Anterior and Posterior Oral Cavity Responsive Neurons Are
Differentially Distributed Among Parabrachial Subnuclei in Rat
CHRISTOPHER B. HALSELL AND SUSAN P. TRAVERS
Section of Oral Biology, The Ohio State University, Columbus, Ohio 43210
INTRODUCTION
Primary gustatory and somatosensory afferent fibers in
the facial, glossopharyngeal, trigeminal, and vagal cranial
920
nerves terminate in an orderly sequence within the rostral
division of the nucleus of the solitary tract (NST) (e.g.,
Hamilton and Norgren 1984). Neurophysiological recordings demonstrate that the organization of NST reflects
its orotopic input (Dickman and Smith 1989; McPheeters et
al. 1990; Ogawa et al. 1984; Sweazey and Bradley 1989;
Travers and Norgren 1995; see also Travers 1993), with
neurons responsive to anterior oral cavity (AO) stimulation
lying anterior and lateral to those responsive to posterior
oral cavity (PO) stimulation. The receptive fields of single
neurons show a similar orderly organization. Convergence
of sensory inputs provides evidence for central integration
but this integration is not random; instead it occurs preferentially between receptors confined to the AO or PO (Travers
and Norgren 1995; Travers et al. 1986).
Although less striking, neurophysiology and Fos immunohistochemistry also suggest a chemotopic arrangement
within NST that seems to be partly a consequence of orotopy
combined with the differential chemosensitivities of peripheral gustatory nerves (Harrer and Travers 1996; McPheeters
et al. 1990; Mistretta 1988; Scott et al. 1986). Finally, the
NST is organized by modality, with neurons responsive
solely to intraoral mechanical stimulation extending lateral
to those cells responsive to gustatory stimulation (Halsell et
al. 1993; Ogawa and Hayama 1984; Ogawa et al. 1984;
Travers and Norgren 1995). The topographic organization
of NST may serve as an anatomic substrate for differential
control of ingestive and rejection responses by different peripheral nerves, modalities, and gustatory stimuli (Frank
1991; Grill et al. 1992; Harrer and Travers 1996; Zeigler et
al. 1985; see also Travers 1993, Travers et al. 1987). An
even more striking segregation between peripheral afferent
inputs occurs in the teleost medulla (e.g., catfish: Finger
1976; Hayama and Caprio 1989; Kanwal and Caprio 1987),
a segregation that mirrors the specific effects of facial versus
vagal input in controlling food selection versus swallowing
in these species (Atema 1971).
The topography of the parabrachial nucleus (PBN), the
main recipient of ascending NST projections in nonprimate
mammals, is less well understood, although an orotopic organization has been suggested along the dorsoventral axis
(Norgren and Pfaffmann 1975; Ogawa et al. 1987). In one
study, it was suggested that the anterior tongue was represented ventral to the posterior tongue (Norgren and Pfaffmann 1975). This conclusion, however, was based on specifically stimulating the anterior tongue by placing it in a
chamber but attempting to stimulate the posterior tongue by
flowing tastants over the rest of the oral cavity, a technique
that probably failed to optimally stimulate buried circumval-
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Halsell, Christopher B. and Susan P. Travers. Anterior and
posterior oral cavity responsive neurons are differentially distributed among parabrachial subnuclei in rat. J. Neurophysiol. 78:
920–938, 1997. The responses of single parabrachial nucleus
(PBN) neurons were recorded extracellularly to characterize their
sensitivity to stimulation of individual gustatory receptor subpopulations (G neurons, n Å 75) or mechanical stimulation of defined
oral regions (M neurons, n Å 54) then localized to morphologically
defined PBN subdivisions. Convergence from separate oral regions
onto single neurons occurred frequently for both G and M neurons,
but converging influences were more potent when they arose from
nearby locations confined to the anterior (AO) or posterior oral
cavity (PO). A greater number of G neurons responded optimally
to stimulation of AO than to PO receptor subpopulations, and these
AO-best G neurons had higher spontaneous and evoked response
rates but were less likely to receive convergent input than PO-best
G neurons. In contrast, proportions, response rates, and convergence patterns of AO- and PO-best M neurons were more comparable. The differential sensitivity of taste receptor subpopulations
was reflected in PBN responses. AO stimulation with NaCl elicited
larger responses than PO stimulation; the converse was true for
QHCl stimulation. Within the AO, NaCl elicited a larger response
when applied to the anterior tongue than to the nasoincisor duct.
Hierarchical cluster analysis of chemosensitive response profiles
suggested two groups of PBN G neurons. One group was composed
of neurons optimally responsive to NaCl (N cluster); the other to
HCl (H cluster). Most N- and H-cluster neurons were AO-best.
Although they were more heterogenous, all but one of the remaining G neurons were unique in responding best or second-best
to quinine and so were designated as quinine sensitive (Q/ ).
Twice as many Q/ neurons were PO- compared with AO-best. M
neurons were scattered across PBN subdivisions, but G neurons
were concentrated in two pairs of subdivisions. The central medial
and ventral lateral subdivisions contained both G and M neurons
but were dominated by AO-best N-cluster G neurons. The distribution of G neurons in these subdivisions appeared similar to distributions in most previous studies of PBN gustatory neurons. In contrast to earlier studies, however, the external medial and external
lateral-inner subdivisions also contained G neurons, intermingled
with a comparable population of M neurons. Unlike cells in the
central medial and ventral lateral subnuclei, nearly every neuron
in the external subnuclei was PO best, and only one was an Ncluster cell. In conclusion, the present study supports a functional
distinction between sensory input from the AO and PO at the
pontine level, which may represent an organizing principle
throughout the gustatory neuraxis. Furthermore, two morphologically distinct pontine regions containing orosensory neurons are
described.
OROSENSORY RESPONSES IN THE PARABRACHIAL NUCLEUS
METHODS
Subjects and preparation
Eighty-two adult male Sprague Dawley rats ranging in weight
from 270 to 460 g were used for recording. The animals were
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anesthetized with ethyl carbamate (urethan, 1.0 g/kg ip) and pentobarbital sodium (Nembutal, 25 mg/kg ip). Supplemental doses of
Nembutal (10 mg/kg ip) were administered as needed to maintain
surgical levels of anesthesia, i.e., areflexia of hindlimb withdrawal
and corneal blink, for the duration of the recording session. A bolt
and headholder assembly was attached to the skull to provide a
secure attachment to the stereotaxic frame and clear access to the
oral cavity (Halsell et al. 1993; Travers and Norgren 1991, 1995;
Travers et al. 1986). The hypoglossal and superior laryngeal nerves
were sectioned bilaterally to prevent tongue movement and reflex
swallowing. A tracheal cannula was inserted and a drain was passed
into the mouth from the pharynx. The clinical crowns of the upper
incisors were amputated. Sutures were placed in the corners of
the mouth and around the lower incisors. When the sutures were
retracted, the entire oral cavity was visible. Sutures also were
placed through the tongue between the intermolar eminence and
the circumvallate papilla. These sutures were used to position the
tongue to maximize exposure of the foliate or circumvallate papillae. The portions of the parietal and interparietal cranial plates
above the transverse sinus and lateral to lambda were trephined.
The dura was reflected around the transverse sinus and the sinus
was ligated and resected.
Recording
Glass-coated tungsten microelectrodes (Z Å 1.0–3.9 MV ) were
used to record extracellular action potentials arising from single
neurons, recognized by their consistent waveform and amplitude.
Neural activity was amplified, monitored, and stored on video format tape using conventional techniques. Voice commentary and
stimulus markers (vide infra) were stored concurrently to facilitate
off-line analysis. The electrode was positioned perpendicular to
the dorsal surface of the skull with the skull flat, i.e., positioned
so bregma and lambda were on the same horizontal plane.
Orosensory-responsive neurons were systematically searched for
throughout the dorsal pontine tegmentum. Electrode penetrations
were made in a grid pattern with 100- to 200-mm steps in the
rostrocaudal and mediolateral dimensions. After passing through
the cerebellum, the electrode was advanced ventrally through the
tissue in 50- to 100-mm steps by means of a piezoelectric microdrive (Inchworm System, Burleigh Instruments). During the
search procedure, single orosensitive neurons in PBN were identified by alternately stimulating the whole-mouth via a syringe using
a mixture of four standard tastants (vide infra) and rinsing with
water, then probing the oral mucosa using a glass probe. After an
orosensory neuron was isolated, it was tested systematically for
taste and/or mechanical sensitivity using the procedures described
below.
Stimulation
All taste stimuli were presented at room
temperature and were preceded by an identical stimulation with
water to control for the somatosensory aspects of stimulus application. The taste stimuli were chosen to represent four standard
taste qualities ( sweet, salty, sour, and bitter ) and consisted of
(in M) 0.01 Na saccharin, 0.3 NaCl, 0.01 HCl, 0.03 HCl, 0.003
quinine hydrochloride, and 0.01 quinine hydrochloride. Two
mixtures of the four representative stimuli also were used and
consisted of the above Na saccharin and NaCl concentrations
and either the higher or lower concentrations of both HCl and
quinine. No major differences were noted in the response properties of neurons stimulated with the higher or lower concentrations
of HCl and quinine. Na saccharin was substituted for the more
typical stimulus, sucrose, because the viscosity of the latter solution made it inconvenient to flow through the small pipette. Na
saccharin was predicted to be a reasonable alternative, due to its
GUSTATORY STIMULI.
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late and foliate taste buds while unintentionally activating
other taste buds including some in the AO (e.g., nasoincisor
duct). Another investigation using more specific stimulation
procedures supported the contention that anterior tongue
neurons are located ventrally but suggested that dorsal neurons receive input, not from the posterior tongue, but rather
from the palate, or palate and tongue, although only a few
neurons optimally responsive to posterior tongue stimulation
were recorded (Ogawa et al. 1987). Further, despite the
specificity of stimulation, there was no evidence that PBN
neurons had orderly receptive fields like those in NST. In
sum, it remains unclear whether the differential medullary
representation of the AO and PO persists in the pons.
A further complication regarding the topography of orosensory responses in PBN is suggested by a recent study
using Fos immunohistochemistry (Yamamoto et al. 1993).
