Download Central projections of the glossopharyngeal and

THE JOURNAL OF COMPARATIVE NEUROLOGY 264~216-230(1987)
Central Projections of the
Glossopharyngeal and Vagal Nerves in the
Channel Catfish, Ictalurus punctatus:
Clues to Differential Processing of Visceral Inputs
JAGMEET S. KANWAL, AND JOHN CAPRI0
Department of Zoology and Physiology, Louisiana State University, Baton Rouge,
Louisiana 70803
ABSTRACT
Transganglionic transport of horseradish peroxidase was used to trace
the pattern of medullary terminations of the glossopharyngeal and vagal
nerve complex in the channel catfish, Ictalurus punctutus. The glossopharyngeal root terminates centrally in the anterior end of the vagal lobe except
for two fascicles that terminate in separate regions of the nucleus intermedius of the facial lobe. Vagal nerve branches innervating regions of the
oropharynx terminate in a n overlapping, segmental fashion throughout the
ipsilateral vagal lobe and the nucleus intermedius of the vagal lobe. The
descending branch of the vagus, innervating the abdominal viscera, terminates in the general visceral nucleus and in the nucleus intermedius of the
vagal lobe. In addition, abdominal visceral fibers decussate through the
commissural nucleus of Cajal and terminate in the general visceral nucleus
of the contralateral side. Efferents included in the oropharyngeal and abdominal branches of the vagus also originate from two morphologically
separable populations of motor neurons.
Key words: medulla, taste, touch, oropharynx, nucleus of the solitary tract
Gustatory information is transmitted to the brain of vertebrates by three pairs of cranial nerves: the facialis (VII),
the glossopharyngeus (IX), and the vagus (XI. In ictalurid
catfish these make up at least two gustatory subsystems
(Herrick, '01,'05; Atema, '71; Finger and Morita, '85a). Facial nerve branches, which innervate primarily the taste
buds located on the external body surface, together with
their central projections constitute the extraoral gustatory
system. This system is implicated in the detection and
localization of a food source (Atema, '71). The glossopharyngeal and vagal nerve branches innervate only those taste
buds located in the oropharyngeal region and thus constitute the oropharyngeal taste system, which is important
for selective food ingestion (Atema, '71). Further, electrophysiological recordings from facial (Caprio, '75, '78, '82;
Davenport and Caprio, '82), glossopharyngeal, and vagal
(Kanwal and Caprio, '83) nerve branches showed that a few
differences exist in the chemosensory inputs from these two
systems.
It is essential to explore the Pattern of central Projection
of the primary sensory fibers belonging to the facial as well
as to the glossopharyngeal-vagal nerve complex if one is to
0 1987 ALAN R. LISS, INC.
elucidate the neural substrate involved in the integration
and coordination of feeding-related behaviors. The peripheral innervation and central distribution of the VII, IX, and
X cranial nerves in catfish was described initially by Herrick ('01). Although experimental confirmation of the central projections of the VII nerve was provided recently
(Finger, '76, '78; Morita et al., '80, '831, few reports (Morita
et al., '80; Morita and Finger, '85a,b) exist on the central
projections of the IX and X nerves in fishes.
From a comparative viewpoint, too, the glossopharyngealvagal (IX-X)complex has special significance as it composes
the largest variety of functional fiber types among the
cranial nerves of vertebrates (Angevine and Cotman, '81).
Nerve trunks belonging to this complex transmit gustatory
and general visceral information from orobranchial re-
Accepted April 15, 1987.
Address reprint requests to J. Kanwal, Department of Cellular
and Structural Biology, University of Colorado School of Medicine,
4200 East, Ninth Avenue, Denver, CO 80262.
CENTRAL PROJECTIONS OF IX-X NERVES IN CATFISH
gions, as well as interoceptive-visceral information from
organs in the coelomic cavity (Dart, '22; Herrick, '22). In
the fish, the peripheral innervation of the glossopharyngeal
nerve is generally restricted to the anterior part of the oral
cavity, whereas the field of innervation for the vagus extends from the orobranchial region to the visceral organs
in the coelomic cavity (Fig. la). At one level of analysis, the
orobranchial region in the fish serves as a source of exteroceptive information (Bullock et al., '77) because of the respiratory flow of water (the environmental medium) over the
orobranchial region. Thus, branches of the vagal complex
transmit either exteroceptive- or interocsptive-visceral information from the external and internal milieus, respectively (Fig. lb). Such a functional-anatomical classification
is found to be more useful for an analysis of the neural
organization in this region than purely physiological (taste
vs. tactile) or functional (special vs. general visceral) criteria. In fact, the branchial branches of the vagus carry different proportions of general (tactile, etc.) and special (taste)
visceral sensory fibers according to the relative number of
taste buds on different regions of the orobranchial epithelium (Herrick, '01). This is also evident from electrophysiological recordings of taste and tactile activity in the
branchial branches of the vagus (Kanwal and Caprio, '83).
The purpose of this study was to examine in the channel
catfish the central pattern of projection of individual
branches of the IX and X nerves, characterized on the basis
of their peripheral distribution.
