Section of Oral Biology, College of Dentistry, The Ohio State University, Columbus, Ohio 43210
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ABSTRACT |
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Dinkins, Mark E. and Susan P. Travers. Altered Taste Responses in Adult NST After Neonatal Chorda Tympani Denervation. J. Neurophysiol. 82: 2565-2578, 1999. Anatomic and behavioral changes have been observed in the taste system after peripheral deafferentation, but their physiological consequences remain unknown. Interestingly, a recent behavioral study suggested that peripheral denervation could induce central plasticity. After neonatal chorda tympani (CT) transection, adult rats demonstrated a marked preference for a normally avoided salt, NH4Cl. In the present study, taste responses were recorded from the nucleus of the solitary tract (NST) in similarly CT-denervated rats to investigate a physiological basis for this behavioral phenomenon. We hypothesized that alterations in functional connectivity of remaining afferent nerves might underlie the behavioral change. Specifically, if NST neurons formerly activated by sodium-selective CT fibers were instead driven by more broadly tuned glossopharyngeal (GL) afferents, neural coding of salt responses would be altered. Such a change should be accompanied by a shift in orotopic representation and increased NH4Cl responses. This hypothesis was not supported. After CT denervation, orotopy was unaltered, NH4Cl responsiveness declined, and no other changes occurred that could simply explain the behavioral effects. Indeed, the most pronounced consequence of CT denervation was a 68% reduction in NaCl responses, supporting previous evidence for a critical role of this nerve in coding sodium salts. In addition, we found "reorganizational" changes similar to, albeit smaller than, those observed in other sensory systems after deafferentation. There was a trend for increased responses elicited by stimulation of receptor subpopulations innervated by the GL and greater superficial petrosal nerves. In addition, the spontaneous rate of nasoincisor duct-responsive cells increased significantly. This effect on spontaneous rate is opposite to that produced by CT anesthesia, suggesting that acute versus chronic denervation may affect central taste neurons differently. In conclusion, the taste system at the medullary level seems more resistant to large-scale plasticity than other sensory systems, but nevertheless reacts to lost afferent input. Because the most robust plastic changes have been documented at cortical levels in other sensory pathways, the substrate for the behavioral effect of neonatal CT transection may be located more centrally in the gustatory system.
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INTRODUCTION |
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Central neural reorganization after peripheral
deafferentation has been well documented in visual, somatosensory, and
auditory systems (reviewed in Buonomano and Merzenich
1998; Donoghue 1995
; Weinberger
1995
). By comparison, little is known of the central effects of
peripheral deafferentation in the gustatory system. Recent behavioral
evidence, however, suggests that neonatal gustatory denervation may
cause central reorganization. Adult rats that received chorda tympani
nerve (CT) transection at 10 days of age, but not those transected in
adulthood, demonstrated a striking behavioral preference for ammonium
chloride at normally avoided concentrations (Sollars and
Bernstein 1996
). Sollars and Bernstein proposed that this
new-found preference might be due to reorganization of remaining
afferent input in the first-order taste relay, the nucleus of the
solitary tract (NST). Indeed, reorganizational changes in other sensory
systems are very robust in younger animals (e.g., Kalaska and
Pomeranz 1979
; reviewed in Kaas et al. 1983
; O'Leary et al. 1994
; Wilson and Kitchener
1996
). For example, restricted lesions of the vibrissal pad on
the day of birth are associated with an expansion and reorientation of
afferents supplying undamaged regions of the whisker pad in the
trigeminal nucleus interpolaris (Renehan et al. 1994
).
Peripheral deafferentation has anatomic consequences in the NST of
developing and adult rodents. Anterior tongue cautery in 2-day-old rats
causes CT terminal field volume to decrease (Lasiter and Kachele
1990); adult CT transection results in transganglionic degeneration (Whitehead et al. 1995
). Thus CT
transection eliminates afferent activity and causes the loss of
synaptic sites, which may allow central reorganization, namely
increased efficacy of spared afferents (Merzenich et al.
1983a
, 1988
). Developmental factors suggest that
neonatal CT denervation could affect glossopharyngeal nerve (GL)
inputs. Chorda tympani fibers begin to terminate in NST prenatally, but
GL termination commences 9-10 days postnatally (Lasiter
1992
, 1993
), coincident with the timing of
behaviorally effective CT transections (Sollars and Bernstein
1996
). Interestingly, the CT and GL respond differently to
salts. Although both are activated by NH4Cl and
the preferred salt, NaCl, some single CT fibers respond selectively to
sodium salts (Boudreau et al. 1983
; Dahl et al.
1997
; Frank et al. 1983
; Hill et al.
1982
, 1983
), whereas GL fibers are much less
selective (Frank 1991
). Together, these considerations
suggest the hypothesis that neonatal CT transection enhances GL input
in the CT field and switches the input of some NST cells from
sodium-selective CT fibers to broadly tuned GL afferents, leading to a
change in central salt coding with behavioral consequences.
These arguments for the reorganization of GL responses, however,
certainly do not exclude the possibility of other alterations. In
particular, although little is known about its development or
single-fiber response profiles, reorganization of the greater superficial petrosal nerve, which innervates palatal taste receptors, also seems feasible, in this case on the basis of its termination pattern. In contrast with the GL, GSP terminations demonstrate a high
degree of overlap with those from the CT (Hamilton and Norgren
1984), and many individual NST neurons receive convergent input
from both the anterior tongue and palate (Travers et al. 1986
; Travers and Norgren 1991
,
1995
). Similar to the CT and GL, whole nerve recordings
from this nerve demonstrate a robust responsiveness to
NH4Cl (Nejad 1986
; Sollars
and Hill 1998
), suggesting that palatal stimulation could also
drive altered behavioral responses to this chemical.
The objective of the current study was to determine whether neonatal CT
transection leads to central reorganization in the adult NST, as
reflected in neurophysiological gustatory responses. Specifically, to
find correlates of the behavioral effects, we investigated whether
GL-mediated posterior tongue responses shifted anteriorly to NST
locations where CT-mediated anterior tongue responses are typically
found (Travers and Norgren 1995) and whether the number
or magnitude of posterior tongue or
NH4Cl-elicited responses increased. In addition,
we examined whether other forms of plasticity were evident: whether
there were increases in spontaneous rate, responsiveness to other
chemicals or taste bud subpopulations, or whether novel receptive field
organizations or chemosensitive neuron types appeared. Although not all
these possibilities would necessarily explain the behavioral changes
noted by Sollars and Bernstein (1996)
, they would be
consistent with denervation-induced changes in other sensory systems
(e.g., Gilbert and Wiesel 1992
; Merzenich et al.
