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Department of Physiology, Faculty of Medicine, Toyama Medical & Pharmaceutical University, Sugitani 2630, Toyama 930-0194 and * Basic Research Laboratory, Central Research Laboratories, Ajinomoto Co. Inc., Suzuki-cho 1–1, Kawasaki 210-8681, Japan
3To whom correspondence should be addressed.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONSUMMARYREFERENCES |
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KEY WORDS: • rats • hypothalamus • amygdala • taste • ingestive behavior
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONSUMMARYREFERENCES |
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, Travers and Norgren 1986
), it is one of
the principal neural systems influencing ingestive behavior. The
brainstem contains a basic neural system that governs ingestive
behavior; this includes brainstem taste areas such as the nucleus of
the solitary tract
(NTS)4
and the pontine parabrachial nucleus (PBN), through which the animal
can manifest different oromotor responses to the four basic tastes
(Grill and Norgren 1978a
and 1978b
). It has been
suggested that the forebrain, including the amygdala (AM) and
hypothalamus, which receives taste information from brainstem taste
areas, is a higher center modulating the activity of brainstem neural
systems via descending projections (Norgren 1995
). The
hypothalamus has been reported to be important in motivation,
regulation of feeding behavior and learning (Olds 1976
,
Rolls 1976
); the AM is important in the evaluation of
the biological significance of sensory stimuli (LeDoux 1987
, Nishijo et al. 1988a
and 1988b
). Lesions
of the AM and hypothalamus are known to alter food preferences in
monkeys and rats (Isaacson 1982
, Klüver and Bucy 1937
, Murray et al. 1996
) and to attenuate
behavioral responses to both preferred and aversive taste stimuli in
rats (Kemble and Schwartzbaum 1969
). Furthermore,
decerebration, or electrical stimulation or inactivation of the
forebrain is reported to modulate the activity of taste neurons in the
NTS and PBN (Di Lorenzo 1990
, Hayama et al. 1985
, Mark et al. 1988
, Matsuo et al. 1984
, Murzi et al. 1986
).
In this study, to investigate the nature of the information processed
in the AM and hypothalamus, we recorded neuronal activity in the AM and
hypothalamus during the discrimination of sensory stimuli associated
with various taste solutions and the ingestion of taste solutions.
Second, because stress is known to induce alterations in ingestive
behavior (e.g., hyperphagia, hypophagia) (Kondoh et al. 1996
, Martí et al. 1994
) and taste
preferences (Antelman et al. 1976
, Vaswani et al. 1983
), we also analyzed the effects of stress on hypothalamic
neuronal activity.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONSUMMARYREFERENCES |
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Male albino Wistar rats (n = 12), weighing 280–350
g, were used. Under pentobarbital anesthesia (40 mg/kg,
intraperitoneal), two concentric bipolar electrodes for intracranial
self-stimulation (ICSS) were implanted into the lateral
hypothalamic medial forebrain bundle, and two stainless steel wires (50
µm diameter) were inserted into the genioglossus
muscle [to monitor electromyogram (EMG) activity]. These electrodes
were run out to a cranioplastic cap, and together with two intraoral
catheters were attached to the skull (Nakamura and Ono 1986
, Nishijo and Norgren 1990
, 1991
and 1997
,
Nishijo et al. 1991
). After recovery from the surgery,
each rat was placed painlessly into a special stereotaxic apparatus
equipped with devices for sensory stimulation (Nishijo et al. 1998
). A "reward" (sucrose solution or ICSS) could be
obtained by licking a spout placed close to its mouth.
For chronic recordings, rats were reanesthetized (as above), and a hole
was drilled through the cranioplastic cap and underlying skull. The
exposed dura was excised, and the hole was either covered with
hydrocortisone ointment or filled with a few drops of a chloramphenicol
solution. The hole was then covered with a sterile Teflon sheet and
sealed with epoxy glue. After recovery from this procedure, each rat
was again placed into the stereotaxic device, and the Teflon sheet was
removed. Thereafter, a glass-insulated tungsten microelectrode (Z
= 1.0–1.5 M
at 1000 Hz) was inserted stepwise with a pulse
motor-driven manipulator into various parts of the AM and
hypothalamus.