217
phate buffer (pH = 7.2). After removal of the fixed brain,
the tissue was embedded in 20% gelatin or egg yolk and
fixed for a n additional period of 4-6 hours in a cold solution
of 4% buffered glutaraldehyde saturated with sucrose. The
tissue was sectioned either transversely or horizontally at
35 pm on a freezing microtome. Sections were collected in
0.1 M phosphate buffer, treated with Hanker-Yates reagent, (Bell et al., '811, and mounted as two alternating
series on chrome-alum-coated (subbed) slides. The perfusion, cutting, treating, and mounting were generally performed within a period of 3-5 days. The mounted and dried
sections were stained with thionin, dehydrated, cleared in
xylene, and mounted with Permount.
RESULTS
Peripheral organization of glossopharyngeal and
vagal nerves
Gross anatomical dissection revealed that prior to entering the first gill arch, the glossopharyngeal nerve gives off
a small branch that rejoins the main trunk after making a
short loop and possibly sending some fibers to the mucosa
on the roof of the oral cavity (Fig. la). The vagal complex
consists of several distinct nerve branches with their ganglia grouped together and located adjacent to that of the
glossopharyngeal nerve, outside of the cranium. Furthermore, the vagal nerve trunks peripheral to the ganglia are
segregated anteroposteriorly into branches innervating the
MATERIALS AND METHODS
Juvenile channel catfish, Ictalurus punctatus, 200-250
mm long, were obtained from a local fish farm and maintained in 75-liter aquaria on a 12:12 hour light-dark cycle.
The fish were anesthetized with tricaine methane sulfonate
WS-222; 1:7,000) and clamped horizontally in a Plexiglas
fish holder. Water containing MS-222 was perfused over the
gills. The IX or X nerve branch was dissected free of the
surrounding tissue in the gill region and transected, and
the central end was sucked into a small section of polyethylene (PE-20 or PE-90) tubing. Horseradish peroxidae W P )
crystals (Sigma type VI) were placed next to the cut end of
the nerve in the tubing after the fluid inside was withdrawn with a cotton wick. The open end of the tubing was
sealed with Super Glue and the tube was glued to the
ventral surface of the cranium. This prevented displacement of the cut nerve from within the tubing as well as
dilution and diffusion of the HRP by tissue fluids. At the
end of the operation Vaseline was applied to the region of
the surgery, the wound was sutured, and the animal was
returned to the tank.
The peripheral innervation of the labelled nerves was
examined from preserved specimens for purposes of nerve
identification and determination of the site of surgery and
HRP application. The specific nerves labelled were (1)the
entire glossopharyngeal nerve peripheral to its ganglion,
(2) the anteriormost branch of the vagus nerve innervating
the second branchial cleft (VN2), (3) the posteriormost
branch of the vagus nerve innervating the viscera (IVN),
and (4)vagal branches located between VN2 and IVN and
identified as VN3, VN4, and VN5, according to their anteroposterior sequence of innervation.
Following a survival period of 3-6 days, each animal was
reanesthetized with an overdose of MS-222 and perfused
transcardially with heparinized freshwater teleost Ringer's
and a cold solution of 4% glutaraldehyde i n 0.1 M phos-
Abbreviations
BC
CB
cia
ci
DC
DMN
dlf
dtv
ELL
FL
GL
GLN
hf
iaf
il
IVN
LL
brachium conjunctivum
cerebellum
interauricular commissure of Wallenberg
commissura i d i m a of Haller
dorsal cap of the vagal lobe
dorsal motor nucleus of the vagus
dorsolateral fascicle of the vagal nerve
descending tract of the trigeminal nerve
electrosensory lateral line lobe
facial lobe
gustatory lemniscus
glossopharyngeal nerve
horizontal fascicle of the vagal nerve
internal arcuate fibers
intermediate lobule of the facial lobe
interoceptive branch of the vagus
lateral line lobe
lateral lobule of the facial lobe
11
medial lobule of the facial lobe
ml
medial longitudinal fasciculus
mlf
nA
nucleus ambiguus
lateral funicular nucleus
nF1
medial funicular nucleus
nFm
primary general visceral nucleus
nGV
nucleus intermedius of the facial lobe
nIF
nlv nucleus intermedius of the vagal lobe
nMIX motor nucleus of the glossopharyngeal nerve
octaval nucleus
nO
reticular formation
RF
spinal cord
S
Tel
telencephalon
opticum tectum
Ti0
tSG (2G)secondary gustatory tract
V
ventricle
VL
vagallobe
VMC vagal motor column
VN
vagal nerve
VN2-4 vagal nerve branches innervating oropharyngeal regions
between the 2nd and 4th branchial arches
VSC
vagal sensory column
J.S. KANWAL AM) J. CAPRI0
218
glossopharyngeal
trunks
viscera
_
/
-
-
organ
oral cavity
o r a l floor
MAJOR COMPONENTS OF T H E GLOSSOPHARYNGEAL-VAGAL
( I X - X ) NERVE COMPLEX I N I C T A L U R I D C A T F I S H
IX-x
ORAL
BRANCHIAL
S P E C I A L and
GENERAL
I
CO E L 0 M I C
(tactile,c hemosensor y ,etc.)
