rostrally and ventrally
positioned granular cell layer.
The corpus cerebellum (CCb) is large
(2,500 µm long, 1,500 µm deep), dorsally
positioned, and caudally directed. Granule
cells are spherical and small (3–5 µm). Purkinje and/or eurydendroid cells are larger
(14–18 µm). A transverse sulcus along the
ventrocaudal surface produces a major and
a minor lobe.
The eminentia granularis (EG) forms a
large group of cells (,400 µm 3 400 µm)
located ventral to the molecular layer of the
CCb. Efferent EG fibers, the crista cerebellares (CC), are short (,1,900 µm) and end
abruptly at the middle medullary level.
Medulla. The medulla is ,1,750 µm
deep. Dorsally, it consists of two distinct
neuropils, one rostral, the other caudal. The
rostral neuropil is elongate (,1,500 µm long
and 800 µm deep) and forms the vagal sensory lobe (Xs). The caudal neuropil is larger
(1,500 µm long, 1,800 µm deep), globose, and
more dorsally positioned. This neuropil is
the spinal sensory nucleus (Sps).
In the ventral medulla, medium size
(10–12 µm) motor neurons of cranial nerves
V and VII are present. More caudally, vagal
motor neurons are positioned ventral and
caudal to Xs. More medially, medium-size
(12–18 µm), spherical to fusiform shaped
neurons are present. These neurons are
likely efferent octavolateralis cells.
ANTARCTIC SNAILFISH BRAIN
Within the caudal medulla, the fourth ventricle is ,800 µm deep. The Sps neuropil is
present and continues into the spinal cord.
Caudal to fourth ventricle, the Sps neuropil
is ,1,000 µm deep (compared to a total
brainstem depth of ,1,300 µm).
Spinal Cord. The spinal cord is ,1,000
µm deep. It contains a prominent Sps that
extends through at least the rostral (S2, 3
level) cord.
Transverse sections
The following descriptions were made using 28 transverse sections from the brain of
PDE 23 (160 mm TL, weight 26.8 g). Fourteen of these transverse sections are illustrated (Figs. 6–9), and were chosen for the
morphological features they demonstrated,
rather than according to predetermined intervals.
Olfactory Bulb (OB). The olfactory bulb
is kidney shaped, concave medially, and
wider dorsally than ventrally. As detailed
above and delimited here, the usual four
concentric layers are present (Fig. 6A).
Telencephalon (Tel). In the rostral telencephalon the medial, dorsal, lateral, and central nuclei of the dorsal telencephalon (Dm,
Dd, Dl, and Dc, respectively) are present
(not shown, see Fig. 6B). The Dm borders
the medial and dorsal medial surfaces of the
telencephalon and consists of small cells,
less dense along the medial surface, and
more dense dorsally; cells are denser than in
the laterally adjacent Dd. The sulcus ypsiloniformes, which separates the Dm from the
Dd in most teleosts, is reduced or absent in
this species. The Dd comprises the dorsalmost telencephalon and consists of small
cells. The Dl consists of a thick layer of small
cells that forms the lateral border of the
telencephalon. The Dd and the Dl are composed of cell clusters arranged in a number
(,10) of concentric rows that parallel the
surface of the telencephalon. The Dc occupies the center of the telencephalon and
consists of irregularly arranged small cells.
In addition to the dorsal nucleus of the
ventral telencephalon (Vd), the ventral and
lateral nuclei of the ventral telencephalon
are also present (Vv and Vl, respectively).
The Vd is composed of a dense cluster of
small cells; cells are most dense near the
ventricle and scatter laterally. The Vv consists of small, densely clustered cells positioned along the ventricle, ventral to the Vd.
223
The Vl is composed of two portions, a medial
portion positioned along the ventromedial
surface of the telencephalon laterally adjacent to the Vv, and a lateral portion positioned along the lateral surface of the ventral telencephalon.
In the dorsal portion of the midtelencephalon (Fig. 6B), the Dm, Dd, Dc, and Dl and the
posterior nucleus of the dorsal telencephalon (Dp) are present. At this transverse level,
cells of the Dm are arranged in rows oriented in concentric lines parallel to the dorsomedial surface of the telencephalon. The
ventromedialmost portion of the Dm consists of larger cells (10 µm) without obvious
orientation. The Dc consists of two recognizable portions, a dorsolateral cluster of small,
scattered cells, and a ventromedial cluster of
more darkly staining cells. The Dp consists
of larger, darkly staining cells arranged in
concentric rows, fewer rows (#6) than are
present in the rostral Dl.