1983a
; Pons et al. 1991
; Schwaber et al.
1993
). To assess whether an orotopic shift had occurred,
results of multi- and single-unit recordings were combined to
systematically map a large area of the NST. Changes in neural
responsiveness were determined by recording from individual neurons.
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METHODS |
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Subjects and anesthesia
Twenty-two male and eight female Long-Evans rats were used, 5 for multiunit mapping and the remaining 25 for single cell recording (232-498 g; males, mean = 406 g and females, mean = 262 g). Procedures for multi- and single-unit recording were similar unless noted otherwise. Rats underwent two surgical procedures. For CT transection at 10 days of age, they were anesthetized with a mixture of ketamine and xylazine (3.7 and 0.74 mg/kg ip, respectively). For neurophysiological tests at adult age (82 ± 2.8; range, 57-115 days), rats were anesthetized with pentobarbital sodium alone (Nembutal, 50 mg/kg ip) or in combination with ethyl carbamate (urethan, 1 gm/kg ip; Nembutal, 25 mg/kg ip). Supplemental doses of Nembutal were given as needed. Animal procedures were approved by the Ohio State University's Institutional Laboratory Animal Care and Use Committee.
Chorda tympani transection
At 10 days of age, rats underwent CT transection similar to that
of Sollars and Bernstein (1996), except that it was
unilateral. Unilateral cuts were made to allow recording from
comparable sites in rostral NST (rNST) in both the transected and
intact state. It was particularly critical to compare responses in the
rostral pole of the NST, i.e., the region that receives CT input. Our strategy of recording from the innervated side of a particular rat and
switching to symmetric locations on the cut side controlled for the
possibility that the denervated area of the rNST could be silent.
Moreover, because primary afferent gustatory input to rNST is almost
entirely ipsilateral (Hamilton and Norgren 1984
), it
seemed likely that transection-induced plasticity would be apparent in
unilaterally transected animals and the contralateral side should serve
as a reasonable control. Although contralateral changes have been noted
in other sensory systems following ipsilateral perturbations,
ipsilateral changes are far more pronounced (e.g., Takemura et
al. 1998
). Importantly, in the present study, the topographic
organization, as well as the mean spontaneous rate on the contralateral
side were not different from those observed in another recent study in
our lab that used a similar design (t = 0.24, df = 56.6, P = 0.81) (Dinkins and Travers
1998
).
For CT transection, a midline ventral neck incision was made. Blunt
dissection was performed to trace the lingual nerve to its anastomoses
with the CT (see Richter 1956, for illustration). Once
the CT was visualized, its distal end was teased from the lingual
nerve, and the remaining proximal portion was removed. Typically, a 5- to 7-mm piece of CT was removed, ensuring that regeneration would be
very unlikely. The wound was closed and sutured. Pups were returned to
the dam after ~2 h and monitored daily for a 1- to 2-wk period. There
were no instances of maternal rejection, and it was common to observe
the pups suckling from the dam immediately after their return. One rat
pup, which did not gain weight during the first 3 days postop, was
removed from the study.
Neurophysiological surgical preparation
Surgical preparatory procedures for acute
neurophysiological recording were similar to those previously described
(Travers et al. 1986; Travers and Norgren
1995
). Briefly, adult transected rats were stabilized on a
stereotaxic apparatus using a mouthpiece and atraumatic earbars (Kopf
Instruments, Tujunga, CA). The rat's head was leveled with respect to
lambda and bregma landmarks on the skull in the horizontal plane. A
headholder device was fastened to one earbar and secured to the skull
via small bone fixation screws surrounded by methyl methacrylate. This
head holder stabilized the rat's head while eliminating the need for a
mouthpiece so that one can stimulate discrete taste bud subpopulations
in the oral cavity (described in Travers et al. 1986
). A
tracheal cannula was inserted to allow unimpeded respiration during
fluid delivery and an oral drain tube, used to evacuate excess fluid,
was placed exiting the same ventral incision (modified from
Halpern and Nelson 1965
). The superior laryngeal nerves
were transected bilaterally. Retraction sutures were placed at four
sites around the oral cavity and through the tongue to allow adequate
stimulation of different taste bud subpopulations (Halsell et
al. 1993
; Travers et al. 1986
). A craniotomy was
then performed posterior to lambda to access the brain for
microelectrode penetration. Physiological saline was applied to the
exposed area of the cerebellum.
Neurophysiological recording session
Neural responses were recorded with glass-coated tungsten
microelectrodes (150-700 k for multiunit mapping and 1.0-1.5 M
for single-cell isolation) on the CT-intact and cut sides. Neural activity was amplified and observed on an oscilloscope and audio monitor. Anterior-posterior (AP) and mediolateral (ML) coordinates relative to lambda were noted for each track. Recording sites (multi-
and single-unit) were marked with electrolytic lesions made with anodal
current (3 µA, 3 s, Grass stimulator) at the recording site or
at a site 200-300 µm ventral to it.
MULTIUNIT MAPPING.
Many tracks (10-18 per side, mean = 13.4 intact and mean = 14.6 cut side) were made to construct a detailed map of multiunit taste
and tactile responsiveness in each rat. Electrode tracks were made in a
systematic manner usually 200 µm apart. Typically, 2-3 tracks at
different ML locations were made per AP level. Responses were
determined at 50-µm intervals dorsoventrally for each track starting
ventral to spontaneous activity characteristic of vestibular nuclei and
ending in strong jaw stretch activity characteristic of reticular
formation. The receptive field(s) for oral taste and tactile responses
were classified qualitatively on the basis of a clear increase in
activity using a storage oscilloscope and audio monitor. This
qualitative procedure was considered sufficient, based on agreement
between similar qualitative and quantitative categorizations from a
previous study (Dinkins and Travers 1998).
SINGLE-CELL ISOLATION. The CT-intact side was sampled first because it was more efficient to locate taste-responsive neurons on this side and then to use similar coordinates to locate taste-responsive neurons on the CT-cut side. Also, by using similar coordinates, similar areas of the NST were sampled on either side. Responses from single cells were recorded on VHS tapes for off-line quantitative analysis.
Taste and tactile stimulation
Neural responses to taste stimulation of the whole mouth,
anterior tongue, nasoincisor ducts, foliate papillae, and soft palate were assessed. On occasion, the circumvallate papilla was also stimulated. Taste buds on the anterior tongue are innervated by the CT,
and those within the nasoincisor ducts are innervated by the greater
superficial petrosal nerve, both are branches of the facial nerve.