This investigation provided provocative evidence that the
taste-responsive region of PBN may extend beyond the
boundaries usually recognized (Yamamoto et al. 1993). Previous neurophysiological studies have focused on a PBN
region located caudally and centered on the middle third of
the superior cerebellar peduncle and, although not typically
related to specific subnuclei, available histological reconstructions suggest taste-responsive neurons are located
mainly in the central medial and ventral lateral subnuclei
(Hill 1987; Norgren and Pfaffmann 1975; Ogawa et al. 1987;
Schwartzbaum 1983; Scott and Perrotto 1980; Travers and
Smith 1984; Van Buskirk and Smith 1981). Indeed, the one
study that localized taste responses within PBN subnuclei
found them confined to these subnuclei in hamster (Halsell
and Frank 1991). The Fos results in rat suggest, however,
that more rostral and lateral neurons in the external medial
and external lateral subnuclei are also responsive to taste
stimuli and, interestingly, that they respond preferentially to
behaviorally aversive stimuli such as quinine and HCl. The
Fos data therefore suggest that neurophysiological studies
may have missed a second taste-responsive PBN region.
Indeed, recent anterograde tracing studies in rat demonstrate
that the external medial and external lateral subnuclei are
labeled heavily with fibers and terminal-like varicosities
after rostral NST injections (Herbert et al. 1990), particularly when the injections are centered into the PO-responsive
NST region (Becker 1992; H. C. Hu and S. P. Travers,
unpublished observations).
The purpose of the current study was to determine the
topographic and receptive field organization of orosensory
PBN neurons. The response properties of single PBN neurons were characterized to determine their sensitivity to specific stimulation of individual taste receptor subpopulations
and to innocuous mechanical stimulation of defined oral regions. A special effort was made to optimize stimulation
procedures for posterior tongue taste buds in the foliate and
circumvallate papillae. Neurons characterized as to modality,
oral receptive field location, and chemosensitivity then were
localized to known cytoarchitectural boundaries of PBN subdivisions.
921
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C. B. HALSELL AND S. P. TRAVERS
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Neurophysiological data analysis
Neurophysiological responses were analyzed and quantified offline. Gustatory response measures were the number of action potentials occurring during the 10 s of stimulus presentation minus the
number of spontaneous action potentials occurring immediately
preceding the initial water stimulation (Fig. 1C). Although the
tactile and thermal components of manual tastant application occasionally elicited small transient responses (Travers and Norgren
1991, 1995; Travers et al. 1986), there were no differences in the
classification of neurons when taste responses were corrected with
spontaneous rate or the activity occurring during water flow. Minor
differences in response magnitude were noted, but for consistency,
the taste response was corrected with spontaneous rate for both
manual and automated application of taste stimuli. The automated
system in the present study provided for a continuous flow of water
followed by tastant so that any tactile and thermal responses were
adapted during the gustatory stimulation period. Indeed, subtracting
the water response would have underestimated the gustatory contribution when the automated flow system was used.
The criterion for a suprathreshold gustatory response was an
increase or decrease in firing rate of ¢10 spikes per 10 s that was
¢2.5 SD of the spontaneous rate (Travers and Norgren 1995).
Spontaneous rate was measured for 10 s preceding each stimulation, and the SD was calculated across these trials. The acrossstimulus correlations between gustatory neurons were analyzed
using multivariate techniques (Systat, SPSS). For hierarchical
cluster analysis, the Pearson product-moment correlation coefficients and average-linkage method were used to calculate taste
profile similarities. For multidimensional scaling, the Pearson product-moment correlation coefficients were used to derive and plot
interneuronal distances in two dimensions. A two-dimensional
space was chosen because the calculated stress levels were very
similar for more than two dimensions.
Mechanical responses consisted of the number of action potentials occurring during stimulation ( Ç5 s ) minus the number
of spontaneous action potentials occurring during the same time
period immediately preceding stimulation. The criterion for a
suprathreshold mechanical response was an increase or decrease
in firing rate of at least five spikes per 5 s that was ¢2.5 SD of the
spontaneous rate. For both gustatory and mechanical responses,
neurons without spontaneous rate met a second criterion of a
change of firing rate at least 1 spikes / s. The level of significance
for all statistical analyses was set at P ° 0.05 and variances
are SE.
Histological reconstruction
Electrolytic lesions (anodal current, 3 mA, 3 s) were used to
mark recording sites (Fig. 1A). Lesions were made either at the
recording site (36% of the cells), near the recording site on the
same track (191 { 16.7 mm distant; 43%) or on an adjacent track
(21%). The mean diameter of the lesions was 138 { 3.24 mm. At
the end of the recording session, the animal was given a lethal
dose of Nembutal (150 mg/kg) and perfused transcardially with
physiological saline and phosphate-buffered formalin. The brains
were removed and cryoprotected in 20% sucrose phosphate-buffered formalin and frozen sectioned in the transverse plane at 40
mm. Alternate sections were stained for Nissl substance with cresyl
violet and for myelin with the Weil technique (Fig. 1, A and B).
Sections containing lesions were drawn using a computer-based
drawing program (Neurolucida, MicroBrightfield). Locations of
recording sites were reconstructed based on electrode track and
lesion locations and plotted onto standard transverse sections of
the PBN (4 roughly equal rostrocaudal levels). The Weil-stained
sections were used to visualize lesions, and the adjacent Nisslstained sections were used to localize anatomic landmarks includ-
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effectiveness in other neurophysiological studies ( Frank 1991;
Giza et al. 1996; Nejad 1986; Travers and Norgren 1991 ) . To
maximize the specificity of the ‘‘sweet’’ component of this stimulus, however, we used a saccharin concentration near the behavioral preference peak for rats ( Ogawa 1972 ) , which is somewhat
less than the 0.02 – 0.03 M range employed in these other neurophysiological studies.
The taste mixture was first applied to the whole mouth via a
syringe fitted with a blunt needle and to the taste buds within
the circumvallate papilla ( CV ) via a a glass micropipette ( tip
diameter 200 – 300 mm) ( see Frank 1991; Halsell et al. 1993 ) . If
the neuron was responsive to whole-mouth taste stimulation, the
other taste receptor subpopulations [ anterior tongue ( AT ) , nasoincisor duct ( NID ) , foliate papillae ( FOL ) , and soft palate
( SP ) ] were tested specifically using a soft nylon brush. If the
cell was still viable, it was further tested by stimulating the
responsive receptor subpopulation with individual taste stimuli
via a pipette. Approximately 2 ml of stimuli were presented to
the whole mouth via the syringe, and Ç1 ml was presented to
the individual receptor subpopulations via the micropipette. The
pipette was positioned to specifically stimulate the individual
taste receptor subpopulations on the ipsilateral side of the mouth
( Halsell et al. 1993 ) . Stimulation of the CV was optimized by
placing the tip of the pipette into the trench that surrounds this
papilla and contains all CV taste buds. Because FOL taste buds
are distributed among several adjacent folds, the pipette was
positioned near the surface of the tongue so that all folds were
contacted by the tastant and stimulus access to the folds was
facilitated by stretching them open. To stimulate the SP taste
buds, the pipette was positioned in front of the anterior SP so
the fluid would flow down the SP behind the tongue and into the
drain tube. The AT was stimulated by gently pulling the tongue
forward and out of the mouth with the sutures. The pipette was
positioned above the AT so the fluid would drip off the end of
the tongue. The specificity of receptor stimulation was verified
in initial experiments by flowing dye through the pipette. Proper
positioning of the tongue with the sutures and constant suction
through the drain tube prevented the taste fluids from flowing to
adjacent taste receptor subpopulations. During data collection,
the flow of the taste fluids was monitored visually to verify
that the fluid was not contacting fields other than the one being
targeted.
Stimulus delivery via the pipette was controlled by a computeroperated pressure system (Halsell et al. 1993). The timing of fluid
flow was controlled using a programmable spreadsheet and a digital
output interface (Modular Instruments) that triggered opening and
closing of solenoid valves (General Valve). The triggering TTL
pulses were recorded on one channel of a video tape (Vetter) to
be used as stimulus onset/offset markers. The stimulus sequence
consisted of 10 s of no stimulus, and then a continuous flow through
the same pipette consisting of 10 s of water, 10 s of stimulus, and
20 s of water rinse. The interstimulus rest period totalled 1 min.
The stimuli were applied in a varied order.
MECHANICAL STIMULATION. Discrete oral regions also were
stimulated to assess the neuron’s mechanosensitivity. Tactile stimulation consisted of stroking the area of interest with a blunt glass
rod using a series of discrete strokes that lasted for Ç5 s. Areas
routinely tested included the AT, intermolar eminence (IME), hard
palate including the incisal papilla and rugae (HP), buccal wall
(BW), upper and lower molars (UM, LM) and incisors (UI, LI),
FOL, CV, posterior tongue between and behind these papillae
(PT), retromolar mucosa (RM), and SP. The force produced was
not quantified but was firm enough to indent the epithelium without
producing any tissue damage. A subset of neurons also was tested
with a camel’s hair brush to simulate a low-threshold stimulus.
Stimulus onset and offset was indicated by voice and recorded on
video tape.
OROSENSORY RESPONSES IN THE PARABRACHIAL NUCLEUS
923
ing the boundaries of the PBN subdivisions defined by Halsell and
Frank (1991) and Fulwiler and Saper (1984). To ascertain whether
there was a topographic organization of orosensory cells according
to their response properties, the positions of cells were analyzed
in relation to their relative positions along the three anatomic axes
and in relation to their subnuclear locations. Because the number
of neurons in some subnuclei was quite small, an inclusive and
quantitative analysis was feasible only using the former method.
To this end, we compared neurons recorded within the rostral
versus caudal halves of the PBN region we recorded from and
neurons recorded dorsal versus ventral to a line bisecting the brachium conjunctivum. For the mediolateral axis, we divided the
PBN into equal thirds instead of halves, because dividing the PBN
into mediolateral halves would have split the largest group of orosensory neurons. The middle versus the medial and lateral thirds
were referred to as the ‘‘core’’ and ‘‘shell’’ regions, respectively.
Although the mediolateral parcellation was not based on morphological criteria, there was overlap with morphologically defined
subdivisions. The core region generally corresponds to the lateral
half of the central medial subdivision (CM), the ventral lateral
subdivision (VL), as well as portions of the ventral medial and
central lateral subdivisions. The shell corresponds to the dorsal
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medial, external medial (EM), external lateral -inner and -outer
(ELi, ELo) subdivisions, as well as the remaining portions of the
central lateral and ventral medial subdivisions.
RESULTS
General response properties
One-hundred ninety-three single neurons were recorded
from PBN, and 142 of these were isolated for a period of time
sufficient to provide meaningful data. These cells provide the
basis for the present results. The additional neurons were
discarded for technical reasons, e.g., cell isolation was lost
before complete testing was finished. Seventy-five of the
142 responded to stimulation with either the taste mixture
or at least one of the individual tastants and so were classified
as gustatory neurons (G neurons) (Ogawa et al. 1990; Travers and Norgren 1995). There were two subsets of G neurons: one responded to both gustatory and intraoral mechanical stimulation (GM neurons, n Å 55), whereas the other
was not mechanically responsive (G-only neurons, n Å 20).