In the ventral portion of the midtelencephalon (Fig. 6B), the Vd and Vv are present. The Vd is smaller than at more rostral
levels. The Vv is less dense at this level than
at rostral levels. The central nucleus of the
ventral telencephalon (Vc; not shown) is
small and present in sections between this
level and the rostrally adjacent level described above. In the lateral portion of the
ventral telencephalon, the endopeduncular
nucleus (E) consists of a loose cluster of
darkly staining cells.
In the posterior telencephalon at the level
of the anterior commissure, the dorsal telencephalon is represented primarily by the Dp,
with caudal portions of the Dm and Dd present dorsomedially, and the caudalmost Dc
present centrally. The ventral telencephalon
is represented by the caudal portion of the
Vv, positioned immediately dorsal to the anterior commissure (AC).
Remnants of the Dp are visible dorsolaterally at the telencephalic-diencephalon junction (Fig. 6C). At this level, the medial and
lateral forebrain bundles (MFB and LFB,
respectively; present on either side of the
endopeduncular nucleus) are present and
large.
Preoptic area. Rostrally, the parvocellular preoptic nucleus (nPp) is present along
the central and ventral medial surface (Fig.
6C). More caudally, the nPp is situated ventral to the large cells of the magnocellular
preoptic nucleus (nPm), which in turn is
positioned ventral to the larger cells of the
224
J.T. EASTMAN AND M.J. LANNOO
Figure 6
ANTARCTIC SNAILFISH BRAIN
gigantocellular preoptic nucleus (nPg; Fig.
6D). Farther caudally, the nPp and nPg are
present (Fig. 6E).
Thalamus. The most rostral portion of
thalamus consists of the ventral thalamus
(ventromedial nucleus, VM; Fig. 6E). In the
dorsal thalamus, the dorsal portion of diencephalic ventricle opens and, therefore, the
cell orientation away from the ventricle is in
a ventral rather than the usual lateral direction (Fig. 6E). The dorsal thalamus consists
of the nucleus A rostrally and the central
posterior nucleus (CP) caudally (not shown);
these nuclei form a lobe that projects into
the diencephalic ventricle. Nucleus A consists of small but variably sized cells (4–8
µm); the CP is composed of cells 6–12 µm,
with the larger cells positioned laterally. In
the caudal portion of the ventral thalamus,
the VM contains cells 8–15 µm in diameter.
Hypothalamus. The rostral portion of the
ventral hypothalamic nucleus (Hv) is positioned ventral to the preoptic area (Fig. 6E).
Cells of the dorsal hypothalamic nucleus
(Hd) spread laterally, where they surround
the lateral recess (LR) of the inferior lobe
(IL). The inferior lobes are small. The ventral surface of the rostral IL contains a dense
cluster of small cells that we refer to as the
lateral nucleus of the hypothalamus (LH);
these cells are medium in size (6–8 µm) and
form a lobule. Within the IL of the hypothalamus, the Hd is present along the LR, the LH
continues to form a lobe, and medium-size (6
µm) cells of the nucleus diffusus (ND) are
present along the lateral margin (Fig. 7A).
Fig. 6. Transverse sections through the brain of
Paraliparis devriesi from the olfactory bulb (A) to the
diencephalon (E). 340. Dc, dorsal central subdivision of
the telencephalon; Dd, dorsal dorsal subdivision of
the telencephalon; Dl, dorsal lateral subdivision of the
telencephalon; Dm, dorsal medial subdivision of the
telencephalon; Dp, dorsal posterior subdivision of
the telencephalon; E, entopeduncular nucleus of the
telencephalon; ECL, external cellular layer of the olfactory bulb; Gl, glomerular layer of the olfactory bulb; Hv,
ventral division of the periventricular hypothalamic region; ICL, internal cellular layer of the olfactory bulb;
nLT, lateral tuberal nucleus; nPg, gigantocellular region
of the preoptic nucleus; nPm, magnocellular region of
preoptic nucleus; nPp, parvocellular region of preoptic
nucleus; nPT, posterior tuberal nucleus; Pit, pituitary
gland; PG, preglomerular complex of the diencephalon;
SC, suprachiasmatic nucleus; SOF, superficial olfactory
fiber layer of the olfactory bulb; Vd, dorsal subdivision of
the ventral telencephalon; VM, ventromedial nucleus of
the thalamus; Vv, ventral subdivision of the ventral
telencephalon.