Taste buds associated with the foliate and circumvallate papillae are
innervated by the lingual-tonsillar branch of the GL, and those on the
soft palate are innervated by the greater superficial petrosal nerve.
The testing session started by stimulating the whole mouth with a
mixture of tastants (0.3 M sucrose, 0.3 M NaCl, 0.01 M HCl, and 0.003 M
quinine hydrochloride), and then ipsilateral individual receptor
subpopulations were tested. For each stimulus trial, spontaneous
activity was recorded for 10 s preceding stimulation, and the
water, tastant, and rinse applications were of an equal duration. Whole
mouth stimulation consisted of sequentially flowing 2 ml of water, 2 ml
of taste mixture, and then 4 ml of water rinse over the lingual,
palatal, and buccal mucosa using a syringe. Individual receptor
subpopulations were stimulated with sable hair brushes in a similar
water-stimulus-rinse sequence. After taste stimulation the whole mouth
was rinsed with water from a syringe (Travers et al.
1986; Travers and Norgren 1995
). Fluid delivery
was observed through an operating microscope to ensure accurate
stimulus application. Single cells were also tested using the same
protocol for stimulating the whole mouth and individual receptor
subpopulations, with individual tastants; 0.3 M sucrose, 0.3 M NaCl,
0.3 M NH4Cl, 0.01 M HCl, and 0.003 M quinine
hydrochloride. Both multi- and single-unit sites were tested for
tactile responsivity using a blunt glass probe applied to the
ipsilateral buccal mucosa, anterior tongue, foliate papillae, circumvallate papilla, and soft and hard palate. Stimulus onset was
marked with verbal comments.
Histological reconstruction of recording sites
For multiunit mapping, approximately half of the tracks were marked with a lesion so that reconstruction would be as accurate as possible without confusing adjacent lesions. The other half were interpolated from the closest lesion, typically 200 µm away, at the same AP level. Almost every single unit (90/94) was marked with a lesion.
After the recording session, rats received a lethal dose of
pentobarbital sodium (150 mg/kg). They were perfused intracardially with physiological saline (300-400 ml) and fixed with 10% buffered Formalin (200-300 ml). The brain was removed and stored in 10% Formalin. Several days before cutting, the brain was transferred to a
20% sucrose/10% buffered Formalin solution for cryoprotection. Brains
were cut at 52 µm and sections mounted on chrome-alum-coated slides,
with alternate sections stained for Nissl substance (cresylecht violet)
or myelin (Weil). Taste-responsive multi- and single-unit sites were
reconstructed with a light microscope interfaced to a computer using
commercially available hardware and software (Vidlucida,
Microbrightfield, Colchester, VT). Electrolytic lesions (~100-150
µm diam) were identified and traced relative to the borders of the
rostral NST and solitary tract. The ML locations of multi- and
single-unit sites were expressed as a proportion of the distance from
the medial border compared with the ML width of the NST. The AP
locations of sites were expressed as a proportion of the rostral NST,
that is, the distance from the rostral pole of the NST to where the
nucleus is adjacent to the IV ventricle. Proportions of ML and AP
locations were used to plot recording sites on a horizontal schematic
of the NST (modified from Travers and Norgren 1995). The
distances of the lesions from the dorsal border of the NST were also
determined to confirm that multi- and single-unit sites were within the NST.
Analysis of orotopic representation
A specific question was whether GL-mediated (posterior tongue) responses on the cut side were more rostral than on the intact side. To assess gustatory orotopic organization, multiunit responses were used to supplement the single-unit recordings because multiunit recordings accomplished a more extensive, systematic map. Although our hypothesis specifically predicted a shift of posterior tongue responses, to simplify the analysis, multi- and single-unit sites were classified using a binary scheme; i.e., as anterior and/or posterior oral cavity taste responsive. The anterior tongue and nasoincisor duct are located within the anterior oral cavity (AOC), and the foliate, circumvallate, and soft palate are located within the posterior oral cavity (POC). The rostral NST was divided into 10 equal AP divisions, with the caudal 5 segments collapsed into one because this area was infrequently sampled. The number of sites (multi- and single-unit sites combined) that responded to AOC and/or POC taste stimulation was compared for each division. The rostral extent of GL-mediated taste responses was compared for each side. Independent t-tests were used to determine differences in mean AP and ML locations of AOC or POC taste-responsive sites within and between sides.
Quantification of single-unit activity
Single cells were differentiated off-line with a window
discriminator using consistency of amplitude and waveform as criteria. Activity was quantified by converting action potentials to digital pulses and accumulating these in 500-ms bins in peristimulus time histograms using MII hardware and software (Modular Instruments, Southeastern, PA). Net-evoked activity was quantified with a standard response measure, defined as the number of spikes over a 10-s period
during taste stimulation minus the number of spikes that occurred
during the preceding water stimulation. The criteria for a
suprathreshold taste response were defined as a minimum 1 spike/s
increase in activity, which also had to be >2.5 times the standard
deviation of the spontaneous rate (Dinkins and Travers 1998; Travers et al. 1986
; Travers and
Norgren 1991
, 1995
; Travers and Smith
1984
).
Statistical analyses of neural responses
To determine an effect of CT transection on cell responses, comparisons between sides were made using several analyses. Initial comparisons were made between all cells recorded on the CT intact versus the cut sides. These determined whether the sides were different but did not provide much insight regarding whether differences were due to central reorganization, because certain changes would be expected based solely on removing CT input. To make more direct comparisons of responses from peripheral sources other than the CT, we compared whole mouth responses after removing cells responsive to anterior tongue stimulation on the intact side. This included removing cells specifically responsive to anterior tongue stimulation as well as anterior tongue neurons with additional convergent inputs. We also compared responses to specific stimulation of nonanterior tongue receptor subpopulations, that is, the nasoincisor duct, foliate, or soft palate.
2 was used to determine the difference in
number of AOC multi- and single-unit responses between sides and to
determine differences in the proportions of neurons with various
receptive fields. Mean spontaneous rates and responses to the taste mix
and individual tastants were compared between sides using two-way
ANOVAs followed by independent t-tests. Because differences
were predicted between sides, a priori, t-tests were not
Bonferroni adjusted. Additionally, Pearson correlation coefficients
were calculated to determine similarities between responses evoked by
pairs of different tastants. It was of special interest to determine
whether the similarity between NaCl and NH4Cl
increased between sides, because this would be consistent with
behavioral differences (Sollars and Bernstein 1996
).