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FIG . 1. A: photomicrograph of a Weilstained section through parabrachial nucleus (PBN) at rostrocaudal level C (see
Fig. 7). r, lesion in external medial (EM),
that corresponds to recording site for cell
213. m, lesion in ventral lateral (VL), that
corresponds to recording site for cell 212.
B: photomicrograph of adjacent cresyl violet stained section. r, same lesion as in A;
*, lesions centers. Note that a second lesion
was made Ç200 mm ventral to lesion indicated by r in A and B. Scale bar is 200
mm for both A and B. C: record of action
potentials for cell 213 during QHCL stimulation of circumvallate papilla (CV). Small
r, time of water flow on/off; Large r, time
of QHCL flow on/off. Down is flow on
and up is flow off. Scale bar is 5 s. Artifacts
apparent in record occur during solenoid
switching. D: bar graph showing response
of cells 212 ( ø ) and 213 ( j ) in spikes/
second to taste mixture stimulation of different receptive fields. Cell 212 is anterior
tongue (AT)-best but also has a suprathreshold response to foliate papillae
(FOL). Cell 213 is CV-best but also has
suprathreshold responses to nasoincisor
duct (NID) and FOL. E: bar graph showing
response to different taste stimuli on CV for
cell 213 in spikes/second. – – – , criteria
level for this cell. F: peristimulus time histogram of responses to mechanical stimulation of different receptive fields for cell
213. Bins are 500 ms. B, buccal wall; CV,
I, intermolar eminence; PT, posterior
tongue between CV and FOL; SP, soft
palate; S, Na sacccharin; N, NaCl; H, HCl;
Q, quinine hydrochloride.
924
C. B. HALSELL AND S. P. TRAVERS
Response properties: G neurons
GUSTATORY RECEPTIVE FIELDS. Sixty-seven of 75 G neurons were characterized for their responsiveness to stimulation of individual taste receptor subpopulations. Two cells
responded when a tastant was applied to the entire oral cavity
but not to any of the individual receptor subpopulations. For
48 G neurons, the most vigorous taste response arose from
stimulating the anterior oral cavity (AO: AT or NID), and
for 17 G neurons, from the posterior oral cavity (PO: CV,
FOL, or SP). Figure 2 depicts the taste responses elicited
by stimulating individual receptor subpopulations. Responses are separated into four groups defined by whether
the neuron responded to stimulation of a single taste receptor
subpopulation (specific neurons) or to multiple receptor subpopulations (convergent neurons) (Travers and Norgren
1995; Travers et al. 1986) and whether the most vigorous,
‘‘best’’ taste response arose from stimulating the AO or
PO. Within groups, AO-best neurons are ordered by their
responses to the AT and PO-best neurons by their responses
to the FOL (Fig. 2, j ). Compared with PO-best neurons,
AO-best neurons had significantly higher spontaneous (t Å
TABLE
1.
Response properties of G versus M neurons
Modality
n
No. of
Nonspontaneously
Active Cells
G
M
75
54
26 (35)
37 (69)
Spontaneous
Rate*
Evoked
Response
Rate
7.8 (1.15)
2.8 (0.78)
24.5 (2.09)
7.1 (0.89)
Spontaneous and evoked activity in spikes/second. Cells with unstimulated firing rates of °1 spikes/s were classified as nonspontaneously active.
Numbers in parentheses are percents. Rate values are means { SE. Evoked
response is to whole mouth mixture for G neurons and tactile stimulation
of the most responsive oral region for M neurons. * Spontaneously active
cells only.
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4.13, df Å 73, P õ 0.001) and evoked (t Å 3.70, df Å 73,
P õ 0.001) response rates (Table 2). The vast majority of
both AO and PO responses were excitatory. Taste stimulation elicited decrements in firing rate in only two neurons.
Interestingly, both inhibitory responses were evoked by PO
stimulation in neurons that responded best and in an excitatory manner to AO stimulation (Fig. 2, downward-oriented
filled bars). The magnitudes of these inhibitory responses,
however, were very small.
For both AO- and PO-best neurons, most cells (91%)
responded best to stimulation of discrete lingual receptor
subpopulations (AT best, n Å 43; FOL best, n Å 11; CV
best, n Å 4; FOL/CV best, n Å 1). The remaining neurons
responded best to palatal stimulation (NID best, n Å 5; SP
best, n Å 1). Notably, although AT-best neurons comprised
only 66% of G neurons, they accounted for 100% of G-only
neurons compared with just 52% of GM neurons ( x 2 Å
13.74, df Å 1, P õ 0.005).
Overall, about equal proportions of G neurons were specific or convergent, but there was a nonsignificant trend for
PO-best neurons to be convergent more often than AO-best
neurons ( x 2 Å 3.08, df Å 1, P Å 0.079; Table 2). For
neurons that responded to stimulation of more than one taste
receptor subpopulation, there was a tendency for an orderly
pattern of convergence. Almost twice as many convergent
neurons received their two most effective inputs from within
the AO or PO than from both the AO and PO ( x 2 Å 3.62,
df Å 1, P Å 0.057; Table 2). When all suprathreshold responses were taken into account, however, notable convergence between the AO and PO was evident. About equal
numbers of convergent neurons responded to stimulation of
taste receptor subpopulations confined to the AO or PO as
responded to stimulation of fields in both these regions.
GUSTATORY AND MECHANICAL PROPERTIES FOR MULTIMODAL
( GM ) CELLS. GM neurons responded to both taste and me-
chanical stimulation. Interestingly, about half of these neurons exhibited transient ( Ç1-s duration) suprathreshold responses to the onset of the water flow that immediately
preceded stimulus application. Complete information on the
location of the mechanical receptive field was obtained for
45/55 GM neurons. The remaining 10 cells were not used
for this analysis. For 38 of the 45 cells, the optimal receptive
fields for the two modalities were located in the same,
nearby, or apposed oral loci confined to the AO or PO. AObest cells, however, were more likely to receive optimal
multimodal input from precisely the same oral locations (21/
23) than PO-best cells (6/15; P Å 0.001, Fisher’s Exact).
The relative magnitudes of the taste and mechanical responses also were related to whether the neuron responded
more robustly to AO or PO stimulation. Neurons that had
optimal receptive fields for both taste and mechanical stimulation in the AO (AO-only, Fig. 3) tended to respond more
vigorously to taste stimulation, whereas neurons with optimal receptive fields for both modalities in the PO (PO only,
Fig. 3) usually responded more vigorously to mechanical
stimulation or equivalently to the two modalities. Correspondingly, the mean taste:mechanical response ratio for AO
neurons (4.4) was significantly larger than for PO neurons
(0.8; t Å 2.36, df Å 26, P õ 0.001). Neurons that received
mixed AO/PO inputs (AO and PO, Fig. 3) exhibited inter-
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Of the 67 nongustatory neurons, 54 responded to intraoral
mechanical stimulation so were designated as M neurons,
whereas the remaining 13 cells were unresponsive to both
gustatory and mechanical stimulation. Unless otherwise
specified, the properties of the evoked taste responses described below refer to responses elicited by whole-mouth
stimulation with the taste mixture, and mechanical response
properties refer to responses elicited by stroking the most
effective region of the oral cavity.
Spontaneous activity was absent or minimal ( °1 spike/s)
for a smaller proportion of G than M neurons ( x 2 Å 14.4,
P õ 0.005; Table 1). Even among cells with spontaneous
firing, G neurons had significantly higher rates of unstimulated activity than M neurons (t Å 3.94, df Å 64, P õ 0.001;
Table 1). Differences between G-only versus GM neurons
followed this trend. The mean spontaneous rate for spontaneously active cells was higher for G-only (means Å 10.9 {
2.94 spikes/s) than GM neurons (means Å 6.0 { 0.77
spikes/s; t Å 2.11, df Å 47, P õ 0.05). In addition to higher
rates of resting activity, G neurons had significantly higher
rates of evoked activity than M neurons (t Å 5.28, df Å 88,
P õ 0.001; Table 1). There was, however, no significant
difference between the mean taste responses for GM versus
G-only neurons (t Å 0.26, df Å 66, P Å 0.798).
OROSENSORY RESPONSES IN THE PARABRACHIAL NUCLEUS
925
FIG . 2. Responses of 60 neurons to stimulation of individual taste receptor subpopulations. Two whole-mouth–only cells are not shown because
their receptive fields were not localized. Five of 26 cells that only responded
to AT stimulation are also not shown because responses to stimulation
of individual taste receptor subpopulations were not taped during testing.
Responses are in spikes/second and responses for a given cell are aligned
on vertical axis. Neurons are grouped by whether individual cells had
suprathreshold responses to a single (SPECIFIC; 2 groups on left) or to
multiple (CONVERGENT; 2 groups on right) receptor subpopulations.
Neurons are further grouped by whether most effective receptor subpopulation was in anterior (AO; AT or NID) or posterior (PO; FOL, CV or SP)
oral cavity. Within the 2 AO-best groups, neurons are ordered by magnitude
of responses to AT stimulation, and within 2 PO-best groups, neurons are
ordered by magnitude of responses to FOL stimulation. j, suprathreshold
responses; h, responses below threshold.
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mediate taste:tactile ratios (3.1) that were not statistically
different from either the AO- or PO-only groups. Thus taste
stimuli were much more effective in eliciting responses from
AO GM neurons whereas tactile stimulation was actually
slightly more effective for PO GM neurons.
GUSTATORY CHEMOSENSITIVITY. Neural response profiles.
For 58 neurons, individual taste stimuli were applied to each
taste receptor subpopulation effective in activating the cell.
Chemosensitive response profiles or spectra (Frank 1991)
for these neurons were derived by using the most vigorous
response to a given stimulus, regardless of the receptive field
location (Travers et al. 1986). For 82% of the neurons, each
response used in the profile was evoked by stimulation of
the same receptor subpopulation; for the remaining 18%,
responses used for different stimuli arose from different receptor subpopulations. For example, cell 191 received convergent input from the NID, CV, and FOL and responded
to all four stimuli, but responses varied depending on which
receptor subpopulation was stimulated. The optimal responses evoked by QHCl and NaCl arose from the CV,
whereas those evoked by HCl and Na saccharin arose from
the NID and FOL, respectively. Consequently, the chemosensitive response profile for cell 191 included responses
from three different receptor subpopulations.
Figure 4 is a dendrogram depicting the results of a hierarchical cluster analysis for all 58 chemosensitive profiles. The
majority of neurons (48/58) fell into two intercorrelated
clusters of neurons (between-neuron correlations in each
cluster ¢0.82). In one cluster, 38/39 neurons responded
most vigorously to NaCl (N cluster) and in the other cluster,
9/9 responded most vigorously to HCl (H cluster). The
remaining 10 neurons did not separate into major clusters,
although three neuron pairs were intercorrelated as highly
as the N and H clusters. On the other hand, nine of the cells
could be distinguished from neurons in the N and H clusters
on the basis of their greater responsiveness to quinine. All
responded best (n Å 5) or second-best (n Å 4) to quinine.