Single neurons were tested with conditioned stimuli, including auditory, visual, somatosensory and olfactory stimuli, associated with a reward. In the auditory conditioned associative task, a 2.0-s conditioned tone preceded protrusion of the spout. Tones of 1200 Hz (Tone 1) and 4300 Hz (Tone 2) signaled availability of 0.3 mol/L sucrose or glucose, and ICSS (0.5-s train of 100 Hz, 0.3-ms capacitor-coupled negative square wave pulses), respectively. Tone 3 (2800 Hz) was used as a neutral sound (associated with no reinforcement). Similarly, either a 2-s stimulation of light (visual), an air puff (somatosensory) or odorized air (olfactory) were also associated with a sucrose solution or ICSS reward. The AM neurons were tested further with taste stimuli through intraoral cannulae at room temperature (23°C). Taste stimuli consisted of four standard solutions as follows: 0.1 mol/L NaCl, 0.3 mol/L sucrose, 0.01 mol/L citric acid, 0.0003 mol/L quinine hydrochloride (QHCl) and two other taste stimuli, 0.1 mol/L monosodium glutamate (MSG) and 0.2 mol/L lysine HCl.
Both neuronal and behavioral data in each trial of the conditioned associative task were counted from the peristimulus histograms in successive 100-ms bins for the following three periods: a pretrial control period (3 s), conditioned sensory stimulation period (2 s) and a rewarding stimulation period (2 s). Neuronal activity was compared by one-way ANOVA among discharge rates in the control period, conditioned sensory stimulation periods with different modalities and a reinforcement (rewarding) period.
Taste responses to intraoral infusions of water and tastant solutions
were analyzed statistically as previously described (Nishijo and Norgren 1990
, 1991
and 1997
). For taste
responses to intraoral infusions, all data analyses were based on the
neuronal activity in 5.0-s samples after the onset of the infusion. A
response to a taste stimulus was considered to be significant if the
neuronal activity increased or decreased at least 2.0 SD
from the mean of the prestimulus water response.
Experiment in the hypothalamus.
Male albino Wistar rats (n = 30), weighing 200–220 g at the beginning of the experiments, were used. The rats were divided into two groups as follows: control (unstressed, n = 15) and stressed (subjected to repeated cold stress; n = 15). The procedures for surgery and neurophysiological recordings were essentially the same as those described above for amygdala experiments. In hypothalamic studies, only conditioned tone stimuli (CTS) were used. The conditioned auditory tones and their related solutions were as follows: 1000 Hz, 0.2 mol/L L-lysine HCl; 2350 Hz, 0.15 mol/L monosodium L-glutamate (MSG); 3500 Hz, 0.05 mol/L L-arginine; 5400 Hz, 0.5 mol/L glycine; 8750 Hz, 0.15 mol/L NaCl (saline); and 1600 Hz, distilled water. Neuronal activity was recorded from the lateral hypothalamic (LHA) and medial hypothalamic areas (MHA), which included the ventromedial (VMH) and dorsomedial hypothalamic nuclei (DMH).
Rats in the stressed group were housed individually in the apparatus
with a built-in heater and cooler that could be controlled by an
adjustable self-timer, except when neuronal activity was recorded.