225
Other diencephalic structures. The suprachiasmatic nucleus (SC) consists of small
cells (3–7 µm) positioned lateral to the nPp
(Fig. 6D). The medial and lateral forebrain
bundles (MFB and LFB, respectively) are
large. The MFB is prominent along the ventricular surface between the preoptic area
(nP) and the ventral thalamus (Fig. 6E). The
LFB forms a lobe lateral to the endopeduncular nucleus (Fig. 6C,D). The few cells of the
lateral tuberal nucleus (nLT) are medium in
size (8–15 µm) and located lateral to the Hv
along the ventral margin of the diencephalon (Fig. 6E). Neurons of the preglomerular
complex (PG) are medium in size (8–10 µm)
and located along the central portion of the
lateral edge of the diencephalon (Fig. 6E).
Smaller (4–6 µm) cells of the posterior tuberculum (TP) line the ventricle between the
VM and the Hd. Centrally, small-to-mediumsize cells (5–7 µm) of the glomerular nucleus
(G) are present (Fig. 7A).
Tectum (Tec) and torus longitudinalis (TL).
The tectum is relatively small, with the dorsal surface flattened caudally (Fig. 7A). The
torus longitudinalis is also small, positioned
along the midline between the bilateral tectal lobes (Fig. 7A).
Torus Semicircularis (TS). The torus
semicircularis forms a moderately sized lobe
extending into the tectal ventricle (not
shown).
Oculomotor Complex. The cell bodies of
oculomotor complex neurons (CN III/IV) are
medium sized (12–18 µm) and are neither
numerous nor prominent (Fig. 7A).
Saccus Vasculosus (SV). The saccus vasculosus forms a prominent ventral midline
structure (Fig. 7A,B). This structure approaches in size one-half the area of the
entire tegmentum.
Cerebellum. The corpus cerebellum
(CCb) is large (Figs. 7B, 8A), occupying an
area larger than the underlying brainstem
(Fig. 7B). The CCb is lobated; the lobe is
caudally directed over fourth ventricle (Fig.
8A). The granule cells of the eminentia
granularis (EG) lie subpially, ventral to the
molecular layer of the CCb. The crista cerebellaris (CC) forms a distinct structure,
capping the medulla dorsolaterally (Fig.
8A,B).
Octavolateralis Region. Aside from the
disparity in size between the anterior and
posterior lateral line nerves, the octavolat-
226
J.T. EASTMAN AND M.J. LANNOO
Fig. 7. Transverse sections through the brain of
Paraliparis devriesi from the rostral mesencephalon (A)
to the isthmus (B). 340. CCb, corpus division of the
cerebellum; G, glomerular complex of the diencephalon;
MLF, medial longitudinal fasciculus; SV, saccus vasculosus; Tec, tectum of the mesencephalon; TL, torus longitudinalis of the mesencephalon; III/IV, mesencephalic oculomotor complex.
ANTARCTIC SNAILFISH BRAIN
Fig. 8. Transverse sections through the brain of
Paraliparis devriesi from the medulla (A) to the bulbospinal junction (C). 340. CC, crista cerebellaris of the
rhombencephalon; CCb, corpus division of the cerebellum; MLF, medial longitudinal fasciculus; MON, medial
227
olfactory nucleus; ON, optic nerve; RF, reticular formation; Vs, spinal sensory division of the trigeminal nerve;
Xm, visceral motor division of the vagus nerve; Xs,
visceral sensory division of the vagus nerve.
228
J.T. EASTMAN AND M.J. LANNOO
eralis region appears to be generalized, without either hypertrophied nuclei or nerves
(Fig. 8A, B).
Other brainstem structures. The spinal
trigeminal tract (Vs) forms prominent lobes
in the caudal medulla (Fig. 8A–C). Internal
arcuate fibers are also prominent (Fig. 8B).
The brainstem motor nuclei that are visible
in our transverse sections include CNs VII,
IX, and X. Centrally, the cell bodies of CN
VII motor neurons extend from dorsomedial
to ventrolateral. The glossopharygeal motor
neurons (IXm) are large (15–18 µm) and
disjunct rostrally from the similarly sized
and extensive neurons in the vagal motor
cluster (Xm; Figs. 8C, 9A,B).
The medial longitudinal fasciculus (MLF)
is present throughout the brainstem (Figs.
7A,B, 8A–C, 9A–D). This tract is extensive
in area, especially in the bulbospinal junction and the rostral spinal cord (Figs. 8C,
9A–D).