In contrast, quinine was never the second-best stimulus for
N- or H-cluster neurons. Thus although the nine neurons
with quinine sensitivity were not highly intercorrelated, they
were considered a functional group and, for brevity, designated as the quinine-sensitive group (Q/ group). The last
neuron amalgamated in the dendrogram was distinct and
actually was correlated negatively with the other 57 (correlation distance ú1.0). This was the only cell that responded
optimally to Na saccharin, which was generally a poor stimulus in the present study.
926
TABLE
C. B. HALSELL AND S. P. TRAVERS
2.
Response properties of AO- versus PO-best taste neurons
Modality
Input
RF
G-only
GM
Specific
Convergent
Spontaneous Rate,
spikes/s
Evoked Response
Rate, spikes/s
H
AO
PO
Total
19
0
19
28
18
46
26
5
31
22
12
34
6.8 { 1.07
1.4 { 0.45
5.1 { 0.80
23.9 { 2.73
10.9 { 2.15
19.8 { 2.10
0.5
0.8
0.6
Input is number of cells with suprathreshold input from single (specific) or multiple (convergent) taste receptor subpopulations. Evoked response is
to whole-mouth mixture. Rate values are means { SE. RF, receptive field; AO, anterior oral cavity (anterior tongue, nasoincisor duct); PO, posterior
oral cavity (folate papillae, circumvallate papilla, soft palate); H, breadth-of-tuning measure; G, gustatory; GM, gustatory and intraoral mechanical
responsive neuron.
NaCl- or HCl-best are positioned between the appropriate
N or H clusters and the quinine-best cells, which lie at the
edges of the neural space.
In addition to differences in best (or second best-)-stimulus designation and profile similarity, neurons in these three
groups could be further differentiated on the basis of breadth
of tuning calculated using uncorrected evoked responses and
the entropy measure adapted by Smith and Travers (1979).
An analysis of variance (ANOVA) revealed a significant
main effect for cluster type (F Å 17.39, df Å 2, P õ 0.001;
Table 3). Q/ neurons were tuned more broadly than N- or
H-cluster neurons, and H-cluster neurons were more broadly
tuned than N-cluster neurons. Finally, neurons in the N and
H clusters were differentiable from the Q/ group on the
basis of their receptive field designation. Significantly more
N- and H-cluster neurons were AO-best whereas more Q/
neurons were PO-best (P õ 0.005, Fisher’s Exact; Table 3).
Receptor subpopulation profiles . The preceding analysis
suggested that the various receptor subpopulations are differentially responsive to the four standard tastants used in
this study. The neural response profiles, however, included
only the most vigorous response to a stimulus for a given
neuron and ignored suboptimal responses arising from converging receptor subpopulations. To more directly compare chemosensitivities between receptor subpopulations,
chemosensitive profiles for receptor subpopulations were
FIG . 3. Suprathreshold
evoked
response
(spikes/second above spontaneous) to taste ( j )
and mechanical ( Ω ) stimulation of best receptive
field for 43 individual gustatory and intraoral mechanical responsive (GM) neurons. Neurons are
grouped by whether the cell receives both taste and
mechanical input from only anterior oral cavity
fields (AO only), both AO and PO fields (AO &
PO) or only posterior oral cavity fields (PO only).
Within the groups, the neurons are ordered by the
response to taste. Two GM neurons that responded
to mechanical stimulation of fields in either the AO
or PO and to taste stimulation of only whole mouth
are not included because locations of their taste
receptor subpopulations are unknown.
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Differences between the groups derived by cluster analysis are evident from an inspection of their mean response
profiles (Fig. 5). The N- and H-cluster neurons show strong
peaks for NaCl and HCl, respectively. On average, N-cluster
neurons responded 2.7 times as well to NaCl, and H-cluster
neurons responded 1.9 times as well to HCl than they did
to the next best stimulus. Although the Q/ group likewise
had a mean profile exhibiting a peak for QHCl, the peak
was not pronounced. On average, Q/ neurons responded
only 1.4 times better to QHCl than to the next best stimulus.
The inset in Fig. 4 is a multidimensional scaling plot that
graphically summarizes relationships among these neural
groups. Except for N- and H-best neurons lying within their
respective clusters (outlined with dashed lines, Fig. 4, inset),
cells are labeled by best stimulus. Neurons in the N and H
clusters form tight groups virtually homogeneous with regard to best-stimulus designation with two exceptions. These
exceptions were the last two neurons amalgamated into the
N cluster. One of these N-cluster neurons responded best to
HCl and the other responded equally well to NaCl and HCl
(n Å H, Fig. 4, inset). This latter neuron (cell 213) was also
unusual in that it had a relatively large sideband response to
quinine (Fig. 1E). In the multidimensional scaling plot, the
nine Q/ neurons do not form a tight group, consistent with
their greater heterogeneity. On the other hand, Q/ neurons
do not intermingle in the N or H clusters, even when they
share the same best stimulus. Instead, Q/ neurons that are
OROSENSORY RESPONSES IN THE PARABRACHIAL NUCLEUS
927
calculated using all suprathreshold responses. For specific
neurons ( n Å 44 ) , responses from one subpopulation contributed to the analysis, whereas, for convergent neurons,
responses from two ( n Å 12 ) or three ( n Å 4 ) subpopulations were used, resulting in a sample size for receptor
subpopulation profiles ( n Å 80 ) that exceeded the sample
of neurons ( n Å 58 ) . Mean responses to the four standard
stimuli for each of the receptor subpopulations appear in
Table 4.
Comparisons were first made between AO (AT and NID,
n Å 52) and PO (CV, FOL, SP, n Å 28) responses, then
between receptor subpopulations within the AO and PO. For
the AO/PO comparison, an ANOVA yielded a significant
interaction between oral region and stimulus (F Å 17.44,
df Å 3, P õ 0.005), suggesting that stimulus efficacy varied
depending on whether a tastant was applied to the AO or
PO. Posthoc Bonferroni adjusted Student’s t-tests revealed
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that NaCl and HCl responses were significantly larger after
AO than PO stimulation (t Å 4.0, df Å 78, P õ 0.001 and
t Å 3.0, df Å 78, P õ 0.005 for NaCl and HCl, respectively).
In contrast, QHCl elicited a larger response from the PO
than AO (t Å 2.10, df Å 78, P õ 0.05). Na saccharin elicited
similar (small) responses, regardless of whether the AO or
PO was stimulated.
An ANOVA analyzing individual receptor subpopulations
within the AO and PO also yielded a significant interaction
between stimulus and receptor subpopulation (F Å 13.69,
df Å 9, P õ 0.001; Table 4). NaCl elicited a larger response
when applied to the AT than NID (t Å 5.50, df Å 50, P õ
0.001), but there were no differences between AT and NID
responses to the other three stimuli. There was also no significant variability in chemosensitivity for the CV versus
FOL. Only one profile was available for the SP, so not
enough data were available for comparison, but this profile
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FIG . 4. Dendrogram derived from hierarchical cluster analysis on the response spectra of 58 G neurons. Cells are labeled
with taste qualities eliciting suprathreshold responses (ordered from most-effective to least-effective quality: N, NaCl; H,
HCl; S, Na saccharin; Q, quinine), by whether they responded optimally to anterior (A) or posterior (P) oral cavity
, Pearson interneuron correlations ú 0.82 (distance õ0.18). Two main clusters of
stimulation and by cell number.
neurons at this correlation level are labeled: N, NaCl cluster; H, HCL cluster. Inset: map derived from multidimensional
scaling of interneuron correlations. Cells that are members of N cluster and H clusters are outlined. Two N-cluster neurons
that are not NaCl-best are labeled with their best stimulus designation [H is cell 81; N is cell 213 (see Fig. 1)]. Ten neurons
not grouped into true clusters are labeled with their best stimulus designation and include 9 Q/ neurons and the lone S
neuron.
928
C. B. HALSELL AND S. P. TRAVERS
TABLE
3.
Properties of neuron classes
Best RF
Neuron Classes
Breadth (H)
AO
PO
S
N
H
Q
0.3
0.5
0.7
0.9
0
33
6
3
1
6
2
6
Breadth (H), breadth-of-tuning measure; H, H-cluster neurons; N, Ncluster neurons; S, S-best neuron; Q, quinine-sensitive neurons (Q/).
was from a SP-best neuron that was the same lone S-best
neuron described earlier.
Response properties: M neurons
Sensitivity to the different oral regions was determined
for 47/54 M neurons. For the other six M neurons, receptive
field data were incomplete so were not used in the following
analysis. Twenty-nine M-neurons responded best to AO
(IME, IP, HP, BW, UM, LM, UI, LI) stimulation and 18 to
PO (FOL, CV, PT, RM, SP) stimulation. In contrast to G
neurons, there was no significant difference between the
magnitude of evoked responses in AO-best versus PO-best
neurons (F Å 0.877, df Å 7, P Å 0.536). Sixteen M neurons
responded to stimulation of a single oral region, seven to
PO sites (2 PT, 2 SP, 3 CV/FOL) and nine to AO sites (5
HP, 2 LI, 1 NID, 1 BW). Most M neurons (31/47), however, responded to input from multiple oral regions and are
referred to as M-composite neurons. The term composite
was chosen instead of convergent because the inference of
central convergence is more uncertain for M than G neurons
due to the continuous distribution of oral mechanoreceptors
compared with the discrete locations of different taste receptor subpopulations. For example, although central convergence is the most likely explanation for a neuron that responds to mechanical stimulation of both the tongue and
palate, either convergence or peripheral branching is a plausible mechanism for a neuron that responds to stimulation
of both the hard and soft palate, because these oral loci are
directly adjacent to one another (see also Travers and Norgren 1995).
Figure 6 depicts responses elicited by stimulating individual oral regions for the 31 M-composite neurons. Neurons
were divided into four groups: those with receptive fields
restricted to the AO (AO Composite, Fig. 6) or PO (PO
Composite, Fig. 6) and those that received input from both
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Topographic organization
BY MODALITY. Recording site locations
were reconstructed on one of four standard sections in the
transverse plane (Fig. 7). A differential distribution was
evident along the rostrocaudal axis for the cells that were
or were not responsive to the stimuli used in this study.