Finally, hierarchical cluster analysis (Pearson correlation coefficients and average-linkage method, Systat) was performed to
determine whether there was any evidence for altered neuron types
between CT-intact and cut sides.
Taste pores and fungiform papillae
The number of taste pores and fungiform papillae on the anterior
tongue was determined for CT-intact and cut sides using a procedure
similar to that described by Spector and Grill (1992). The anterior 5 mm of each tongue was stained with 0.5% methylene blue
and observed under light microscopy. An observer blinded to the
denervated side counted taste pores and fungiform papillae for each
side. Pores and papillae counts were averaged per side and compared by
paired t-tests. For all analyses in this study, error terms
are presented as SEs and significance levels set at P < 0.05.
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RESULTS |
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Taste pores and fungiform papillae
There were fewer taste pores and fungiform papillae on the CT-cut side of the tongue (t = 26.29, df = 28, P < 0.001; t = 8.39, df = 28, P < 0.001, respectively; Fig. 1). These results confirm the efficacy of the CT transection and provide evidence that this procedure results in long-term denervation of the tongue.
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Orotopic representation of multi- and single-unit taste responses
Based on multi- and single-unit activity in 30 rats, the orotopic representation of taste responses did not change after long-term CT transection. Figure 2 depicts taste responses from both the multiunit (squares) and single-unit (circles) recording experiments, classified by their responsiveness to AOC and/or POC stimulation. In the five multiunit mapping procedures, 139 tracks were made in the vicinity of the rNST, and 109 tracks passed through the nucleus. Of these, 33 taste-responsive tracks were identified on the CT-intact side and 19 on the cut side (Fig. 2). The remaining tracks were unresponsive or responsive to other types of orosensory stimulation (see next paragraph). During 25 single-unit recording preparations, responses were obtained from 94 taste-responsive cells; 51 on the CT-intact and 43 on the cut side. The locations of 78 single neurons that were histologically reconstructed and could be classified as AOC- and/or POC-responsive are also shown in Fig. 2.
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Combining multi- and single-unit data, AOC taste-responsive sites were found rostral and lateral to POC taste-responsive sites on both sides (intact side, AP, t = 6.27, df = 65, P < 0.001, ML, t = 5.68, df = 64, P < 0.001; cut side, AP, t = 3.76, df = 41, P = 0.001, ML, t = 3.10, df = 41, P < 0.005). In contrast, mean AP and ML locations for AOC taste-responsive sites were not significantly different between sides (AP, t = 1.08, df = 75, P = 0.29; ML, t = 1.31, df = 74, P = 0.19), nor were mean locations of POC taste-responsive sites (AP, t = 1.76, df = 31, P = 0.09; ML, t = 0.65, df = 31, P = 0.52). Thus contrary to our hypothesis, POC taste responses were not represented further rostrally in the NST following neonatal transection. Furthermore, in the multiunit recording experiments, we found that the orotopic representation of mechanical responses was also unaltered by neonatal transection (not depicted).
Instead of a rostral migration of POC taste responses, the rostral pole
of the NST (rostral 40%) on the cut side was less responsive to taste
stimulation. There were fewer sites in the rostral pole of the NST
responsive to AOC stimulation on the cut side (23 vs. 46). At locations
homologous to those yielding robust anterior tongue taste responses on
the intact side, responses to depressing the mandible ("jaw
stretch") were typically found. In fact, a higher proportion of
tracks on the cut side were characterized only by responses to jaw
stretch (2 = 9.50, P < 0.005;
see large and small asterisks, Fig. 2). Five of these tracks on the cut
side passed through a clear unresponsive region, 50-100 µm in depth,
that was just ventral to the high-amplitude activity characteristic of
the vestibular nucleus, but dorsal to responses to depressing the
mandible (large asterisks, Fig. 2). The greater number of "jaw
stretch only" tracks, particularly those with this dorsal,
unresponsive region, implies that neonatal CT transection renders the
rostral pole of the NST relatively unresponsive. Alternatively, because
these observations are based on multiunit activity and ventrally placed
lesions, the precise location of the jaw stretch responses is unknown,
and it is conceivable that they were recorded from cells in an unusual
location, i.e., in NST. However, in the single-unit
experiments, six jaw stretch neurons were marked with
lesions and were always found ventral to or in the ventral subdivision
of NST, on both the CT-intact and cut sides. Thus, although jaw stretch
responses were noted more frequently on the cut side, there is no
evidence that their position changed.
General description of single cells
The number of taste-responsive cells per side was similar (2.00/intact side and 1.83/cut side per rat; t = 0.31, df = 23, P = 0.76). Also, a similar number of taste-responsive cells were isolated per taste-responsive track (0.42 cells/track intact side vs. 0.37 cells/track cut side; t = 0.61, df = 21, P = 0.55). However, more tracks were made on the CT-cut side to find the same number of taste-responsive cells (mean = 7.5 tracks/rat on the intact side vs. mean = 10.5 tracks/rat on the cut side; t = 3.96, df = 23, P = 0.001). Therefore identifying the taste-responsive area of the NST was more difficult on the CT-cut side.
Receptive field organization
Although there was no evidence for orotopic reorganization,
differences in the proportions of cells responsive to particular receptor subpopulations were found. Table
1 classifies cells by receptive field,
and Fig. 3 graphically compares the
proportions of neurons activated by each receptor subpopulation for the
two sides, excluding those (few) cells that only responded to whole mouth stimulation. A high proportion of neurons on the intact side,
28/39 (~72%) responded to anterior tongue stimulation. However, on
the cut side, as expected, anterior lingual stimulation was virtually
ineffective. Only one cell whose response barely met criteria responded
to anterior tongue stimulation. Most cells on the cut side, 19/30
(~63%) responded to stimulation of the nasoincisor duct. Contrary to
our hypothesis, an increase in the incidence of GL-responsive cells was
not observed (2 = 0.21, P > 0.05). However, an increase in palatal-responsive cells was found: the
proportion of nasoincisor duct-responsive cells increased over twofold
on the cut side (
2 = 10.14, P = 0.001), and the incidence of soft-palate responsive cells increased
even more markedly. Soft palate-responsive cells comprised only ~8%
of the cells on the intact, but over 40% on the cut side
(
2 = 12.09, P = 0.001). Thus
on the denervated side, palatal but not foliate responses increased to
compensate for the missing anterior tongue responses.