Reticular formation (RF) neurons are large
(8–18 µm) and are present throughout the
brainstem (Figs. 8A–C, 9A). They are replaced in the spinal cord by the motor neurons of the ventral horn (Spm; Fig. 9B–D).
Vagal Sensory Lobes (Xs). The vagal sensory lobes are large and form medial lobes
that define the ventrolateral walls of IVth
ventricle (Figs. 8B,C, 9A). The bulk of each
vagal lobe lies rostral to the entrance of the
vagal nerve. Caudally, the Xs lobes meet
along the dorsal midline (Fig. 9A).
Spinal Sensory Nucleus (Sps). The spinal sensory nuclei are large (Fig. 9A–D) and
associated rostrally with a dorsal commissure. Caudally, the Sps and the dorsal funiculi form a large dorsal area (Fig. 9A–D).
Most caudally, the Sps forms lobes that together create a dorsal midline sulcus (Fig.
9C,D).
Interstitial Nucleus of Cajal (nC). This
midline nucleus is present dorsally (Fig. 9B).
Supramedullary Neurons. A number of
large (50 µm) neurons are located dorsomedial to the rostral spinal cord (Fig. 9C). These
neurons resemble the supramedullary neurons (SM) of Bennett et al. (’67). The function of supramedullary neurons is unknown.
DISCUSSION
Neural morphology is the combined result
of persistent phyletic features—those inherited from ancestral species (plesiomorphic in
cladistic terminology), and derived features
(apomorphic in cladistic terminology), and
those established during speciation (cladogenesis). Whereas the brain of Paraliparis
devriesi is unusual, interpretations of the
origins—generalized within the family or
derived with speciation—and causes of this
brain morphology are hindered by the absence of studies of closely related species. To
provide a phyletic perspective regarding the
origin of the brain morphology of P. devriesi,
we first survey the sensory and nervous systems of four species of scorpaeniforms and
then comment on the Antarctic deep-shelf
habitat as it relates to the evolution of liparids and notothenioids.
Comparative neurological studies
of scorpaeniform teleosts
Euteleostean fishes are so numerous that
entire families, even orders, are without neuroanatomical description. For example, a recent compilation contains no mention of the
neuroanatomy of any of the 1,200 scorpaeniforms (Butler and Hodos, ’96). Whereas the
gross brain morphology of scorpaeniforms
has not been previously described, several
aspects of scorpaeniform neuroanatomy have
been investigated (Table 1), including a description of the cranial nerves of the scorpaenid Scorpaena scrofa (Allis, ’09), documentation of the pattern of the ramus lateralis
accessorius in 15 scorpaeniforms (Freihofer,
’63), and studies of the innervation and chemosensory properties of the free pectoral fin
rays in triglids (Finger, ’82; summaries in
Whitear, ’86a and Kotrschal, ’96). Furthermore, several aspects of the brains of the
scorpaenid Sebastiscus marmoratus have
been studied, including the retinal ganglion
cells (Ito and Murakami, ’84), thalamic fiber
connections (Ito et al., ’86), ascending projections of the spinal dorsal horn (Murakami
and Ito, ’85), telencephalic ascending acousticolateral system connections including the
nucleus preglomerulosus (Murakami et al.,
’83), connections of the telencephalon (Murakami et al., ’86), and the telencephalic area
dorsalis pars lateralis (Yamane et al., ’96).
With the exception of observations on the
degenerate retina of a liparid inhabiting waters at a depth of 6,000 m by Munk (’64, ’66),
no work has been conducted on the sensory
and nervous system biology of liparids.
In order to compare a more closely related
species and to provide a basis for the discussion of the neural features in Paraliparis
devriesi, we dissected the brain of the North
Atlantic lumpfish, Cyclopterus lumpus (Table
ANTARCTIC SNAILFISH BRAIN
Fig. 9. Transverse sections through the brain of
Paraliparis devriesi from the bulbospinal junction (A) to
the SN1-SN2 level of the spinal cord (D). 340. MLF,
medial longitudinal fasciculus; nC, interstitial nucleus
229
of Cajal; RF, reticular formation; SM, supramedullary
neurons; Spm, spinal motor nucleus; Sps, spinal sensory
nucleus; Xm, visceral motor division of the vagus nerve;
Xs, visceral sensory division of the vagus nerve.