More unresponsive neurons were located in the rostral half
(Fig. 7, levels C and D) of the PBN region we recorded
from, and more G and M neurons were in the caudal half
ORGANIZATION
4. Mean responses to stimulation of receptor
subpopulations with standard taste stimuli
TABLE
Stimulus
S
N
H
Q
AT
0.8
24.5
10.4
00.4
{
{
{
{
NID
0.63
2.31
1.58
0.85
1.4
4.6
7.9
2.3
{
{
{
{
1.09
4.0
2.74
0.87
CV
1.6
5.0
3.1
5.2
{
{
{
{
1.19
4.35
2.98
1.61
FOL
1.5
5.3
3.3
4.4
{
{
{
{
0.99
3.6
2.47
1.33
Values are means { SE in spikes per second. H, HCl; N, NaCl; Q,
quinine; S, na saccharin.
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FIG . 5. Mean evoked responses to each of 4 tastants for each cluster or
group classification (N, NaCl cluster; H, HCl cluster, Q/, quinine sensitive
group; S, Na saccharin-best cell). Responses are in spikes/second and error
bars are means { SE. Number of neurons comprising each cluster or group
with best receptive fields in either AO or PO is indicated.
halves of the oral cavity but responded best to AO (Both
Composite: AO Best, Fig. 6) or PO (Both Composite: PO
Best, Fig. 6) stimulation (Travers and Norgren 1995). Despite their complexity, the configurations of these receptive
fields were orderly. Many more composite neurons received
their two most effective inputs from within the AO or PO
(n Å 24) compared with both the AO and PO (n Å 7; P õ
0.05, Fisher’s Exact), although about equal numbers of Mcomposite neurons exhibited suprathreshold responses to
stimulation of both the AO and PO.
As observed for G neurons, mechanical stimulation usually elicited excitatory responses in M neurons (Fig. 6, filled
pyramid-shaped bars). Inhibitory responses were only noted
in four cells. One M neuron responded in a purely inhibitory
manner; stimulation of several AO regions, the AT, incisal
papillae, and rugae (Fig. 6, open pyramid-shaped bars, AO
Composite) each evoked response decrements. Another cell
received inhibitory input from the PO but excitatory input
from the AO, and the response magnitudes of the inhibitory
and excitatory responses were comparable (Fig. 6, Both
Composite: AO Best). The remaining two neurons also received antagonistic inputs from the AO and PO. In these
cells, AO stimulation elicited inhibitory responses and PO
stimulation elicited excitatory responses but the magnitudes
of the excitatory responses far exceeded those of the inhibitory responses (Fig. 6, Both Composite: PO Best).
OROSENSORY RESPONSES IN THE PARABRACHIAL NUCLEUS
929
(Fig, 7, levels A and B; x 2 Å 12.67, P õ 0.001; Table
5). Although as a group, orosensory neurons were more
numerous in caudal PBN, this depended on modality (Fig.
7, Table 5). G neurons were located predominantly caudally
but M neurons were distributed evenly between the rostral
and caudal halves of PBN ( x 2 Å 14.59, P õ 0.001). Indeed,
at the most rostral level (Fig. 7, level D), the only orosensory
neurons were M neurons.
Distribution along the mediolateral axis was also related
to modality (Fig. 7, Table 5). More G neurons were located
in the mediolateral middle third or core (demarcated by
– – – in Fig. 7) than the medial and lateral thirds or shell,
but more M neurons were in the shell than core ( x 2 Å 16.99,
P õ 0.001). Nearly one-third of M neurons were clustered
in the lateral shell at level C, within the EM and Eli subdivisions. In contrast, the majority of G neurons in the core were
located as a tight cluster in CM and VL and in the cell
bridges that span the superior cerebellar peduncle between
FIG . 7. Location of neurons plotted on
line drawings of 4 standard transverse levels through PBN based on modality and
best receptive field. Level A is most caudal
and level D, most rostral. Distance between
levels A and B, B and C is Ç200–250 mm
each and between levels C and D is 300–
350 mm. Filled symbols are AO-best and
open symbols are PO-best. s and ●, gustatory neurons (G neurons); m and n, oral
somatosensory neurons (M neurons). Unresponsive cells are indicated by small ●.
– – – , division of PBN into 3 equal mediolateral segments (core and surrounding
shell). Dorsal is toward top, and lateral
is to right. Inset: PBN subdivisions. CL,
central lateral; CM, central medial; DM,
dorsal medial; EL, external lateral; ELi, external lateral-inner; ELo, external lateralouter; EM, external medial; IL, internal lateral; VL, ventral lateral; VM, ventral medial; KF, Kolliker-Fuse nucleus; LC/Me5,
Locus Coeruleus and Mesencephalic trigeminal nucleus. Scale bar is 0.5 mm.
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FIG . 6. Responses of 31 M-composite
neurons (suprathreshold responses to stimulation of multiple individual oral receptive
fields). Responses are given as a ratio of
suprathreshold responses to each field for
a given cell with the most vigorous response set as maximum y-axis value and
responses below threshold set at 0. Individual neurons are aligned along rows and are
labeled with cell number. Individual receptive fields are aligned along columns.
Neurons are grouped by whether the cell
receives input only from anterior oral cavity receptive fields (5 fields on right, AO
COMPOSITE), only from posterior oral
cavity (4 fields on left, PO COMPOSITE),
from both anterior and posterior oral cavities but with most effective receptive field
in AO (BOTH COMPOSITE: AO BEST)
or PO (BOTH COMPOSITE: PO BEST).
j, excitatory responses; h, inhibitory responses. AI, anterior tongue and incisal papilla; I, lower incisors; HP, hard palate; M,
upper and lower molars; A/, other anterior
oral cavity regions (e.g., intermolar eminence, buccal wall); CF, circumvallate and
foliate papillae; RM, retromolar mucosa;
P/, other posterior oral cavity fields (e.g.,
posterior tongue).
930
TABLE
C. B. HALSELL AND S. P. TRAVERS
5.
Topographic organization summary
Modality
RF
PBN Division
G
M
U
AO
PO
Rostral half
Caudal half
12
50
21
16
11
2
15
52
18
14
Core
Shell
49
13
14
23
7
6
52
15
11
21
Dorsal half
Ventral half
23
39
20
17
7
6
26
41
17
15
G, G neurons; M, M neurons; U, unresponsive neurons; PBN, parabrachial nucleus.
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6. Numbers of different neuron types within CM/VL
versus EM/ELi
TABLE
G neurons
AO-best
PO-best
N-cluster
H-cluster
Q/
S-best neuron
M neurons
U neurons
CM/VL
EM/ELi
Other
42
30
8
29
4
4
1
6
2
6
0
6
1
1
2
0
8
1
14
16
2
6
4
1
0
22
10
Other, subdivisions other than CM/VL or EM/ELi. CM, central medial;
VL, ventral lateral; EM, external medial; ELi, external lateral-inner.
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these two subdivisions (‘‘waist’’ region) at level B. G neurons in the shell were somewhat more scattered, occupying
the dorsal medial, CM, VL, central lateral, and EM and ELi
subdivisions, although almost half were concentrated in EM
and Eli. The G neurons in EM and ELi were GM neurons.
In contrast to the statistically significant distribution of
modality along the rostrocaudal and mediolateral axes, there
was only a tendency for such an organization along the
dorsoventral axis. G neurons were somewhat more frequent
ventrally compared with M neurons, which were distributed
evenly along the dorsoventral axis of PBN ( x 2 Å 2.712,
P Å 0.1; Fig. 7, Table 5).
OROTOPIC ORGANIZATION. A differential distribution along
the rostrocaudal axis was also apparent for receptive field
(Fig. 7, Table 5). Collapsing across G and M neurons, most
AO-best neurons were found caudally compared with just
under half of the PO-best neurons ( x 2 Å 11.2, df Å 1, P Å
0.001). When considered alone, G neurons exhibited a similar orotopic arrangement modified by the overriding tendency for G neurons to be located caudally. More than six
times as many AO-best G neurons were located caudally
versus rostrally, compared with only 1.7 times as many PObest neurons (P Å 0.006, Fisher’s exact). Although PO-best
G neurons in caudal PBN outnumbered those in rostral PBN,
the proportion of G neurons that were PO-best at a given
level actually increased at successively more rostral locations: level A, 8.3%; level B, 24.3%; and level C, 50%. The
trend for a reversed orotopy was also evident for M neurons,
with three times as many PO-best M neurons being located
rostrally as caudally whereas slightly more AO-best neurons
were located caudally compared with rostrally ( x 2 Å 3.82,
df Å 1, P Å 0.051).
There was also a mediolateral orotopy for receptive field
(Fig. 7, Table 5). Collapsing across G and M neurons, many
more AO-best neurons were encountered in the core than
shell whereas the reverse was true for PO-best neurons ( x 2
Å 17.50, df Å 1, P õ 0.001). This mediolateral orotopy,
however, only reflected the distribution of G neurons:
44/46 AO-best G neurons versus 5/16 PO-best G neurons
in the core (P õ 0.001, Fisher’s Exact). Less than half of
the M neurons were found in the core, regardless of whether
they were AO- or PO-best ( x 2 Å 0.001, df Å 1, P Å 0.97).
The majority of AO-best neurons were located as a tight
cluster in the CM and VL subdivisions and waist region
(Fig. 7, filled symbols). There were a few AO-best cells
(mainly M neurons) distributed in other subdivisions, but
they were exceedingly rare in EM/ELi; i.e., these subdivisions contained only 1 of the 67 AO-best neurons. PO-best
neurons were more scattered between subdivisions than AObest neurons (Fig. 7, open symbols), but a cluster of PObest G and M neurons, accounting for about one-third of all
neurons responding optimally to PO stimulation were evident in EM and ELi (level C, Fig. 7). Thus with one exception, each neuron in EM and ELi was PO-best.
There was no clear evidence for orotopy along the dorsoventral axis for AO- versus PO-best neurons (Table 5).
Other aspects of receptive field configuration were not reflected in anatomic distribution. For example, no topography
was evident for cells receiving input from single versus multiple oral sites or neurons with input restricted to the AO or
PO versus those that had inputs from both oral regions.
CHEMOTOPIC ORGANIZATION. Because more than two-thirds
of the neurons that we characterized for chemosensitivity
were N-cluster neurons, definitive conclusions regarding the
topographic arrangement of chemical sensitivity in PBN cannot be drawn from the present data. Although not statistically
significant, a greater number of each neuron class were located caudally than rostrally. On the other hand, more Nand H-cluster neurons were located ventrally and within the
core, whereas Q/ neurons were about evenly distributed
dorsoventrally and between the core and shell.