b
Fig. 1. a: A diagrammatic sagittal view of the peripheral pattern of
innervation of the glosspharyngeal (1x1 and the exteroceptive (branchial)
and interoceptive-visceral branches of the vagus (X) nerve in the oropharyngeal region of the channel catfish. b: Two functional-anatomical subdivisions of nerve fibers in the glossopharyngeal-vagal complex. The
glossopharyngeal nerve and branchial branches of the vagus together constitute the exteroceptive-visceral subdivision, which is distinct from the
group of exteroceptive-visceral fibers of the vagus innervating coelomic
viscera.
second, third, and fourth gill arches and the corresponding
portions of the floor of the oral cavity. Separate branches
also innervate other structures such as the palatal organ in
the oropharyngeal region. A distinct, posterior branch of
the vagus nerve complex turns caudally to innervate visceral organs such as the stomach, heart, and liver.
Central organization of glossopharyngeal afferents
Afferent fibers of the glossopharyngeal nerve enter the
brainstem adjacent to the vagal nerve complex. After traversing rostrodorsally along the lateral aspect of the vagal
lobe, the IX fibers split into two rootlets-a dorsolateral
fascicle and a horbontal fascicle (Fig. 2). The dorsolateral
fascicle curves along the dorsal surface of the vagal lobe,
ventral to the dorsal cap, and terminates heavily in the
dorsolateral portion of the vagal lobe. (Fig. 2C,D). The horizontal fascicle proceeds medially coursing through the
bundles of the secondary gustatory tract. After reaching
the medial border of the vagal lobe these fibers diverge
dorsally and split into two components. One component
continues posteriorly for a few hundred microns before terminating along the medial edge of the vagal lobe in the
region of the nucleus intermedius of the vagal lobe ( n N )
(Herrick, '05). The other component turns anteriorly and
then laterally into the vagal lobe proper where it intermingles with the dorsal rootlet fibers before terminating. Most
of the glossopharyngeal afTerents terminate diffusely in the
anterior portion of the vagal lobe, where it constricts before
merging with the facial lobe. In addition, a small root of
the glossopharyngeal nerve continues rostrally and eventually splits into two fascicles, each fascicle making a caudoventromedial turn before reaching small, separate areas
in the region of the nIF (Fig. 2A). Both terminal fields are
located along the ventral border of the fourth ventricle Fig.
3). The most rostra1 branch turns ventrally, while the other
turns dorsally prior to termination.
Central organization of vagal afferents:
I. Exteroceptive-visceral roots
Sensory fibers of the vagus nerve can be considered to
consist of two divisions: (1)exteroceptive-visceral afferents,
which innervate the gill arches and posterior portions of
the oral cavity and transmit sensory information from the
water flowing through the orobranchial region, and (2) the
descending interoceptive-visceral branch (Fig. lb). The exteroceptive-visceral roots exhibit a pattern of termination
in the vagal lobe similar to that described for the glossopharyngeal nerve (Fig. 41, sections A-C). Thin fibers ascend
obliquely and course in a rostrodorsal direction toward the
area of termination of the dorsal fibers of the IX nerve. The
Fig. 2. Central projection pattern of the glossopharyngeal nerve root in
the rostra1 part of the vagal lobe (sections C and D) and in the region of the
nucleus intermedius of the facial lobe (nIF) (sections A and B). Note that
the glossopharyngeal fibers do not terminate in the dorsal cap region (DC)
of the vagal lobe. Continuous lines indicate path of the nerve roots and
dotted lines indicate regions of termination. Filed triangles indicate location
of cell bodies of glossopharyngeal efferents. The anteroposterior levels of
the sections are indicated on a dorsal view of the catfish brain.
D
Fig. 3. a: Photomicrograph of a section caudal to Figure 2 (section B)
showing the medial projection and caudal terminal zone of HRP-labelled
glossopharyngeal fibers (solid arrows) in the region of the nucleus intermedius of the facial lobe (nIF).h: Photomicrograph of a section caudal to Figure
2 (section A) showing HRP labelled fibers (arrows) of the glossopharyngeal
nerves coursing toward the region of the nIF in the facial lobe.
CENTRAL PROJECTIONS OF IX-X NERVES IN CATFISH
221
I
F
Fig. 4. Central projection pattern (I) of the most anterior exteroceptivevisceral branch, VN2, and (11) the interoceptive-visceral branch, IVN, of the
vagus. Continuous lines indicate path of the nerve roots and discontinuously dotted lines or stippled areas indicate regions of terminations. Filled
triangles indicate location of cell bodies of vagal efferents. Section A is at
the same anteroposterior level as section D of Figure 2, sections B and C
are located in the rostra1 half of the vagal lobe, while sections D and E are
located in the caudal part of the vagal lobe. Section F is immediately caudal
to the vagal lobe.
thicker fibers also ascend for a short distance, turn medially over the spinal V tract, and descend to the nIV near
the lateral wall of the fourth ventricle. A small fascicle of
the dorsal rootlet of the anterior branch of the vagus nerve
continues dorsally over the lobe and terminates along the
medial half of the dorsal cap of the vagal lobe (Fig. 5a). The
dorsal cap is a dorsolateral nuclear region that can be
distinguished easily as a lamina separated from the rest of
the vagal lobe by a thin capsule of fiber fascicles. The most
posterior branchial root terminates extensively throughout
the caudal two-thirds of the vagal lobe even though the root
enters the lobe at its most caudal region. In addition, a
small fascicle continues for some distance in a rostrodorsal
direction and finally terminates in the lateral half of the
dorsal cap region (Fig. 5b).