230
J.T. EASTMAN AND M.J. LANNOO
1), a representative of the family Cyclopteridae. Until recently liparids were placed in
the lumpfish family Cyclopteridae, and it is
likely that cyclopterids and liparids form a
monophyletic group (Nelson, ’94). Cyclopterus lumpus is a sedentary inshore species
with a maximum depth range of a few tens
of meters (Bigelow and Schroeder, ’53). Most
neural features in P. devriesi depart from
the generalized condition (Table 1).
Evolution of liparids and notothenioids
and the Antarctic shelf
Although notothenioids dominate Antarctic shelf habitats ,500 m deep, liparids prevail at midslope depths of 800–1,000 m (Andriashev and Stein, ’98). Antarctic liparids
have a North Pacific origin and have been
considered to be a somewhat younger faunal
element than the indigenous notothenioids
(Andriashev, ’65, ’87; Eastman, ’93). Liparids are hypothesized to have arrived in
the Antarctic as deep-sea migrants during
the Miocene, 25–5 mya. As the fish fauna of
the Antarctic shelf and slope becomes more
completely known, a more complicated chronology is likely (Andriashev and Stein, ’98).
For example, divergence times inferred from
two different classes of molecules suggest
that phyletically derived notothenioid groups
may be younger than previously suspected,
probably diversifying no longer than 15 mya
(Bargelloni et al., ’94; Chen et al., ’97) and
possibly much more recently. Moreover, the
radiation of trematomid nototheniids is estimated to have taken place during the
Pliocene, ,3.4 mya (Ritchie et al., ’96).
Equivalent molecular data are not available
for liparids.
These faunal ages, especially the length of
time in a particular habitat, are important
in evaluating different degrees of adaptation
to a similar environment in unrelated groups
of fishes (Montgomery and Pankhurst, ’97;
TABLE 1. Comparison of the brain of five scorpaeniform teleosts, the generalized Scorpaena scrofa (from Allis, ’09)
in ventral view, the generalized Sebastiscus marmoratus (from Ito et al., ’86; and Murakami et al., ’86), the derived
Prionotus carolinus (from Finger, ’82) in dorsal view, Cyclopterus lumpus (Eastman and Lannoo, unpublished
data) and the derived Antarctic Paraliparis devriesi, in ventral view
Scorpaenidae
Structure
Olfactory nerves
Olfactory bulbs
Telencephalon
Preoptic area
Pituitary
Habenula
Optic nerves
Tectum
Torus semicircularis
Subependymal expansions
Valvula cerebelli
Inferior lobes
Saccus vasculosus
Corpus cerebelli
Medulla
Crista cerebellaris
Lateral line nerves
Vagus
Spino-occipital nerve
Sps
Dorsal funiculus/horn
Scorpaena
scrofa
ø
ø1
ø
ø
ø
—
●3,4
●
—
—
—
ø
ø
—
ø6
—
ø
—
ø9
—
—
Sebastiscus
marmoratus
Triglidae
Prionotus
carolinus
Cyclopteridae
Cyclopterus
lumpus
Liparidae
Paraliparis
devriesi
—
ø1
●2
ø
—
ø
●
●
ø
ø
ø
●
—
●
ø
ø
ø
●
●10
ø
ø
—
—
C
ø
—
—
—
●
—
—
—
—
—
●5
●
—
—
—
—
—
●11
●
●
ø
ø
—
—
●3
ø
—
—
—
ø
ø
ø
ø
●
●8
ø
ø9
ø
ø
●
●1
●
●
●
—
C3
C
C
●
C
C
●
●
●
C7
●8
●
●10
●
●
(Symbols: ø 5 presumed actinopterygian generalized condition; ● 5 structure enlarged or augmented; C 5 structure reduced; — 5 structure not examined).
1Sessile.
2Dl large.
3Right nerve dorsal.
4Pleated.
5Uniformly wide.
6Narrow.
7Caudally truncated.
8Anterior larger.
9One dorsal root, two ventral roots.
10Two dorsal roots, three ventral roots.
11Derived, chemosensory.
ANTARCTIC SNAILFISH BRAIN
Montgomery and Macdonald, ’98). Although
the sensory environment is similar, different
evolutionary time scales, longer by a few
tens of millions of years in the phyletically
basal deep-sea fishes, may account for the
more extreme sensory adaptations in primary deep-sea fishes compared to the more
recently derived notothenioids (Montgomery and Macdonald, ’98) or liparids, which
are a secondary deep-sea group. Given the
current uncertainty about the age of the
Antarctic fish fauna, we will assume that
liparids and notothenioids have occupied the
Antarctic shelf for approximately the same
length of time—10–15 my.