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The increase in number of palatal responses is provocative, but
removing anterior tongue input dictates that other cell types increase
proportionally, even without altered input. To address this possibility
more directly, we reanalyzed the data without including anterior tongue
responses. Interestingly, there was still a higher
proportion of soft palate-responsive cells on the cut side
(2 = 4.43, P < 0.05). On the
other hand, the proportion of foliate-responsive cells decreased
significantly (
2 = 5.22, P < 0.05) and the proportion of nasoincisor duct-responsive cells was the
same (
2 = 0.69, P > 0.05).
The selective increase in soft palate-responsive neurons suggests that
afferent input from this receptor subpopulation may become more
efficacious after denervation.
Although the proportions of cells responding to particular receptor
subpopulations differed between sides, the proportion that received
convergent input arising from separate receptor subpopulations did not
(2 = 0.361, P > 0.05). Twelve
of 42 (29%) cells on the intact side and 11 of 35 (31%) on the cut
side responded to more than one receptor subpopulation (e.g., both the
nasoincisor duct and soft palate). The remaining neurons received input
from a single receptor subpopulation. Even when cells responsive to
anterior tongue stimulation were removed from the analysis, the
incidence of convergence still did not vary; convergent neurons
comprised 21% of cells on the intact and 29% on the cut side
(
2 = 0.32, P > 0.05). These
results suggest that patterns of afferent input to single cells were
unaltered by neonatal CT denervation.
Altered neural responses in the NST
The preceding analyses investigated the possibility of central reorganization by categorizing neurons according to suprathreshold responses, without regard to response magnitude. The following analyses explore the possibility of more graded changes with respect to spontaneous or evoked activity by analyzing changes in firing rates.
SPONTANEOUS ACTIVITY.
Because previous work has shown that the spontaneous rate of NST cells
that receive CT input is greater in magnitude than cells that do not
(Dinkins and Travers 1998; Travers et al.
1986
), a change in the characteristic spontaneous activity
could suggest denervation-induced plasticity. The overall mean
spontaneous rate on the CT-intact versus the cut side was lower but not
statistically significant [2.08 ± 0.39 (SE) spikes/s intact vs.
2.95 ± 0.67 spikes/s cut side; t = 1.13, df = 68.7, P = 0.26]. However, when anterior
tongue-responsive cells were removed to directly compare cells without
CT input, the mean spontaneous rate was significantly higher for cells
on the CT-cut side (2.97 ± 0.69 spikes/s cut side vs. 0.70 ± 0.26 spikes/s intact side; t = 3.09, df = 50.7, P < 0.005). This effect was explored further and found
to be restricted to cells that responded best to nasoincisor duct
stimulation. Cells that responded best to nasoincisor duct stimulation
on the CT-intact side exhibited a much lower mean spontaneous rate than on the CT-cut side (Fig. 4; 1.68 ± 0.61 spikes/s vs. 4.75 ± 1.06 spikes/s, respectively; t
= 2.51, df = 31, P < 0.05).
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TASTE RESPONSES TO MIXTURE STIMULATION. Response magnitudes evoked by stimulating each receptor subpopulation with taste mixture for each cell on the CT-intact and cut sides are depicted in Fig. 5; mean responses appear in the insets for each panel. Across all cells, an ANOVA of the mean responses (top line in insets) revealed a significant interaction between receptor subpopulation and side (ANOVA, F = 9.68, df = 4, P < 0.001). Specifically, responses to anterior tongue stimulation were robust on the intact side but virtually obliterated on the cut side (t = 5.15, df = 47.2, P < 0.001). In contrast, foliate responses were not different between sides (t = 1.23, df = 47.7, P = 0.23), whereas nasoincisor duct and soft palate responses were greater on the cut side (t = 2.73, df = 58.5, P < 0.01; t = 2.40, df = 41.2, P < 0.05, respectively).
|
TASTE RESPONSES EVOKED BY INDIVIDUAL TASTANTS.
The mixture analysis suggested denervation-induced changes in taste
responsiveness, but because effects could vary according to quality,
responses to individual tastants were also analyzed. We were
particularly interested to determine whether
NH4Cl responses increased in magnitude following
denervation. Instead of increasing, however, both
NH4Cl and NaCl responses decreased on the cut
side, and only sucrose responses tended to increase (Fig.
6; ANOVA, F = 7.60, df = 4, P < 0.001 for interaction between
tastants and side; t = 3.08, df = 64.1, P < 0.005; t = 3.18, df = 54.7, P < 0.005; t = 1.79, df = 42.6, P = 0.08, respectively, for
NH4Cl, NaCl and sucrose). Further, it seems
likely that these differential effects simply reflect the greater
sensitivity of the CT to salts, and the greater superficial nerve to
sucrose (Nejad 1986; Sollars and Hill
1998
; Travers et al. 1986
), along with the
increased proportion of palatal neurons on the cut side. Because few
individual receptor subpopulations were tested with single tastants,
however, restricted analyses like those performed for the mixture were not possible. Another approach to directly compare nonanterior tongue
responses was to remove all anterior tongue-responsive neurons from the
data set and analyze whole mouth responses. This approach was less
comprehensive because many neurons with convergence from the anterior
tongue and other receptor subpopulations could not be used, but still
resulted in a reasonable sample size. Using this strategy, there was no
significant interaction between tastants and side, suggesting that the
relative chemical responsiveness of residual taste responses was
unaltered by denervation (ANOVA, F = 0.76, df = 4, P = 0.56).
|
Neuron types
Finally, we examined chemosensitive response profiles using
hierarchical cluster analysis (Fig. 7). A
difference in chemosensitive groups could imply that afferent inputs
were resorted after denervation. A scree analysis of the cluster tree
suggested four groups of cells on the CT-intact side (Fig. 7, top
panel), although two groups included most (36/41) neurons. Mean
profiles are depicted in the left panel of Fig.
8. The largest group (n = 28) was the "NH" cluster. These cells nominally responded best to
NH4Cl, but their mean response to NaCl was almost
as great. These cells were heterogeneous, encompassing those that
responded better to NaCl, better to NH4Cl, or
similarly to both. The next-largest cluster (n = 8)
included neurons that responded best to sucrose ("S" cluster), but
this group also exhibited notable sideband responsiveness to both
salts. The remaining neurons responded optimally to HCl or quinine, and
these few "H" and "Q" cluster neurons had low response rates.