Central organization of vagal afferents:
11. Interoceptive-visceralroots
The general visceral fibers innervating the viscera form
a unique pattern of central projection and termination. This
root of the vagus contains only general visceral sensory
(tactile, general chemosensory, etc.) fibers innervating the
visceral organs and is thus referred to as the interoceptivevisceral branch in order to make a clear distinction from
Fig. 5. Photomicrographs of terminations in the dorsal cap region (DC)
of the vagal lobe of the branchial branches (a)VN2 and (b) VN4 of the vagus
labelled with HRP. The sections, taken from different animals, represent
approximately the same anteroposterior level in the vagal lobe. The lateral
portion of the dorsal cap labelled in (b) extends toward the caudal end of the
vagal lobe.
CENTRAL PROJECTIONS OF IX-X NERVES IN CATFISH
223
Fig. 6. HRP-labelled fibers and terminations in (a) the nIV and (b) the nGV ipsi- and contralateral
to the site of HRP injection in the interoceptive branch of the vagus (IVN). Segregated fiber fascicles
decussate through the commissura infima of Haller to terminate in the nGV of the contralateral side.
the exteroceptive-visceral branches of the vagus, which contain special visceral (taste) as well as general visceral (tactile, etc.) fibers (Herrick,'Ol, '06; Kanwal and Caprio, '83).
Unlike the branchial roots, the interoceptive-visceral root
does not split into a dorsal and horizontal rootlet (Fig. 411,
sections D-F). Instead, the entire root terminates just caudal to its point of entry, in the general visceral nucleus
(nGV), with a few fascicles continuing rostrally and terminating in the nucleus intermedius of the vagal lobe (nW)
(Fig. 411, section F, Fig. 6a,b). A few fibers cross through
the commissura irfima of Haller in the form of segregated
fascicles and continue in a rostrodorsal direction before
terminating in the nGV of the contralateral side. For this
vagal root, no terminations were observed in the vagal lobe
Fig. 7. Photomicrographs of horizontal sections of the brainstem of the catfish in which two vagal
nerve branches, VN2 and IVN, were simultaneously labelled with HRP. a: Only terminations of VN2
are seen in a section through the vagal lobe proper. b: At levels ventral to the vagal lobe, terminations
of IVN in the nGV and portions of the horizontal and dorsolateral fiber fascicles of VN2 are visible.
CENTRAL PROJECTIONS OF IX-X NERVES IN CATFISH
MOTOR FIBERS
CENTRAL
SENSORY
PROJECTION ZONES
N E R V E TRUNK
J
FL
VN2
VN4
IVN
\
* -V
/
Fig. 8. Diagrammatic scheme of the visceral sensory (VSC) and vagal
motor (VMC) columns projected onto a sagittal view of the medulla to show
the segmental pattern of projections and partial overlap of terminations of
the sensory and motor components o f the IX-X complex. Arrows to the side
face of the sensory column indicate the primary projection zone of the
sensory fibers (stippled vs. blank zones), while arrows to the front face
indicate the rostrocaudal extent of fiber terminations for each nerve branch
labeled with HRP. Hatched areas indicate zones where no labelling was
observed. The locations of cell bodies (CB) of motor neurons and the region
of exit of efferent fibers (F) from the medulla are indicated separately for
each nerve. Both columns (VMC and VSC) are represented on the same
scale and axis. Numbers along the midline indicate the distance in millimeters from the rostral end of the vagal lobe. Motor neurons of the glossopharyngeal nerve are located anterior to the vagal lobe. The interoceptivevisceral branch of the vagus (IVN) projects to the general visceral nucleus
located caudal to the vagal lobe. Specific rostral sites of termination of the
glossopharyngeal nerve, a t the level of the facial lobe, are not shown.
proper on either the ipsi- or the contralateral side (Fig. 6).
This distinction between terminations of the exteroceptive
and the interoceptive vagal roots and the segmental pattern of projection of orobranchial roots is best seen in photomicrographs of horizontal sections of the brainstem (Fig.
7a,b).