Interpretation of the sensory systems
and brain of Paraliparis devriesi
The gross brain morphology of Paraliparis
devriesi differs in almost every aspect from
that of other scorpaeniforms (Table 1). It
differs from notothenioids as well, and comparisons are detailed below.
Olfaction
Based on the histology of olfactory lamellae and on the size of the olfactory nerves
and bulbs, olfaction appears to be an important sense in Paraliparis devriesi. The olfactory apparatus is also well developed in Cyclopterus lumpus, but not in the more
generalized scorpaenid Scorpaena scrofa. In
P. devriesi, olfaction is likely used for identification of mates in the deep-sea rather than
for locating food (Marshall, ’67). The cephalic lateral line system and possibly taste
are more important in prey detection (see
below).
Vision
The visual system of Paraliparis devriesi
is reduced compared to more generalized
shallow-water scorpaeniforms (Table 1). The
visual system includes a retina consisting
exclusively of rods, a high convergence ratio
of photoreceptors to ganglion cells, a nonpleated optic nerve, a small tectum, and
small extrinsic eye muscles. This morphology is consistent with two environmentally
determined low-light conditions: life at
depths of 500–650 m, and habitation of a
polar region characterized by four months of
darkness.
Most teleosts have both rods and cones in
the visual cell layer of the retina (Nicol, ’89),
as do all Antarctic notothenioids examined
to date (Eastman, ’88). Rods, responsible for
231
vision in dim light, are frequently the only
photoreceptor present in fishes living at
depths of .1,000 m (Munk, ’66; Marshall,
’79; Nicol, ’89). A photoreceptor layer consisting exclusively of rods has also been documented in two species of Comephorus, deepliving (150–1,500 m) cottoid scorpaeniforms
from Lake Baikal, an environment with a
photic regime similar to the deep sea (Pankhurst et al., ’94; Smirnova, ’95). The liparid
Liparis liparis inhabits the intertidal zone
to depths of 300 m (Stein and Able, ’86) and,
unlike Paraliparis devriesi, has cones in its
retina (Munk, ’64, Plate XIII, Fig. 7).
The convergence ratio of Paraliparis devriesi is intermediate between the 58:1 of Dissostichus mawsoni (Eastman, ’88), perhaps
the most scotopic notothenioid, and those of
some deep-sea fishes like Bathylagus in
which ,150 visual cells converge on a single
ganglion cell (Munk, ’66, p. 53). The retina of
P. devriesi shows no indication of degeneration as does the retina of the extremely deepliving (6,660 m) liparid Careproctus kermadecensis (Munk, ’64, ’66).
The presence of only rods and the relatively high convergence ratio (82:1) suggest
enhanced visual sensitivity but with some
compromise in acuity or resolution (Nicol,
’89:125). The retina of Paraliparis devriesi is
intermediate between shallow and deepliving liparids, but is more specialized for
vision under dim light than is the retina of
sympatric notothenioids, a coastal perciform
group.
The functional significance of pleated optic nerves is unknown, but this condition is
thought to be a basal feature of euteleosts
(Northcutt and Wullimann, ’88). The nonpleated optic nerve of Paraliparis devriesi
represents a simplification, perhaps the result of a reduction in numbers of retinal
afferents. Tectal size can also reflect the
number of retinal afferents (Butler, ’92) and
is clearly reduced in P. devriesi.
Taste
Paraliparis devriesi has taste buds on the
long, separated rays of the lower lobe of the
pectoral fin. The shallow-living North Atlantic liparid Liparis inquilinus also has taste
buds in this location (Able and Musick, ’76).
These buds in liparids are innervated by the
pectoral branch of the ramus lateralis accessorius derived from the facial-vagal trunk
(Freihofer, ’63). The heavy innervation pattern and observation of captive specimens
suggest that the liparid pectoral fin, espe-
232
J.T. EASTMAN AND M.J. LANNOO
cially the lower lobe, is an important sensory
surface used in exploring the environment
(Freihofer, ’63; Able and Musick, ’76; Gosline, ’94).
Lateral line mechanoreception
In Paraliparis devriesi, the anterior lateral line nerve, the second largest cranial
nerve, is larger than the posterior lateral
line nerve. This morphology reflects the importance of the cephalic lateral line and the
reduction in the trunk lateral line.
Brain and spinal cord
Compared to more generalized scorpaeniforms, Paraliparis devriesi possesses a relatively large telencephalon, preoptic area, pituitary, subependymal region, medulla,
spino-occipital nerve, spinosensory nucleus,
and dorsal funiculus/dorsal horn (Table 1).