The chemosensitive groups tended to have unique receptive fields,
consistent with peripheral nerve sensitivities (Frank
1991; Nejad 1986
; Sollars and Hill
1998
; Travers et al. 1986
). Most (79%) NH
neurons responded to the anterior tongue, and these receptors usually
comprised the optimal receptive field. S cluster neurons also received
anterior tongue input, but less frequently (50%), and except for one S
neuron, the foliate papillae or palate was the optimal receptive field.
Only one H or Q cluster neuron had any input from the anterior tongue;
instead their receptive fields included the foliate papillae or palate.
|
|
A cluster analysis suggested five instead of four chemosensitive types following CT transection (Fig. 7, bottom panel). However, except for the extra group, relative response profiles strongly resembled those on the intact side (Fig. 8). For each group the order of effectiveness of the five stimuli was virtually identical. Further, most cut-side cells (24/31) were also NH or S neurons. Despite these broad similarities, NH and S cluster neurons did appear more narrowly tuned on the cut side. For NH neurons, there was a 77% reduction in the sodium, but only a 35% decrement in the ammonium response and consequently, on average, these cells responded more specifically to NH4Cl. Indeed, in contrast to the intact side, each NH cell on the cut side responded best to NH4Cl. In addition, proportions of S versus NH cells varied between the two sides. There were equal numbers on the cut side but NH cells outnumbered S cells by a 3:1 ratio on the intact side.
Although the proportions and responsiveness of S and NH neurons exhibited differences, it seems doubtful that they indicate active plastic changes. Rather, the profiles on the cut side appear to simply represent the chemosensitivity that remains after removing anterior tongue input. The middle panel of Fig. 8 depicts response profiles for cells on the intact side that did not receive anterior tongue input. Their numbers are too few for statistical analysis, but it is worth noting that they resembled corresponding groups on the cut side. There were equal numbers of nonanterior tongue S and NH neurons, and they tended to be more narrowly responsive. Finally, although infrequent, it was interesting that a novel cell type was delineated on the cut side. Four cells responded very specifically, albeit weakly, to NaCl. Another distinguishing feature of these cells was that three of four responded best to soft palate stimulation. Somewhat surprisingly, cells with a similar specificity for NaCl did not occur on the intact side. Although a subcluster from the NH group (n = 9) responded better to NaCl, except in one case, both salts evoked suprathreshold responses.
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DISCUSSION |
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Orotopic representation and receptive field organization
This study was designed to determine whether neonatal CT nerve
transection leads to changes in the orotopic representation or other
changes in single-unit gustatory responses in NST. However, the orderly
organization of AOC and POC taste responses was unaltered following
unilateral CT nerve transection in young rats. We tested the hypothesis
that POC taste-responsive neurons would shift rostrally on the CT-cut
side. Instead, POC responses were found in symmetrical locations,
caudal and medial to AOC responses. Importantly, the orotopic
organization on both sides was virtually identical to that reported in
our previous studies (Dinkins and Travers 1998; Travers et al. 1986
; Travers and Norgren
1995
), making it unlikely that changes occurred but were masked
because they occurred bilaterally. The lack of an orotopic
reorganization suggests that large-scale functional changes that would
be expected if anatomic changes (e.g., axonal sprouting or increased
dendritic arborization) took place, do not appear to occur in the NST
following CT transection in 10-day-old rat pups. Instead of receiving
novel afferent inputs from other receptor subpopulations, the rostral
pole of the NST (rostral 20%) was less responsive to taste stimulation
on the CT-cut side. In the multiunit experiments 2 of 16 tracks on the CT-cut side were taste-responsive, compared with 12 of 17 on the intact
side. Likewise, only 5 taste-responsive single units were isolated on
the cut side versus 10 on the intact side.
Contrary to the present results, changes in topographic representation
after peripheral denervation are common in other sensory systems.
Median nerve transection results in altered responses in the primary
somatosensory cortex in monkeys (Merzenich et al. 1983a;
reviewed in Buonomano and Merzenich 1998
;
Merzenich et al. 1988
). After denervation, neurons that
previously responded to the denervated receptive field respond to an
adjacent receptive field innervated by an intact nerve (e.g., the ulnar
nerve). Studies over the last decade have shown that somatotopic
reorganization in the somatosensory cortex of monkeys after peripheral
deafferentation are reflected in similar changes at lower levels of the
neuraxis, including the spinal cord and medulla (Florence and
Kaas 1995
; Garraghty and Kaas 1991a
). These
denervation-induced shifts in topographic organization are thought to
reflect a functionally adaptive capacity for activity-induced
plasticity (Jenkins et al. 1990
). Changes result not
only from reduced afferent drive, as occurs after denervation, but also
from increases in sensory activity. A striking instance occurs in the
somatosensory system of people who play string instruments; they
exhibit larger areas of cortex dedicated to fingering digits than
nonfingering digits (Elbert et al. 1995
).
The lack of an orotopic reorganization in the present study could be
taken to suggest that topography is less plastic in the gustatory
system. Indeed, coding the location of a sapid stimulus is probably not
a very important function of the taste system, and activity-dependent
plasticity for taste bud subpopulations would be of limited use given
that all are simultaneously stimulated during normal function. On the
other hand, orotopic organization in the mammalian taste system is
coarse, and we studied it at a relatively crude level, limiting the
sensitivity of our assay to major shifts. In addition, we studied only
a single time point after denervation. Although plasticity can occur
just after denervation (Merzenich et al. 1983b;
Xu and Wall 1997
), denervation can also temporarily
render the central representation silent (Merzenich et al.
1983b
, 1984
), and the most dramatic topographic
shifts have been reported after lengthy periods (years) of denervation (e.g., Pons et al. 1991
). In addition, central
reorganization is often confined to a critical period (Wiesel
and Hubel 1963
). With regard to the current findings, it is
relevant that decreases in CT terminal field volume after neonatal
anterior tongue cautery occurred when this manipulation was performed
at 2, but not 10 days of age (Lasiter and Kachele 1990
).
We chose the timing of denervation and testing in the present study to
match conditions under which behavioral changes in salt responsiveness
are apparent (Sollars and Bernstein 1996
). Although we
can rule out topographic shifts in the first-order relay as an
explanation for this instance of behavioral plasticity, such changes
could certainly occur with earlier or longer periods of denervation.