Central organization of glossopharyngeal and
vagal efferents
All of the IX-X efferent roots originate from cell bodies
located in a continuous longitudinal column, bordering the
fourth ventricle, along the ventromedial portion of the medulla (Fig. 8). These motor roots then travel caudolaterally
and join their respective afferent roots before emerging
from the cranium (Fig. 2,4). The IX-X motor column is
broadened dorsoventrally toward the caudal end of the vagal lobe and tapers to a ventral location before terminating
225
in the region of the obex. As in Silurus glanis (Berkelbach
van der Sprenkel, '15; Black, '171, this column is not continuous with the facial motor nucleus and terminates approximately 150 pm before the appearance of the VII motor
nucleus rostrally. The cell bodies of glossopharyngeal efferents are located only at the rostral extremity of the cell
column at the level of the caudal portion of the facial lobes
(Figs. 2B, 3a, 8). These cells (approx. 40 pm along the long
axis) are ovoid to conical in shape with the long axis directed in a ventrolateral plane. The axons of these neurons
proceed caudally along the ventromedial margin of the
ventricles before turning dorsolaterally. These fibers then
travel through the nIF and loop around the dorsal aspect of
the spinal V tract before turning caudally to exit the brain
along with the afferent fibers (Fig. 2). This root finally
makes a sharp rostral turn and becomes the main glossopharyngeal nerve trunk.
The most anterior branch of the vagus, which innervates
the second gill arch, has cell bodies of its efferents located
in the anterior portion of the vagal lobe at the level of
termination of the glossopharyngeal afferents (Fig. 8). The
cell bodies (approx. 40 pm in size) are morphologically similar to those of the glossopharyngeal efferents. As observed
previously (Herrick, '01; Morita and Finger, '85a), the dendrites of these cells extend well into the lateral portion of
the reticular formation and the axon originates from the
base of the dendrites. Another branchial branch, which is
referred to as VN3, and innervates primarily the palatal
organ, is nearly devoid of efferents (Fig. 8). Only one labelled cell body was observed and this was located rostral
to the level of afferent terminations of this nerve root (VN3).
Whereas the cell bodies of most branchial branches appear
to be arranged in a segmental fashion along the long axis
of the visceral motor column (Fig. 81, those of the most
posterior branch of the vagus (IVN) are distributed
throughout the posterior half of the motor column (Fig. 9a).
These cell bodies (approx. 30 pm in size) are more rounded
and arranged more loosely than the motor neurons with
efferents in the branchial branches of the vagus (Fig. 9b).
Also, dendrites belonging to motor neurons of the IVN do
not project laterally into the adjacent reticular formation.
In contrast to a restriction of the cell bodies of efferents of
the branchial branches of the vagus (VN2, VN3, and VN4)
to the anterior part of the vagal motor nucleus, those of the
IVN form the caudal half of the IX-X motor column (Fig. 8).
DISCUSSION
Several studies (Bardach et al., '67; Atema, '71; Johnsen
and Teeter, '80) have confirmed the role of gustation in the
feeding behavior of ictalurid catfish since Herrick first proposed this hypothesis (Herrick, '04,'05). In keeping with
Herrick's approach, the present results are considered from
a functional viewpoint and delineate further the neural
substrate involved in feeding. A comparison of our results
with other anatomical studies in fishes as well as land
vertebrates also provides an evolutionary perspective on
the pattern of central projections of the IX and X nerves.
The pattern of projection of the IX-X complex in the brainstem of the channel catfish, I. punctatus, generally conforms to Herrick's ('05) description in the bullhead catfish,
I. nebulosus. HRP labelling of fibers and cell bodies, however, reveals some new and important aspects of neural
organization.
226
J.S. KANWAL AND J. CAPRI0
Fig. 9. Photomicrographs showing (a) the location and (b) the cell morphology of parasympathetic
neurons (of the presumptive DMN) of the interoceptive-visceral branch of the vagus in the caudal
region of the medulla. The rostrally extended distribution and circular shape of these neurons make
them distinct from the triangular, segmental arrangement of other motor neurons whose efferent
fibers project peripherally in the branchial branches of the vagus.
CENTRAL PROJECTIONS OF IX-X NERVES IN CATFISH
Comparative considerations
Atferent and efferentroots of the glossopharyngeus. The
central organization of the visceral afferent and efferent
areas has been described in several groups of vertebrates.
Among mammals, the glossopharyngeal visceral afferents
in the cat (Torvik, '56; Kerr, '62; Kalia and Mesulam,
'80a,b), the rat (Kalia and Sullivan, '82; Hamilton and
Norgren, '84), and the lamb (Sweazey and Bradley, '86)
terminate extensively in the nucleus of the solitary tract
and extend from the caudomedial border of the terminal
zone of chorda tympani afferents to the region of the obex.