By the same comparison, P. devriesi has a
relatively small torus semicircularis, valvula cerebelli, and crista cerebellaris. Paraliparis devriesi and Cyclopterus lumpus share
relatively large olfactory nerves and bulbs
and a large anterior lateral line nerve. These
features may be synapomorphies of the liparid-cyclopterid clade.
The stalked telencephalon is one of the
most unusual features of the brain of Paraliparis devriesi. This morphology is also known
from chimaeriform fishes (Northcutt, ’78),
where it is the result of a packing problem—
the position and size of the eyes impose
constraints on the neurocranium. This is not
the situation in P. devriesi, where the eyes
are not unusually large, dorsal, nor closely
positioned.
Although Mauthner neurons are generally present in scorpaeniforms (Zottoli, ’78),
among liparids they are present in shallow
water Liparis but absent in deep-water
Paraliparis (Bone and Marshall, ’83). This is
testimony to the derived nature of the genus
Paraliparis and reflects the general trend
toward reduction or loss of these neurons in
anguilliform swimmers and sedentary species.
Some of the derived sensory and neural
features of Paraliparis devriesi are associated with a deep-water habitat. These include: a small optic nerve, only rods in the
photoreceptor layer of the retina, a welldeveloped cephalic lateral line, a large olfactory nerve, a thick olfactory epithelium with
the sensory cells distributed over much of
the surface of the lamellae, a small tectum,
and expanded sensory input to the rhombencephalon. Paraliparis devriesi does not, however, exhibit sense organ and brain specializations characteristic of primary deep-sea
fishes. They do not have tubular eyes, an
extremely elongated body and lateral line,
sexual dimorphism in the size of the olfactory apparatus and telencephalon, hypertrophied octavolateralis system, papillate neuromasts, or photophores (Montgomery and
Pankhurst, ’97; Montgomery and Macdonald, ’98). In this sense P. devriesi is intermediate between the phyletically derived notothenioids, a coastal perciform group with
which it is sympatric in McMurdo Sound,
and the primary or true deep-sea pelagic
fishes that are confined to phyletically basal
(and presumably older) euteleostean superorders (Nelson, ’94; Haedrich, ’96). This is
consistent with differences in the degree of
specialization of the sensory systems between notothenioids and primary deep-sea
fishes (Montgomery and Pankhurst, ’97;
Montgomery and Macdonald, ’98), as well as
with the designation of deeper dwelling liparids as secondary deep-water fishes (Andriashev, ’77).
There are other derived characteristics of
the brain of Paraliparis devriesi that defy
simple explanation: the preoptic-pituitary
hypertrophy and a suite of features that
may be linked to the expanded spinal sensory nucleus (Sps). The hypertrophied preoptic area (nP) of P. devriesi is reminiscent of
the hypertrophied preoptic area in the most
phyletically derived notothenioid species
(Lannoo and Eastman, ’95). The notothenioids with the greatest preoptic hypertrophy
inhabit the coldest (21.9°C) shelf waters
(Lannoo and Eastman, ’95). There is, however, a major difference between notothenioids and liparids. The correlation between
the size of nP and nLT neurons observed in
notothenioids is absent in liparids. In P.
devriesi, nLT consists of a relatively few,
small cells. The causal basis for this relationship between nP and the size of the pituitary
remains an open question and will be difficult to pinpoint. It may be that the same
factors acting to produce preoptic hypertrophy in notothenioids underlie the preoptic
hypertrophy in Paraliparis. Both liparids
and notothenioids have subependymal expansions, and these curious enlargements of
the vascular lacunae of the ventricular lining are correlated with the habitation of
subzero waters.
ANTARCTIC SNAILFISH BRAIN
The second set of features, the expanded
somatosensory region of the rhombencephalon and rostral spinal cord, may be indirectly related to a distinctive somatic feature of Paraliparis devriesi, the presence of
a watery, gelatinous, subdermal extracellular matrix (SECM). The SECM accounts for
one-third of the body weight of P. devriesi
and serves as a buoyancy agent (Eastman et
al., ’94). The SECM in P. devriesi may affect
the performance of epidermally or dermally
positioned neuromast mechanoreceptors. To
function properly, neuromasts require a
stable substrate against which incoming water displacements can be evaluated. In contrast, the SECM is gelatinous and therefore
a less stable substrate than typical hypodermal and muscle tissue. For P. devriesi, body
movement or water motion may create deformation waves in the SECM and skin. Since
the SECM is 97% water (Eastman et al.,
’94), which is nearly incompressible, the
SECM may not be stabilized even at the
500–650 m depths inhabited by P. devriesi.