SUBNUCLEAR ORGANIZATION. One goal of the present study
was to determine if there was a relationship between morphologically defined PBN subdivisions and orosensory response characteristics. The evidence presented above suggests that, although orosensory neurons were not confined
to specific PBN subdivisions, there were two separate foci
of orosensory cells. One was centered in the CM/VL subdivisions and the other in the EM/ELi subdivisions, and these
subnuclei were dominated by distinctive cell types (Table
6). CM/VL was populated mostly by G neurons (both GM
and G-only neurons), which were AO-best, with 76% belonging to the N cluster. In contrast, EM/ELi was populated
by both M and G PO-best neurons, with all the G neurons
being GM neurons. Only four neurons in this subdivision
were characterized for chemosensitivity, but only one was
a N-cluster cell. Fig. 1 depicts recording sites and response
properties of two PBN G neurons (cells 212 and 213) that
typify some of these relationships. Both cells were recorded
at the same rostrocaudal PBN level (about level C) but
neuron 213 was located in EM and neuron 212 was in VL
OROSENSORY RESPONSES IN THE PARABRACHIAL NUCLEUS
(Fig. 1, A and B). Correspondingly, neuron 213 was PObest (specifically CV-best, Fig. 1, D). Although this neuron
was classified as a N-cluster neuron, it was the last neuron
amalgamated in this cluster and not typical of cells in this
group. It responded optimally and equally to NaCl and HCl,
but it also responded quite vigorously to quinine (Fig. 1,
E). As was typical of PO-best G neurons, this cell could be
further classified as a GM neuron, and it responded equivalently or more robustly to mechanical stimulation of several
PO sites (Fig. 1, F). In contrast, neuron 212 was an
AO(AT)-best G-only neuron that responded well to NaCl
(Fig. 1, D).
DISCUSSION
Receptive field properties
The substantial convergence of input from different taste
receptor subpopulations and oral regions onto both G and M
neurons reported herein supports previous reports of spatial
convergence at several levels of the central gustatory pathway, from NST to cortex (Hayama et al. 1987; Norgren
and Pfaffmann 1975; Ogawa and Hayama 1984; Ogawa and
Nomura 1988; Ogawa et al. 1982, 1992a,b; Sweazey and
Bradley 1989, 1993; Travers and Norgren 1995). Numerous
cells responsive to both gustatory and mechanical stimulation similar to those in the present study also have been
reported in these earlier studies and may represent another
aspect of convergence. However, some of this dual responsiveness may merely reflect the multimodal responses reported in peripheral fibers (discussed in Travers 1993).
Our proportion of convergent G neurons (52%) falls
within the large range reported for PBN cells (24–61%)
(Hayama et al. 1987; Norgren and Pfaffmann 1975; Ogawa
et al. 1982), a range that may be attributed partially to
differences in methods of stimulation and data analysis. For
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example, responses arising from the CV and FOL often are
stimulated or analyzed as a single field, thus underestimating
the amount of convergence between these two lingual fields.
In the present study, a significant proportion (15%) of G
neurons received both CV and FOL input, a clear instance
of central processing, because single glossopharyngeal nerve
fibers do not respond to stimulation of both papillae (Frank
1991).
For both G and M neurons, orosensory convergence onto
pontine neurons was orderly. A greater amount of convergence occurred between inputs within the AO or PO than
between these oral regions. A similar organization has been
reported by this laboratory for NST neurons (Travers and
Norgren 1995; Travers et al. 1986), but except for one report
of mechanically sensitive neurons in the sheep NST
(Sweazey and Bradley 1989), other reports of central convergence in gustatory relays have not noted this pattern
(Hayama et al. 1985, 1987; Ogawa et al. 1984). The lack
of systematic convergence in other studies may be mainly
a matter of definition. Receptive fields typically are defined
simply by the presence or absence of suprathreshold responses. The orderliness observed in PBN was dependent
on comparing the relative magnitudes of responses arising
from different receptive fields. When all suprathreshold responses were treated equivalently, no orderly pattern
emerged in the present data either. Orderliness also was
noted for across-modality convergence. The taste and tactile
receptive fields of most GM neurons were both restricted to
the AO or PO. A similar organization was found for dually
responsive NST neurons, such that gustatory and mechanical
receptive fields showed substantial spatial overlap (Travers
and Norgren 1995).
Although receptive fields in NST and PBN resembled one
another, there was evidence for further processing at the
higher level, at least for G neurons. When the present data
were compared with summarized data from two comparable
NST studies from this laboratory (Travers and Norgren
1995; Travers et al. 1986), a trend for increased integration
was suggested. Although proportions of convergent neurons
were similar at the two levels (53% in NST; 48% in PBN),
differences emerged when the details of receptive field configuration were assessed. If receptive fields were defined
using all suprathreshold inputs, 69% of medullary neurons
had receptive fields within the AO or PO, but in PBN, only
41% of the cells exhibited these confined receptive fields
( x 2 Å 5.41, df Å 1, P Å 0.015). Similarly, there was a
trend for more medullary (83%) than pontine (65%) neurons
to receive their two most effective inputs from the same half
of the oral cavity ( x 2 Å 3.48, df Å 1, P Å 0.062). On the
other hand, no significant difference was apparent in patterns
of convergence for NST (Travers and Norgren 1995) versus
PBN M neurons, though data from fewer NST cells were
available for comparison. Almost identical proportions of
NST and PBN M neurons (45.7 and 46.9%, respectively,
x 2 Å 0.009, df Å 1, P Å 0.924) had confined suprathreshold
receptive fields. If there was any difference in the two levels,
it was a slight trend in the direction opposite to that for G
neurons when inputs from the two most effective receptive
fields were analyzed; 66% of NST versus 80% of PBN neurons had confined optimal receptive fields ( x 2 Å 1.758,
df Å 1, P Å 0.185). The lack of increased integration for
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The results of the present study support a functional distinction between sensory input arising from the anterior and
posterior oral cavities within PBN. Significant differences
were noted in the spontaneous and evoked response rates
and chemosensitive profiles of neurons receiving optimal
input from AO or PO receptor subpopulations, in convergence patterns across receptor fields and modalities and in
the topographic organization of AO- and PO-best neurons
within PBN subdivisions. The AO/PO distinction appears
to be conserved generally from the periphery through the
NST and PBN and possibly at the thalamic and cortical
levels (vide infra) and may represent an underlying organizing principle throughout the gustatory pathway.
The higher spontaneous rate noted in the present study
for AO-best neurons than PO-best neurons may be centrally
mediated because there is no substantial difference in spontaneous rates of chorda tympani and glossopharyngeal fibers
(Boudreau et al. 1987; Frank 1991; Frank et al. 1988). That
larger taste responses arise from AO-best than PO-best neurons is consistent with a previous report of an unquantified
‘‘smaller’’ taste response within the PBN arising from stimulating the AT versus the rest of the mouth (Norgren and
Pfaffmann 1975) and is similar to our previous observations
in the NST (Travers and Norgren 1995).
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C. B. HALSELL AND S. P. TRAVERS
Response properties
GUSTATORY CHEMOSENSITIVITY. In general, the chemosensitivity of different groups of PBN neurons was consistent
with predictions based on their receptive field characteristics
and known sensitivities of peripheral taste fibers. The majority of N neurons received their strongest input from the AO,
and most of these responded only to AT stimulation. NaCl
also elicited a significantly larger response from the AT than
the other taste receptor subpopulations. These relationships
mirror the peripheral responsiveness of gustatory afferent
nerves (Boudreau et al. 1987; Frank 1991; Frank et al. 1983;
Nejad 1986). The highly intercorrelated, relatively narrowly
tuned AT-best N neurons we observed were similar to types
previously reported in hamster PBN (Smith et al. 1979,
1983), NST-PBN projection neurons (Monroe and Di Lo-
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renzo 1995; Ogawa et al. 1984), and rodent chorda tympani
fibers and geniculate ganglion cells (Boudreau et al. 1983;
Frank et al. 1983; Smith et al. 1979, 1983).
The AT/NaCl neurons recorded in the present study may
comprise the pontine substrate for a conserved, amiloridesensitive, AT-mediated pathway that demonstrates a striking
sensitivity to sodium (Bernstein and Taylor 1992; Formaker
and Hill 1991; Giza and Scott 1991; Hettinger and Frank
1990; Ninomiya and Funakoshi 1988; Scott and Giza 1990).
This pathway has been suggested to be necessary for the
discrimination of sodium and involved in sodium appetite
and is probably modifiable based on the homeostatic state
of the organism (Contreras and Frank 1979; Jacobs et al.
1988; Spector and Grill 1992; Sollars and Bernstein 1992).
Interestingly, PBN lesions that abolish the adaptive change
after sodium depletion appear to be effective only when the
lesions are centered in the CM/VL PBN subnuclei (Flynn
et al. 1991; Hill and Almli 1983; see also Spector 1995),
the location where N neurons were most numerous in the
present study. This is also the PBN location where expression of the immediate early gene c- fos is observed when
rats ingest 0.2 M NaCl (Yamamoto et al. 1993). When NaCl
is presented with amiloride, however, c- fos is not expressed
in this area. Preliminary electrophysiological evidence from
our lab supports the preferential amiloride-induced suppression of NaCl-evoked responses in N-cluster neurons in PBN.
Using a modification of the procedure of Hettinger and Frank
(1990), we found that the responses of N-cluster, AT-best
neurons that were evoked by NaCl were reduced by 49%
after amiloride application, but the comparable reduction in
H-cluster neurons was only 27% (unpublished observations). This reduction is similar to that found in NST (Giza
and Scott 1991), although attenuated compared with chorda
tympani fibers (Hettinger and Frank 1990).
One caveat regarding the specificity of the N-cluster neurons in the present study, however, needs to be mentioned.
At odds with the current findings, a previous study from this
lab found that a subset of AT-responsive NST neurons that
were sensitive to sodium also responded strongly to NID
stimulation, usually to sucrose (Travers et al. 1986). In the
present study, we used Na saccharin instead of sucrose and
obtained poor responses to this sweet tastant (vide infra).
Thus it seems possible that some of the apparent AT-only
NaCl-best neurons observed here might have exhibited a
sensitivity to palatal stimulation with sweet stimuli had a
more effective representative tastant been employed. Indeed,
in chronic recording studies, many sodium-best PBN neurons exhibit significant sideband responses to sweet stimuli
(and vice versa), although narrowly tuned NaCl-best neurons are also evident (Nishijo and Norgren 1990).
In the present study, H neurons also comprised a coherent
cluster. H neurons usually responded optimally to HCl but
also responded to NaCl. In contrast, although N neurons also
responded to HCl, the response to the sideband stimulus
was smaller. Correspondingly, H neurons were tuned more
broadly than N neurons (Table 3). Neurons resembling the
H-cluster neurons in the present study have been observed
frequently in other studies of brain stem taste processing
(Chang and Scott 1984; Di Lorenzo and Schwartzbaum
1982; Giza and Scott 1991; Ogawa et al. 1987; Travers and
Smith 1979 1984). The small proportion of PO-best units
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PBN M neurons is consistent with a more important role for
stimulus localization for the somatosensory compared with
the gustatory system.