Further, a small contralateral projection of the IX nerve
via the commissural nucleus exists in some mammals (Kalia and Mesulam, '80a; Kalia and Sullivan, '82). In ranid
frogs, the termination zone of the glossopharyngeal nerve
is quite similar to that of mammals and is reported to be
entirely ipsileteral (Matesz and Szekely, '78; Hanamori and
Ishiko, '83; Stuesse et al., '84). Among teleostean species,
the brainstem region corresponding to the nucleus of the
solitary tract is highly variable in its morphology. In general, this continuous column can be divided morphologically into the facial, glossopharyngeal, and vagal lobes. In
the ictalurid catfishes, the glossopharyngeal lobe is reduced
and is not visible as a separate entity from the surface. The
present study, however, confiims earlier reports (Herrick,
'05; Morita et al., '80, '83; Morita and Finger, '85a) of the
presence of glossopharyngealterminations in the transition
zone of the facial and vagal lobes. The restricted anteroposterior extension (rostral part of the vagal lobe and caudomedial region in the facial lobe) of this zone is unlike the
caudal location of glossopharyngeal terminations in the
nucleus of the solitary tract of most mammals (Kalia and
Mesulam, '80a; Kalia and Sullivan, '82; Hamilton and Norgren, '84) and amphibians (Hanamori and Ishiko, '83;
Stuesse et al., '84). Nevertheless, with respect to laterality,
the pattern is like that observed in Rana pipiens and R.
catesbiana (Stuesse et al., '84). As in most vertebrate species
studied, there is also some overlap of glossopharyngeal
projections with the region of termination of vagal afferents
(Fig. 8).
The general pattern of projection of the glossopharyngeal
nerve in the channel catfish is similar to previous descriptions in the bullhead catfish (Herrick, '01; Morita and Finger, '85a) and the carp (Morita et al., '80). An important
additional observation included in this study relates to the
distinct rostral projections of the glossopharyngeal root seen
after labelling the nerve with HRP. A similar pattern of
central projections of glossopharyngeal afferents exists in
the Japanese sea catfish, Plotosus lineatus (personal observation), which suggests that this may be a general feature
of silurids. The possible functional significance of these
projections is discussed later. It is interesting that a similar
rostral course of the glossopharyngeal root was recently
reported for ranid frogs (Stuesse et al., '84) and, among
mammals, in the lamb (Sweazey and Bradley, '86). A detailed investigation of the glossopharyngeal nerve was not
performed in the single experimental study on this nerve
in a fish (Morita et al., 80). Moreover, previous reports are
based on either staining or degeneration techniques, both
of which are relatively insensitive and less reliable than
the HRP technique.
The location of the glossopharyngeal motor nucleus in
ictalurid catfish is quite similar to that of other vertebrates
studied (Hamilton and Norgren, '84; Sweazey and Bradley,
227
'86). This nucleus forms the rostral extremity of the ventromedial part of the visceral motor column. The circuitous
path taken by the motor root of the IX is consistent with
previous reports and is apparently a characteristic feature
of this nerve in all teleosts (Barnard, '36).
Merent and efferent roots of the vagus. The present
results indicate that exteroceptive-visceral and interoceptive-visceral vagal roots exhibit two distinct patterns of
projection. The roots of all the exteroceptive-branchial
branches of the vagus contain general (including tactile,
proprioceptive, etc.) as well as special (taste) visceral afferents (Herrick, '01, '06). These two categories of fibers may
separate centrally according to the observed splitting of
each root into a dorsolateral and a ventral (horizontal)
rootlet in lctalurus (present study), Silurus (Berkelbachvan
der Sprenkel, '15), and Carassius (Morita et al., '80). In
spite of this separation, both rootlets eventually enter the
vagal lobe proper and terminate over partially overlapping
domains within the lobe. An apparent lack of bimodal (taste
and tactile) units in the vagal lobe (Kanwal and Caprio,
'84), however, indicates that these two fiber types may not
generally converge onto the same interneurons of the vagal
lobe.
The central projection pattern of the most posterior, or
interoceptive-visceral, branch of the vagus provides additional support for considering this branch as being distinct
from the branchial branches of the vagus. Interoceptivevisceral afferents do not enter the vagal lobe (Fig. 411, 7)
but project solely to the ipsilateral general visceral nucleus
with some fibers crossing over to the contralateral side via
the commissural nucleus of Cajal. The only region common
to the termination field of these two sets of vagal roots is
the most caudal portion of the nucleus intermedius of the
vagal lobe (nIV), which is contiguous with the rostral end
of the general visceral nucleus. The bilateral projection
pattern of interoceptive-visceral afferents has been consistently observed in all species of vertebrates investigated
(Kalia and Mesulam, '80b; Kalia and Sullivan, '82; Katz
and Karten, '83b; Hamilton and Norgren, '84; Stuesse et
al., '84; Sweazey and Bradley, '86). However, the discrimination between exteroceptive-branchial and interoceptivevisceral fibers is difficult in the peripheral and central
nervous system of most vertebrates other than teleosts.
Changes in the fasciculation and branching pattern of the
vagal nerve trunk associated with changes in the anatomy
of the oropharyngeal region during evolution confound this
distinction in the rapidly evolving vertebrate lines. Previous studies on I. nebulosus (Herrick, '01, '05, '06) and S.
glanis (Berkelbach van der Sprenkel, '15) report the presence also of a general cutaneous component (somatic afferents) in the vagal roots, which, after separating centrally,
descends and terminates within the spinal V nucleus. No
such fibers were evident in the channel catfish although
they may be present in the few caudal branchial branches
not labelled in the present study.