Increased convergence from multiple receptive fields would also
indicate functional changes in NST. However, the degree of convergent
input from intact nerves in the NST did not change after CT
transection. A considerable amount of convergence normally occurs in
NST between individual receptor subpopulations, especially between the
anterior tongue and nasoincisor ducts (Dinkins and Travers
1998; Travers et al. 1986
; Travers and
Norgren 1991
, 1995
). Because convergence between
the anterior tongue and other receptor subpopulations could not occur
on the cut side, it is somewhat surprising that the degree of
convergence remained the same. This is probably due to the greater
number of palatal-responsive cells on the cut side, because these cells
displayed frequent convergence between nasoincisor duct and soft palate
receptor subpopulations. Therefore cells that responded to anterior
tongue and other receptor subpopulations on the intact side were
replaced with cells that responded to both palatal receptor subpopulations.
Spontaneous firing rates
Although neither changes in orotopy nor the organization of
receptive fields were observed, spontaneous rates of NST cells were
different between sides. Interestingly, we found an increase in mean
spontaneous rate of nasoincisor duct-responsive cells after CT
transection. However, in a previous study of the effects of CT
anesthesia, we found the opposite effect for the same cell type; a
trend toward a decrease in spontaneous rate (2.99 ± 1.18 spikes/s
before anesthesia vs. 0.56 ± 0.20 spikes/s during anesthesia; t = 2.025, df = 9.5, P = 0.072, see Fig. 9) (Dinkins and Travers 1998). Because there was no significant difference in the
spontaneous rate of nasoincisor duct-responsive cells on the intact
side of this study and those from the anesthesia study
(before CT anesthesia), we can rule out potential variables
between studies (1.58 ± 0.48 spikes/s intact side vs. 2.99 ± 1.18 spikes/s CT anesthesia study; t = 1.11, df = 12, P = 0.29). Although it is tempting to speculate that chronic denervation led to reactive changes in the CNS to account
for the difference in the direction of spontaneous rate changes of
CT-denervated animals, this could also be due to different peripheral
reactions to the denervation methods used; i.e., anesthesia versus
transection. Chorda tympani anesthesia may result in decreased spontaneous rate by decreasing peripheral input, but CT transection may
trigger neuroma formation in the proximal nerve. In the somatosensory system, damaged peripheral nerves can form spontaneously active neuromas (Wall and Gutnick 1974
). If this also occurred
after CT transection, it would be expected to result in increased
spontaneous activity in NST cells with CT input. Under denervated
conditions, nasoincisor-duct responsive cells should be affected
because anterior tongue and nasoincisor duct responses often converge.
Unfortunately, the possibility of neuroma formation was not considered
at the time of the experiment and hence cannot be ruled out. Similar to
the somatosensory system, where spontaneous activity from neuromas has
been implicated as a cause of phantom limb pain (Nystrom and Hagbarth 1981
), if such neuromas do form after CT transection, they may be a cause for "dysgeusias," i.e., unpleasant tastes of
unknown origin (Bull 1965
; Miller and Bartoshuk
1991
), or "burning mouth syndrome" (Bartoshuk et al.
1996
).
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Evoked firing rates
Also contrary to our CT anesthesia study (Dinkins and
Travers 1998), which provided no evidence that anesthesia
caused mean taste responses to increase, the present results are
suggestive that denervation resulted in increased responses arising
from receptor subpopulations innervated by nerves other than the CT. Across all cells, taste mixture responses to nasoincisor duct and soft
palate stimulation were greater on the cut side. Even when restricted
to cells responsive to a particular receptive field, a trend for
increased palatal and foliate responses persisted. In addition, the
proportion of cells that responded to the soft palate was greater.
Taken together, these results provide some evidence that GL- and
greater superficial petrosal-mediated responses become more efficacious
after CT denervation. This type of neural compensation could explain
why human patients do not report deficits in taste after CT damage; a
phenomenon termed "whole mouth taste constancy" (Lehman et
al. 1995
). That is, remaining input to the CNS may be
strengthened and compensate for lost CT input. However, caution is
warranted in drawing firm conclusions. Although a sizeable sample of
nasoincisor duct responses was recorded (n = 37),
smaller samples (<20) of foliate and soft palate responses were
obtained. Thus larger numbers of POC responses are necessary to confirm the increases. An additional caveat is required when response rates are
compared with the previous CT anesthesia study from our lab
(Dinkins and Travers 1998
). The CT-cut side foliate
responses in the current study resembled those in the previous study
(before CT anesthesia) but intact-side responses were
actually lower. Thus we cannot argue that the elevated foliate response
rates on the cut side are outside the "normal" range. In fact,
although it seems unlikely based on the purely ipsilateral projections of the CT to NST (Hamilton and Norgren 1984
), we cannot
rule out the possibility that differences between sides are due to
contralateral decreases rather than ipsilateral increases. In addition
to lower response rates evoked by foliate stimulation, anterior tongue responses in the current investigation were also somewhat reduced compared with our earlier investigation, although nasoincisor-evoked responses were comparable. Finally, it is interesting that, despite their increased magnitude, the proportion of foliate responses actually
declined on the cut side. This may have occurred because the foliate
papillae receive a dual innervation from the GL and CT nerves
(Miller et al. 1978
; Whiteside 1927
).
Their decreased number may represent elimination of CT-driven foliate responses.
Taste bud subpopulations and chemosensitivity
Although they most likely reflect loss of CT input rather than
plastic changes, there were dramatic differences in relative chemosensitivity between the CT-intact and cut sides. These are relevant to the proposed functional heterogeneity between gustatory nerves (discussed in Smith and Frank 1993;
Travers et al. 1987
; Travers and Norgren
1995
). Previous behavioral (Markison et al. 1995
; Spector and Grill 1992
; St John et
al. 1997
) and neurophysiological studies (Boudreau et
al. 1983
; Frank et al. 1983
) suggest that the CT
makes a selective contribution to electrolyte, particularly sodium,
sensitivity. Our results support this contention. Cutting the CT in
neonatal rats produced a dramatic decrease in the mean response to
NaCl. The average NH4Cl response was blunted,
albeit less. These decrements did not extend to other stimuli. The
relatively poor sucrose and quinine responsiveness of the rat CT
(Frank et al. 1983
; Ogawa et al. 1968
)
corresponds with the lack of a decrement after denervation. On the
other hand, the CT responds well to HCl (Erickson et al.
1980
; Frank et al. 1983
; Ogawa et al.
1968
), and thus a decrease in acid responsiveness was also
predicted. However, despite a nonsignificant decrease on the cut side,
even on the intact side, HCl-evoked responses were surprisingly small. The minimal impact of denervation on HCl-responsiveness is most easily
explained as a floor effect, combined with the robust responsiveness of
other taste nerves to acids (Frank 1991
; Nejad
1986
). There was no obvious reason for the small HCl responses
we observed. However, the magnitude of central acid responses varies
across studies, and small acid responses are not unique to our study (e.g., Nakamura and Norgren 1993
).