Despite the increase in AO/PO convergence for PBN gustatory neurons, the orderliness of the receptive field organization of both G and M neurons remained a striking feature
of PBN orosensory cells. The functional significance of this
organization is not certain but may provide part of a mechanism that underlies the spatiotemporal control of the transport of ingesta from the anterior to posterior oral cavity
and then through the pharynx and successive regions of the
alimentary canal, as suggested for the similar functional organization in NST (Altschuler et al. 1989, 1991; Sweazey
and Bradley 1989; Travers 1993). In addition, the limited
convergence between certain sets of taste receptor subpopulations, e.g., the AT and CV, may be necessary for maintaining central separation in the processing of tastants, such
as salt and quinine, that are differentially effective for these
groups of receptors.
The functional significance of spatial convergence and
dual taste/mechanical sensitivity is unclear. The extensive
convergence of taste and tactile information suggests a circuitry where intraoral tactile information can influence taste
information processing or vice versa. Because most convergence involves multiple excitatory responses, a logical prediction might be that natural feeding conditions lead to simultaneous activation of different oral regions and that the
resulting signals are summed centrally to produce more vigorous responses. One previous study compared separate and
simultaneous stimulation for 11 convergent gustatory NST
neurons and suggested that the situation is considerably more
complicated than this simple prediction (Sweazey and Smith
1987). Indeed, similar to taste mixture interactions (Travers
and Smith 1984; Vogt and Smith 1993a,b), linear summation was rarely observed. Further experiments are required
to gain insight into this question. In particular, it will be
interesting to analyze differences in integration between different taste bud groups, because some findings have suggested inhibitory interactions between the AO and PO (Halpern and Nelson 1965; Lehman et al. 1995; Miller and Bartoshuk 1991, but see Dinkins and Travers 1996). A hint of
such an interaction was evident in a few neurons in the
present study in which antagonistic responses were evoked
by AO versus PO stimulation.
OROSENSORY RESPONSES IN THE PARABRACHIAL NUCLEUS
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to the representative sweet stimulus, Na saccharin. Consistent with the robust responsiveness to sugars and behaviorally similar stimuli exhibited by the greater superficial
nerve (Nejad 1986), this lone S-best neuron responded most
vigorously to stimulation of SP taste receptors on the Geschmacksstreifen. Aside from this match in sensitivities, the
generally poor saccharin response in the present study is
perplexing. We routinely stimulated each of the rat taste
receptor subpopulations exhibiting good sensitivity to sweeteners; i.e., the hard and SP (Nejad 1986; Travers and Norgren 1991; Travers et al. 1986) and posterior tongue (Frank
1991). It is possible that a bias against isolating neurons
responsive to these tastants may have existed due to mixture
suppression effects when we employed our quaternary taste
mixture to ‘‘search’’ for responsive neurons. There is evidence for suppression between qualitatively different stimuli
in binary mixtures, specifically suppression of sugar-evoked
responses by quinine or acid (Travers and Smith 1984; Vogt
and Smith 1993a,b). Although our previous studies in NST
revealed a sizable population of cells responsive to sweeteners despite using mixtures as a search stimuli, those mixtures
contained 0.3–1.0 M sucrose: concentrations which are
probably more effective than the Na saccharin concentration
(0.01 M) in the present study (e.g., see Travers and Norgren
1991). Thus although it may not completely explain our
results, a bias against sampling cells optimally responsive
to sweeteners may have existed due to the additive effects
of mixture suppression and a suboptimal representative stimulus. These same factors could have contributed to the relatively poor palatal response. Only 9% of the cells in the
current investigation responded best to palatal stimulation,
compared with 27–31% in previous NST investigations in
which 1.0 M sucrose was used instead of saccharin (Travers
and Norgren 1995; Travers et al. 1986).
TACTILE RESPONSES. The responses of the mechanical neurons recorded in the present study were generally similar
to those reported by Ogawa and colleagues at the pontine,
thalamic, and cortical levels (Nomura and Ogawa 1985;
Ogawa et al. 1982, 1984, 1987). The percentage of M neurons recorded in the present study (42%) was also similar
to that reported by Ogawa and colleagues in the PBN (mean Å
32%) (Ogawa et al. 1982, 1987) using similar stimulating
techniques. Because the NST also contains M neurons and
is the source of a robust afferent PBN projection, a logical
assumption would be that PBN M neurons simply receive
input from the analogous neuronal population in NST. Several experiments, however, raise questions regarding the
connectivity of PBN M neurons. An antidromic stimulation
study demonstrated that only 13% of NST-PBN projection
neurons were M neurons; the remaining majority were tasteresponsive cells (Ogawa et al. 1984). This physiological
evidence suggesting only a sparse NST-PBN M neuron projection is supported by both anterograde and retrograde tracing data. After injections of biocytin into the lateral, mechanically responsive NST, there was only sparse PBN terminal
labeling, compared with much denser labeling after similar
injections into the more medial gustatory-responsive NST
(Becker 1992). Complimentary results were obtained with
Fluorogold injections into PBN (Halsell et al. 1996). Many
more NST neurons were labeled retrogradely in the more
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classified in the H cluster (Table 3) is somewhat surprising
in light of the fact that the glossopharyngeal nerve contains
a high proportion of fibers highly responsive to HCl (Frank
1991). However, HCl-best cells are also common in the
chorda tympani nerve and the broadly tuned average profile
for H neurons in the present study bears a greater resemblance to their chorda tympani than glossopharyngeal counterparts, given that chorda tympani H fibers are tuned more
broadly (Boudreau et al. 1983; Frank 1991; Frank et al.
1983, 1988). In fact, in contrast to the average response
profile, the two H-best neurons that received optimal input
from the PO exhibited relatively specific responses to HCl.
The third chemosensitive group in the present study exhibited a heightened response to quinine. More Q/ neurons
were PO-best than AO-best, consistent with the relative sensitivities of the glossopharyngeal versus chorda tympani
nerves (Frank 1991; Frank et al. 1983). On the other hand,
in contrast to the narrowly tuned quinine-best fibers observed
in the glossopharyngeal nerve, the Q/ neurons that we recorded were the most broadly tuned of all the PBN groups.
If these Q/ PBN neurons are central recipients of information from glossopharyngeal Q units, the responses are transformed dramatically at the second-order relay. The apparent
transformation in neural responsiveness to quinine could be
due partially to convergence, because, for most of the Q/
neurons, responses from two or three receptor subpopulations contributed to the chemosensitive profiles. Convergence is probably an insufficient explanation for the attenuation of quinine specificity, however, because most of Q/
unit profiles were composites of similar profiles from the
CV and FOL. It is somewhat difficult to compare the Q/
neurons in the present study with quinine-responsive neurons
in other central recording studies. Although quinine-best
neurons have been reported at all levels of the rodent central
taste neuraxis, they tend to comprise a small percentage of
recorded cells, and their properties are variable or incompletely described. Indeed, in many investigations, even when
whole-mouth stimulation or chronic recording techniques
were used, such cells constituted õ5% of the population
(e.g., Giza and Scott 1991; Nishijo and Norgren 1991; Nomura and Ogawa 1985; Norgren and Pfaffmann 1975;
Ogawa et al. 1987; Ogawa and Nomura 1988; Ogawa et al.
1982, 1987; Travers et al. 1986; Yamada et al. 1990). Two
studies of rat cortex, however, reported proportions of quinine-best neurons comparable with other best-stimulus
classes, though absolute numbers of cells were small. In one
study, quinine-best neurons were similar to the cells we
observed in exhibiting very broad tuning and relatively low
response rates (Ogawa et al. 1992a), whereas in the other
investigation, they were relatively narrowly tuned and had
comparable response rates (Yamamoto et al. 1989). Clearly,
much remains to be learned about the central representation
of bitter-tasting stimuli. The lack of more robust central
responses to this class of stimuli is somewhat puzzling (Norgren et al. 1989) but observations in this lab suggest that
PO-responsive neurons are more difficult to isolate than AOresponsive cells (Halsell et al. 1993; Travers and Norgren
1995; M. Dinkins and S. P. Travers, unpublished observations), which may make it problematic to obtain a representative sample of PO cells, including quinine-best neurons.
Only one neuron in the present study responded optimally
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C. B. HALSELL AND S. P. TRAVERS
Topographic and subnuclear organization in PBN
When sensitivities of neurons were compared with their
locations, a clear anatomic organization by modality and
receptive field emerged (Table 5). Thus the same response
properties appear reflected in the topography of orosensory
PBN as in NST (Halsell et al. 1993; Travers and Norgren
1995). However, it is difficult to compare the relative degree
of anatomic segregation in the two relays quantitatively.
Another important conclusion regarding PBN anatomic
organization is that the extent of orosensory responsiveness
in this nucleus is greater than usually has been realized on
the basis of neurophysiological data. In the present study,
two main groups of oral sensory neurons were indicated
within PBN and contained most of the G neurons and almost
half of the M-neurons (Table 6). The largest group was
evident caudally within the mediolateral middle of the nucleus. This is especially evident at level B in Fig. 7. The
neurons were generally within the morphologically defined
CM and VL subdivisions (Fulwiler and Saper 1984; Halsell
and Frank 1991). This corresponds to the location of the
classically described pontine taste area (Norgren and Leonard 1973) where gustatory neurons appear to be located in
most neurophysiological studies of PBN (Hill 1987; Norgren
and Pfaffmann 1975; Ogawa et al. 1987; Schwartzbaum
1983; Scott and Perrotto 1980; Travers and Smith 1984; Van
Buskirk and Smith 1981). The second group of G and M
neurons was located further rostrally and laterally within the
coextensive EM and ELi subdivisions (Fulwiler and Saper
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1984; Herbert et al. 1990). Neurophysiological studies have
not previously linked this region with gustatory responsiveness, but Yamamoto’s group recently suggested a taste
function based on c- fos immunohistochemistry (Yamamoto
et al. 1994). This region also has been suggested to be
part of a visceral and somatosensory-pain ‘‘relay’’ to dorsal
thalamus based on anatomic and physiological studies (Bernard and Besson 1988, 1990; Bernard et al. 1989; Feil and
Herbert 1995; Fulwiler and Saper 1984). The results of the
present study suggest that an orosensory function be added
to the multimodal nature of EM/ELi.