Gross morphological evidence suggests that the posterior
lateral line nerve in fish, traditionally regarded as a branch
of the vagus, is a separate, phylogeneticaly primitive cranial nerve that has disappeared with the advent of land
vertebrates (Cole, 1896, 1898; McCormick, '83). This suggestion is supported by the uniqueness of its embryogenesis, peripheral innervation, and central projections and the
unique nature of the sensory information transmitted centrally. For similar reasons, it may be appropriate to regard
228
the exteroceptive-visceral branches as forming a separatecranial nerve trunk, distinct from the interoceptive-visceral
branch of the vagus. Such a clear separation is not evident
in the mammalian system because of a peripheral and
central reorganization of the exteroceptive-branchial
branches into the pharyngeal, laryngeal, and other
branches of the vagus. Previous studies (Torvik, '56; Kalia
and Mesulam, '80a; Kalia and Sullivan, '82) may have
failed, therefore, to delineate a functional organization in
the nucleus tractus solitarius (NTS) of mammals because of
an apparent intermingling of small fascicles of phylogenetically separate cranial nerve trunks. Nevertheless, the single detailed study on the rat (Hamilton and Norgren, '84)
showed a minimal overlap between terminals in the NTS
of the gustatory nerves and those of the cervical branch of
the vagus. In addition, in the lamb (Sweazey and Bradley,
'86) distinct differences were observed between the neural
projections of the lingual tonsillar branch of the glossopharyngeal and the superior laryngeal nerve of the vagus,
suggesting a functional basis for neural organization within
the brainstem.
The visceral motor column has been of considerable interest classically as a model for the study of neurobiotaxis
(Black, '17) and more recently with respect to the relationship of cellular topology and architectonics with region- and
organ-specific representation in mammals (Lawn, '66) and
birds (Katz and Karten, '83a, '85). The present results do
indicate a clear difference between the motor neuron distribution in the root of the branchial branches (VN2-4) and
the interoceptive-visceral branch of the vagus. The branchial motor neurons are restricted to compact regions of the
vagal motor column, whereas cell bodies of efferents within
the interoceptive-visceral branch are distributed throughout the caudal half of the vagal motor column. In amniotes,
two populations of vagal motor neurons, the dorsal motor
nucleus and the nucleus ambiguus, are consistently observed (Brodal, '81). In Amphibia, the main portion of the
vagal motor nucleus has been homologized with the nucleus ambiguus of mammals (Matesz and Szekely, '78;
Stuesse et al., '84). In fish, this distinction is not sufficiently
clear. The differing patterns of distribution, observed in the
channel catfish, for efferents in the exteroceptive- and interoceptive-visceral vagal roots may be evidence for the
existence of at least two functionally different motor nuclei
within a topologically single, diffuse nucleus. In fact, the
single detailed experimental study in the goldfish distinguishes several populations of neurons (subnuclei) within
the visceral motor column (Finger and Morita, '85b; Morita
and Finger, '87).In the channel catfish, cell bodies of efferents in the IVN are distributed similar to the gut efferents
in the vagal motor column of ranid frogs (Stuesse et al., '84)
and in the dorsal motor nucleus of mammals (Kalia and
Mesulam, '80b) and may, thus, be homologous to a portion
of the dorsal motor nucleus of modern mammals. Cell bodies of efferents in the branchial branches of the vagus would
then correspond to topographically arranged neurons of the
nucleus ambiguus. The absence of direct terminations of
primary afferents onto vagal motor neurons is consistent
with previous observations in catfish (Herrick, '06; Barnard, '36).
Neuroethological and physiological considerations
The specialized ability of ictalurid catfish to monitoi
chemical stimuli in the environment is correlated with the
relative enlargement of the facial lobe (Herrick, '05, '06;
J.S. KANWAL AM) J. CAPRI0
Atema, '71). The glossopharyngeal lobe is morphologically
inconspicuous and the vagal lobe does not show any kind of
lobular or laminar organization seen in the facial lobe of
the bullhead catfish (Herrick, '05) or the vagal lobe of the
goldfish (Morita and Finger, '85b). Lack of such a distinctive organization in the vagal lobe of ictalurid catfish is
further reflected in the absence of a discrete topographic
map of oropharyngeal receptive fields in the vagal lobe of
the channel catfish (Kanwal and Caprio, '84, and in
preparation).
The IX roots project within the transition zone between
the facial and vagal lobes. Unlike the goldfish (Morita and
Finger, '85b) and the crucian carp, Carassius carassius
(Morita et al., '80),the pattern of termination of the glossopharyngeal roots in the channel catfish is similar to that of
the branchial nerve trunks of the vagus. The main root of
the glossopharyngeal nerve and branchial branches of the
vagus nerve run in a parallel fashion peripherally and
innervate sequential segments of the oropharyngeal region
(Fig. 1).Electrophysiological recordings from the peripheral
nerve trunks of the IX-X complex indicate that these nerve
branches transmit similar types of information (i.e., taste
and tactile) from specific portions of the oropharynx (Kanwal and Caprio, '83).