The contribution of the CT to sodium responsiveness is also evident in the proportions and profiles of the chemosensitive groups on the two sides. On the intact side, where anterior tongue-best neurons dominated, NH cluster neurons comprised a majority of the cells. Some NH neurons responded best to NaCl. On the cut side, NH cluster neurons also occurred but represented a minority of the population, they were less responsive than their intact-side counterparts, and none responded best to NaCl.
Although our observations suggest that salt, especially sodium,
responsiveness is severely compromised by CT transection, it is
certainly not eliminated. The proportion and response rates of NH cells
decline, but such cells still represent a sizeable, reasonably
responsive group. In addition, although the sodium-best subcluster of
NH cells is not apparent on the cut side, an additional "sodium-specific" group emerged, although these cells were few in
number and minimally responsive. It is interesting that the residual
salt sensitivity we observed was attributable mainly to neurons with
optimal receptive fields on the palate. This sensitivity is consistent
with recent data (Sollars and Hill 1998) that show substantial sodium and ammonium responsiveness in the greater superficial petrosal nerve.
The current results also support previous neurophysiological data
(Nejad 1986; Sollars and Hill 1998
; see
also Harada and Smith 1992
), suggesting that the greater
superficial petrosal nerve is more important than the CT in conveying
information about "sweet" tastants in the rat. More neurons on the
cut side responded to palatal stimulation, and sucrose was the only
tastant that tended to elicit a larger response on that side.
Differential contributions to sucrose responsiveness were also evident
in the receptive field organization of S cluster neurons. Although a majority of intact side neurons responded best to anterior tongue stimulation, only a single S cluster neuron did. Instead, about one-half of the S neurons responded most vigorously to the palate and
one-half to the foliate papillae. On the cut side, proportions of S
cluster neurons increased in tandem with neurons that responded best to
palatal stimulation. The current observations agree with our earlier
results in NST, which found no sucrose-best neurons that only responded
to the anterior tongue, but a substantial number with convergent input
from the anterior tongue and nasoincisor duct (Travers et al.
1986
). The present results further suggest that many S cluster
neurons have receptive fields on the soft palate or foliate papillae.
Neonatal CT transection: behavioral versus NST responses
A striking increase in behavioral preference for
NH4Cl after CT transection in 10-day-old rats was
demonstrated by Sollars and Bernstein (1996), yet the
physiological changes that account for the behavior remain unknown. A
simple hypothesis was that neurons in the rostral pole of NST that
responded preferentially to stimulation of the anterior tongue with
NaCl would be replaced by cells that responded broadly to NaCl and
NH4Cl applied to the posterior tongue.
Corollaries of this hypothesis predicted increases in the magnitude or
number of posterior tongue and NH4Cl responses. This simple hypothesis is clearly untenable. As discussed above, instead of being more responsive to posterior tongue taste stimulation, the rostral pole of NST was less responsive to taste stimulation in
general. Instead of being more responsive to
NH4Cl, the mean response to whole mouth
NH4Cl stimulation was reduced. Augmented responses to foliate stimulation suggest increased synaptic efficacy of
the GL, but the proportion of neurons driven by this receptor subpopulation actually declined. Despite a thorough analysis, no other
alterations in neural response that might explain the behavior emerged.
Although we did not find a correlate of increased
NH4Cl preference, we did note a change in
NH4Cl responsiveness that should have behavioral
consequences. The Pearson correlation between NaCl and
NH4Cl decreased on the cut side. This decrease
persisted when restricting the analysis to cells without CT input,
suggesting that it may reflect plasticity rather than merely a
difference in anterior tongue versus nonanterior tongue responsive
cells. However, a relatively small number of cells without CT input
(n = 11), were available for this analysis, making this
interpretation tentative. Further, the change was opposite to that
predicted from behavioral observations. In addition to the preference
shift, rats with neonatal CT transections generalize more between NaCl and NH4Cl (Sollars and Bernstein
1996), a change that should be accompanied by an increase in
across-neuron correlations. This discrepancy between the neural and
behavioral results is difficult to explain.
The lack of plastic changes in NST responses consistent with the
behavioral changes induced by neonatal CT transections (Sollars and Bernstein 1996) implies that neural correlates of the
altered behavior reside elsewhere, or that our experiment failed to
reveal them. It should be noted that the present study did use a
different rat strain (Long-Evans) than the one (Wistar) used in the
behavioral experiment (Sollars and Bernstein 1996
), and
it is possible although it seems unlikely that this disparity would
have obscured such changes. Another difference between the behavioral
experiment (Sollars and Bernstein 1996
) and the present
investigation was that the former study used bilateral cuts but that we
sectioned the CT unilaterally and compared the two sides of the brain.
It is possible that the neural plasticity requires bilateral cuts. However, this also seems unlikely. In most models of
deafferentation-induced plasticity, unilateral transection produces
profound neural changes (e.g., Jones and Pons 1998
;
Merzenich et al. 1983a
; Pons et al. 1991
;
Wiesel and Hubel 1963
). Thus it seems more likely that
plasticity at higher levels of the gustatory neuraxis underlie the
behavioral change. This would be consistent with other sensory systems.
Although plastic changes certainly occur at subcortical levels
(Florence and Kaas 1995
; Garraghty and Kaas
1991a
), alterations are cumulative and are larger at higher
levels of the neuraxis (Florence and Kaas 1995
;
Florence et al. 1998
; Garraghty and Kaas
1991b
). The competence of brain stem circuits for making basic
gustatory discriminations (Grill and Norgren 1978
)
suggests the parabrachial nucleus as a possibility. However, the
complexity of taste preference behavior also favors several forebrain regions.
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ACKNOWLEDGMENTS |
---|
We thank Dr. Ilene Bernstein and M. Roitman for initial discussions and for demonstrating the CT transection procedure. We thank Drs. Keith Alley, J. P. Baird, Scott Herness, and Joseph Travers for helpful comments on previous versions of the manuscript. We greatly appreciate the excellent technical assistance provided by E. Hauswirth, Dr. Hecheng Hu, and K. Urbaneck.
This work was supported by National Institute of Dental Research Grant DE-00357 (Dentist-Scientist Award) to M. Dinkins and National Institute on Deafness and Other Communication Disorders Grant DC-00416 to S. Travers.
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FOOTNOTES |
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The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 18 March 1999; accepted in final form 2 July 1999.
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REFERENCES |
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