ORGANIZATION BY MODALITY. The significant differences in
G and M neuron distribution observed along the rostrocaudal
(levels A and B vs. levels C and D) and mediolateral (core
vs. lateral shell) axes (Table 5) were reflected in the differential distribution of G and M neurons within CM/VL and
EM/ELi (Table 6), because these subnuclei are discrete
along the same anatomic axes. Histological reconstructions
from a previous study by Ogawa’s group were also suggestive of some differential distribution of G and M neurons,
but the separation was less striking and not noted by the
authors (Ogawa et al. 1987).
In contrast to G and M neurons, the majority of our unresponsive neurons were located rostrally (Table 5). Only one
of these cells was within CM/VL and none were within
EM/ELi (Table 6). These unresponsive neurons did not
respond to oral taste, tactile, or thermal (though not systematically tested) stimuli nor were they respiratory (based on
visual inspection of a lack of rhythmic firing patterns synchronized with breathing movements). These neurons may
be responsive to other sensory modalities represented in PBN
(e.g., cardiovascular, gastrointestinal, pain) (Bernard et al.
1989; Cechetto 1987; Chamberlin and Saper 1992; Han et
al. 1991) or to input from higher brain regions (for review,
see Travers 1993).
OROTOPY. Collapsed across G and M neurons, orotopy also
occurred along the rostrocaudal and mediolateral axes (Table
5). Although CM/VL and EM/ELi were dominated by different neuronal populations (Table 6), it should be emphasized that there was not a complete segregation of neurons
according to receptive field in PBN. Indeed, although AObest G neurons dominated the CM/VL and were more numerous in this region, PO-best neurons were just as frequently encountered here as in EM/ELi, though they were
the only type of G neuron encountered in the latter area.
In addition, although the AO/PO organization established
in NST mostly appears conserved in PBN, it ought to be
noted that the configuration changes in the pons. In NST,
the AO and PO are represented rostrally and caudally, respectively. In PBN, their representation was reversed along
this axis. In addition, NST orotopy is not related to subnuclear boundaries, but in PBN, AO- and PO-dominant regions appear to have morphological correlates. AO and PO
responses have also been suggested to occupy adjacent but
separate regions within the ventral posteromedial thalamus
and insular cortex in rat, hamster, and rabbit based on electrical stimulation of the chorda tympani and glossopharyngeal
nerves combined with multiunit and surface potential mapping (Emmers et al. 1962; Yamamoto and Kawamura 1975;
Yamamoto and Kitamura 1990; Yamamoto et al. 1980). A
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medially located rostral central subnucleus compared with
the more laterally placed rostral lateral subnucleus. Thus it
would appear that a direct NST-PBN circuit may not fully
account for PBN M neurons. Indeed, although the response
properties of PBN M neurons generally resembled NST M
neurons (Travers and Norgren 1995), there were some differences in receptive field location, e.g., an increased number
of cells responsive to periodontal stimulation, implying input
from a source outside NST. One candidate for this additional
input is the spinal trigeminal nuclei, especially the paratrigeminal islands, as suggested by anterograde tract-tracing
studies (Cechetto et al. 1985; Feil and Herbert 1995). It
is also possible, of course, that divergence of M neuron
projections from NST contributes to the discrepancy between the sizeable population of PBN M neurons and the
apparently small population of mechanically sensitive NSTPBN projection neurons.
Although not systematically tested, a subset of M neurons
(n Å 17) were stimulated using a camel’s hair brush to test
their sensitivity to a lower-intensity stimulus. The majority
of responsive cells (11/14) were AO-best, and for most of
these, the most effective field was the incisal papilla and
antemolar rugae (9/11). This sensory representation in PBN
is compatible with a role for the pontine relay in controlling
oromotor behavior because gentle stroking of the anterior
palate elicits chewing or licking-like movements (van Willigen and Weijs-Boot 1984; Zeigler et al. 1985). In agreement
with this hypothesis, recent observations in our lab have
demonstrated a projection from orosensory PBN to the region of the parvocellular reticular formation implicated in
coordinating oromotor behavior (Karimnamazi et al. 1996).
OROSENSORY RESPONSES IN THE PARABRACHIAL NUCLEUS
ARRANGEMENT OF CHEMOSENSITIVITY. A previous neurophysiological study in rat suggested a chemotopic organization in PBN, such that NaCl-best cells were most frequently
located caudally and ventrally and HCl-best cells rostrally
and dorsally (Ogawa et al. 1987). The present data similarly
suggest a caudal and ventral clustering of NaCl-best cells.
The consistent finding of a caudal representation of salt responsiveness is further supported by c- fos immunohistochemistry in rat (Yamamoto et al. 1994) and by neurophysiological findings in another species, the hamster (Van Bus-
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kirk and Smith 1981). HCl-best neurons in the current investigation were most frequent caudally, in contrast to their
rostral location in the previous study (Ogawa et al. 1987).
The reason for this discrepancy is unclear.
It was intriguing that, despite the large number of Ncluster neurons recorded, only one was located in EM/ELi.
In fact, this particular neuron (cell 213, Fig, 1) was unusual
for a member of this cluster in that it responded optimally
and equally to NaCl and HCl and second-best to quinine.
Each of the other three gustatory neurons in EM/ELi responded best to aversive gustatory stimuli. Thus there were
two Q/ neurons that responded best to quinine and a H/
cluster neuron that responded optimally to HCl. Although
preliminary, our data on the chemosensitivity of G neurons
in EM/ELi are consistent with immunohistochemical data
that demonstrate a preferential expression of the Fos protein
in EM and EL after QHCl and HCl compared with NaCl or
sucrose (Yamamoto et al. 1994). Although both types of
data suggest an important role for EM/ELi in processing
aversive gustatory stimuli, our data further suggest it is unlikely that EM/ELi are unique in processing these tastants.
Yamamoto and colleagues (Yamamoto et al. 1994) make
no mention of quinine or acid-elicited Fos expression in
CM/VL but the present study clearly demonstrates that responses to these stimuli occur in the other subnuclei. Indeed,
about half of both the H cluster and Q/ occurred in CM/
VL (Table 6).
TASTE FUNCTION IN EM / ELI . The literature on the gustatory
function of PBN has been based primarily on CM/VL (Norgren 1995; Spector 1995; Travers 1993). Recently, however,
on the basis of a shift in gustatory-elicited Fos after conditioned
taste aversion or satiety, Yamamoto and colleagues (Yamamoto et al. 1994) suggested the interesting hypothesis that a
subset of neurons in EL represent the negative hedonic properties of gustatory stimuli rather than taste quality, per se. The
present data can provide no explicit support for such a suggestion, especially in light of the poor saccharin responses in our
population of cells. However, the fact that each neuron in EM/
ELi responded well to aversive taste stimuli does not conflict
with this interpretation. Data from anatomic studies provide
further support that EM/ELi may be a region distinct from
CM/VL. Although both sets of PBN subnuclei project to the
same taste-related forebrain nuclei, there are notable differences in the topography of their projections within these regions, for example, to the central nucleus of the amygdala
(Bernard et al. 1993). Further, in contrast to CM/VL, neurons
in EM/ELi do not project to medullary oromotor reflex circuits
(Karimnamazi et al. 1996). Likewise, immunohistochemical
studies suggest differences between these regions. A higher
proportion of neurons in EM/ELi are immunoreactive for calcitonin-gene–related peptide, compared with those in CM/VL
(Yasui et al. 1989; unpublished observations). Interestingly,
the regions of EM/ELi that we recorded from were positioned
adjacent and possibly within the PBN region involved in the
spinoreticular autonomic and pain arousal system (Saper
1995). It seems possible that the robust arousal elicited by
aversive taste stimuli (Grill and Norgren 1978) could use this
same circuitry.
The authors thank N. Burkhardt, T. Copelin, and L. McConnell for assistance with the animal preparation and histology and L. DiNardo, Dr. Joseph
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robust AO/PO distinction occurs in the teleost medulla and
possibly in the PBN homolog (Finger 1976; Hayama and
Caprio 1989; Kanwal and Caprio 1987; Lamb and Caprio
1992; Morita and Finger 1985), thus suggesting a phylogenetically conserved organization. Indeed, in the fish, anatomic studies suggest an arrangement of the facial and vagal
nerve representation in the pontine superior secondary gustatory nucleus (Morita and Finger 1985) that is strikingly
similar to what we have observed in the mammalian PBN.
On the other hand, the available neurophysiological data in
the fish suggest extensive intermingling and convergence of
extra- and intraoral input within this nucleus (Lamb and
Caprio 1992).
In the present study, orosensory neurons in CM/VL
mainly occupy the lateral half of these subnuclei (levels A
and B, Fig. 7). A previous neurophysiological study that
used only anterior tongue stimulation similarly noted this
lateral clustering, and based on its lack of responsiveness,
the medial half of CM/VL was hypothesized to be sensitive
to posterior oral cavity stimulation (Halsell and Frank
1991). Data from the present study provide a hint that this
is the case. Four of six G neurons in the medial shell, including the three most medially segregated neurons, were PObest (level B, s, Fig. 7). In addition, multiunit responses
to posterior oral cavity stimulation were noted routinely in
this area (unpublished observations). Consistent with these
neurophysiological observations, a previous anatomic study
from this lab demonstrated that biocytin injections into the
PO-responsive NST produced terminal labeling in CM and
VL in PBN that was focused medial to that observed after
similar injections into the AO-responsive NST (Becker
1992). Further data are clearly necessary to determine
whether the medial half of CM/VL is similar to EM/ELi
in responding preferentially to posterior oral stimulation.
Contrary to previous suggestions (Norgren and Pfaffmann
1975; Ogawa et al. 1987), the locations of single-unit recording sites in the present study did not suggest strong
orotopy along the dorsoventral axis, either with respect to
the representation of AO and PO or tongue and palate. On the
other hand, multiunit responses obtained while attempting to
isolate single units suggested that optimal AT responses were
located ventral to optimal PO lingual and palatal responses
(unpublished observations). Because the taste-responsive
PBN is relatively small dorsoventrally, our technique of
marking recording sites with lesions (sometimes made below
the recording site) may not have been sensitive enough to
reveal this organization. A similar discrepancy between single- and multiunit results was evident in Norgren and Pfaffmann (1975). Further work is required to clarify the nature
of orotopic organization along the dorsoventral axis.
935
936
C. B. HALSELL AND S. P. TRAVERS
Travers, and Dr. Hamid Karimnamazi for valuable comments on an earlier
version of this manuscript.
This work was supported by the National Institute of Deafness and Other
Communication Disorders Grant DC-00416 to S. P. Travers.
Address for reprint requests: C. Halsell, Section of Oral Biology, College
of Dentistry, The Ohio State University, 305 West 12th Ave., Columbus,
OH 43210.
E-mail: [email protected]
Received 30 September 1996; accepted in final form 6 May 1997.
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