A significant deviation from this pattern concerns the
two specific connections made by a few fibers of the IX
nerve root with cells in the ventromedial portion of the
facial lobe. The caudal one of these two projections possibly
functions as a reflex circuit since these afferents terminate
near the glossopharyngeal motor neurons which lie anterior to the main zone of termination of the glossopharyngeal afferents. A similar arrangement was also observed
for the anterior branch of the vagus nerve in Amia calua,
where the efferent vagal nucleus is situated ventromedially
within the zone of glossopharyngeal afferent terminations
(Barnard, '36).
The most rostra1 afferent projection of the IX nerve is also
of special interest from a neuroethological perspective, because it may constitute the neural substrate for mixing
information in the central nervous system. Gustatory information from oral taste buds converges onto neurons in the
region of the nucleus intermedius of the facial lobe (nIF),
which also receives input from extraoral taste buds via the
facial afferent (Herrick, '05). Electrophysiological experiments previously showed that neurons in this region have
large tactile receptive fields that extend from the oral to
the extraoral surface (Marui and Caprio, '82). Some of these
neurons are bimodal in character and respond to chemical
as well as tactile stimulation (personal observation). Herrick regarded the nIF as a correlation center (Herrick, '06).
The present results indicate that a portion of the nIF may
integrate extraoral gustatory information related to food
search with the consequent oral stimulation leading to food
ingestion or rejection (Table 1).This may play an important
role in the development of a n efficient foraging strategy.
The dorsal cap of the vagal lobe, a region showing dense
enkephalin-like immunoreactivity in the bullhead catfish
(Finger, '81), is another specific region of the vagal lobe
whose function has not been described adequately. The
present results suggest that the dorsal cap may relate information from the anterior and posterior portions of the oropharynx. Intrinsic neurons in this region may therefore
have relatively large or dual receptive fields as reported
recently for the nucleus of the solitary tract of the rat
(Travers et al., '86). Also, small HRP injections restricted to
the dorsal cap region may reveal a difference in its neu-
CEN'I'RAL PROJECTIONS OF IX-X NERVES IN CATFISH
TABLE 1. Correlation of Visceral Information in the Brainstem of
Ictalurid Catfish
Converging visceral
inputs
Brainstem regions
Nucleus intermedius of the
FL (nIF)
Dorsal cap nucleus (DC)
Nucleus intermedius of the
VL (nIV)
Extraoral and oral gustovisceral
inputs
Spatially segregated
oropharyngeal visceral inputs
Exteroceptive- and interoceptivevisceral inputs
ronal connectivity as compared to the other parts of the
vagal lobe.
Finally, the descending branch of the vagus (i.e., the
interoceptive-visceral branch) is nongustatory in function
and anatomically distinct from the exteroceptive-visceral
branches of the vagus (Fig. 1,4).This interoceptive-visceral
branch does not converge directly onto secondary gustatory
neurons. Instead, it terminates in the caudal region of the
nucleus intermedius of the vagal lobe (nIV)and the general
visceral nucleus (nGV) of the ipsi- and contralateral side
via decussations through the commissura infima of Haller
(Fig. 5a,b). Anatomically,the nGV is adjacent to the caudal
end of the nIV. The nIV also receives fibers from branchial
branches of the vagus and may thus constitute another
correlation center (Herrick, '05; Kanwal and Caprio, '84),
which integrates gustatory input with interoceptive-visceral input related to the physiological state of the animal.
Oropharyngeal sensory input in mammals is also known
to evoke a variety of vagal-dependent physiological (Kuwahara, '83)and hormonal (Brand et al., '82) responses including initiation of food ingestion. Regulation of short-term
(Gonzalezand Deutsch, '81; Lorenz and Goldman, '82; Alino
et al., '83) and long-term (Sharma and Nasset, '62; Chinna
and Bajaj, '72; Li and Anderson, '84) food ingestion is further accomplished by the central influence of the interoceptive-visceral sensory input via the coelomic branches of the
vagus. The present results suggest the possibility that some
of these functions may be modulated by central connections
of neurons in the nIV.
CONCLUSIONS
The present results, in general, confirm the previous observations relating to the pattern of projection of IX-X nerve
roots in the brainstem of fishes. The new findings suggest
several interesting aspects of neural organization and information processing in the teleostean brainstem. The nucleus
intermedius of the facial lobe (nIF), the dorsal cap of the
vagal lobe, and the nucleus intermedius of the vagal lobe
(nIV)are implicated as sites for visceral interactions related
to feeding. The exteroceptive-visceral nerve branches remain distinct, peripherally and centrally, from the interoceptive-visceralbranch of the vagus. Thus, the brainstem
of ictalurid catfish is a good model with which to investigate principles of the functional organization in the brainstem of vertebrates. The present study provides important
anatomical clues to the differential processing of visceral
information in this neural structure that may play an important role in the regulation of food search and ingestion.
ACKNOWLEDGMENTS
We thank Dr. Thomas Finger for his useful suggestions
regarding the HRP technique and for critically reviewing
229
the manuscript. This research was supported in part by
NIH grant NS14819 to J. Caprio and NIH grant NS15258
to T. Finger.
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