The ability of neuromasts to detect water
displacements may, therefore, be compromised. Not only do neuromasts function optimally when they are stable relative to the
stimulus, but brains have evolved elaborate
feedback mechanisms to reduce noise interference in octavolateralis systems (Maler and
Mugnaini, ’94; Montgomery and Bodznick,
’94; Montgomery et al., ’95; Janssen, ’96).
We suggest that the extensive SECM in
Paraliparis devriesi may have had consequences for the sensory and neural biology.
The SECM is thickest over the trunk, and
the trunk lateral line is reduced to a single
suprabranchial pore innervated by a small
posterior lateral line nerve. The number and
extent of free neuromasts on the trunk are
unknown. The caudal crista cerebellares, responsible for feedback to the first-order
mechanosensitive nucleus (MON) from the
cerebellar eminentia granulares is also reduced. The torus semicircularis, the secondorder lateral line nucleus, forms a small,
shallow lobe. Loss of trunk canal neuromasts is common; fishes that lack scales,
like P. devriesi, frequently lack trunk lateral
line canals (Coombs et al., ’88). It is noteworthy that in P. devriesi the Sps, a first-order
somatosensory nucleus mediating touch, is
hypertrophied, as are the dorsal horns and
funiculi of the spinal cord. As mentioned
previously, somatosensory input to the pecto-
233
ral fin is expanded, possibly compensating
for the reduction in the trunk lateral line.
How does this information on sensory biology relate to what is known about the epibenthic life of Paraliparis in general and Paraliparis devriesi in particular? There are no
direct observations of P. devriesi swimming
or feeding at depth in McMurdo Sound. They
are attracted to bottom traps baited with
chopped fish, but we do not know whether
they are detecting an odor plume or the
swarms of scavenging amphipods that are
also drawn to the bait. A similar feeding
behavior is seen in Paraliparis bathybius
living at 4,000 m in the North Atlantic. This
species has been classified as a necrophagivore, perhaps chemically attracted to food
falls and the associated amphipods in the
deep ocean (Lampitt et al., ’83; Gartner et
al., ’97). Photographs from submersible vehicles (Wenner, ’79; Lampitt et al., ’83) and
observations of aquarium specimens (Eastman et al., ’94) suggest that neutrally buoyant Paraliparis are inefficient swimmers and
that they drift passively or hover in tidal
currents near the bottom (Lampitt et al.,
’83). The expanded sensory modalities associated with the lower lobe of the pectoral fin
may be involved in the perception of and
orientation to currents as well as in the
exploration of the epibenthic habitat for food.
Finally, how does sense organ and brain
morphology in Paraliparis devriesi compare
with that of sympatric notothenioids, both
groups having occupied the Antarctic shelf
for approximately the same length of time?
The brain of P. devriesi diverges more from
other scorpaeniform brains (see above) than
notothenioid brains diverge from basal perciforms (Eastman and Lannoo, ’95). Furthermore, with reduced reliance on vision, the
well-developed olfactory system, cephalic lateral line, cutaneous taste buds, and hypertrophy of somatosensation to the pectoral fin, P.
devriesi more closely resembles a primary
deep-sea species than does any notothenioid. The olfactory system is also expanded in
some notothenioids. However, this may be
a phylogenetic effect in both groups since
these notothenioids are basal in the suborder, and a liparid outgroup (Cyclopterus lumpus) possesses similar morphology. Other
similarities between brains of P. devriesi and
notothenioids include an enlarged preoptichypophyseal axis and subependymal expansions. Although the functional significance
is unknown, these latter two features are
234
J.T. EASTMAN AND M.J. LANNOO
correlated with habitation of the relatively
deep subzero waters of the Antarctic shelf
(Lannoo and Eastman, ’95).
ACKNOWLEDGMENTS
We thank Danette Pratt for producing the
illustrations, Tim Creamer, Jennifer Jacobberger, and John Sattler for photographic
work, and Susan Johnson Lannoo for providing histological assistance. Art DeVries developed the techniques for successfully trapping Antarctic liparids and aided greatly in
collection of the specimens. David Stein generously provided us with the manuscript of
his forthcoming work on liparid taxonomy
and evolution (Andriashev and Stein, ’98).
We also thank Andrew Bass for identifying
the supramedullary neurons.
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