The environmental temperature in this apparatus alternated between 24
and -3°C at 1 cycle/2 h from 1000 to 1800 h (four cycles
between 1000 and 1800 h). It was kept at -3°C from 1800 h
until 1000 h the following morning. For the stressed group, the
recording session began 7 d after the start of stress loading; at
this point, the rats are thought to have reached a new steady state
(Hata et al. 1984
, Hori et al. 1993
).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONSUMMARYREFERENCES |
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Of the 1039 AM neurons, 420 (40.4%) responded to one or more sensory stimuli. Of the 420 responsive neurons, 227 responded exclusively to a single sensory modality (i.e., auditory, visual, oral-sensory, somatosensory or olfactory stimuli), 120 responded to various combinations of the sensory stimuli and the remaining 73 could not be classified. The responses to conditioned sensory stimuli were modulated during extinction and reassociation learning (data not shown). Of the 420 cells, 108 responded to oral-sensory stimulations (i.e., significant responses during ingestion of sweet solutions in the conditioned associative task). Of these 108 oral-sensory neurons, 84 could be further classified as taste and nontaste oral-sensory based on the data from intraoral infusions. Twenty-four cells were classified as taste sensitive because they responded more strongly to gustatory stimuli than to water, and 60 neurons as nontaste oral-sensory neurons. Of the 84 oral-sensory neurons tested with intraoral infusions, 11 responded to conditioned tones and 5 responded to unconditioned sounds.
Figure 1
shows an example of a unimodal taste neuron responding during intraoral
infusions. The neuron responded briskly to 0.0003 mol/L QHCl (Fig. 1A1
). Tongue muscle EMG activity occurred just after
infusion of QHCl solution, and did not correlate with the ongoing
neuronal discharge (Fig. 1A2
). The response profile of this
neuron during intraoral infusions is depicted in Figure 1B
.
The neuron responded selectively to QHCl. Neuronal activity of the same
neuron during the conditioned associative task is illustrated in Figure 1C
. The neuron did not respond during conditioned trials
using auditory (Fig. 1C1
), somatosensory (Fig. 1C2
) and visual (Fig. 1C3
) stimuli, nor during
licking a spout to obtain 0.3 mol/L sucrose. Thus, the neuron responded
only to QHCl infused through an intraoral cannula.
|
). Sucrose was most correlated with NaCl (
= 0.440) among the
four basic chemicals and least with QHCl ( = 0.138). NaCl was
most correlated with citric acid ( = 0.672) and less with
sucrose ( = 0.440) and QHCl ( = 0.573). Citric acid was
most correlated with QHCl ( = 0.905) and less with NaCl (
= 0.672). QHCl was most correlated with citric acid ( = 0.905) and least with sucrose ( = 0.138). This pattern of
interstimulus correlation coefficients suggests that taste quality is
organized on the basis of palatability; taste stimuli could be arranged
in one dimension in that sucrose (most palatable), NaCl, citric acid
and QHCl (least palatable) are sequentially plotted on a
one-dimensional line. If this one-dimensional arrangement of
taste chemicals is true, pairs of neighboring chemicals should be
highly correlated as noted above. The MSG had moderate correlation
coefficients with most sapid chemicals including NaCl ( = 0.862) and sucrose ( = 0.433). Moderate correlation
coefficients with NaCl and sucrose were consistent with those in the
previous study in the PBN of awake rats (Nishijo et al. 1991
). Lysine HCl at a concentration of 0.2 mol/L was not a
preferred solution for rats (Pritchard and Scott 1982
).
Lysine HCl was moderately correlated with the most aversive taste
stimulus (QHCl) ( = 0.716), and highly correlated with less
aversive chemicals such as citric acid ( = 0.852), and
moderately preferable solutions such as MSG ( = 0.890) and NaCl
( = 0.813).
|
and 1997
) (Fig. 2)
.
Correlation coefficients between basic sapid stimuli with a similar
degree of palatability were larger than those in the PBN, whereas
correlation coefficients between basic sapid stimuli with different
degrees of palatability were low in both the AM and PBN. For example,
correlation coefficients between NaCl and sucrose (palatable solutions)
were -0.129 and -0.126 in the PBN; these are significantly smaller
than the coefficient (0.440) in this study (two-tailed t
test after Fisher’s Z-transformation, P < 0.05).
Correlation coefficients between citric acid and QHCl (aversive
solutions) were 0.769 and 0.386 in the PBN, which were also
significantly smaller than that (0.905) in this study (two-tailed
t test after Fisher’s Z-transformation, P
< 0.05). Furthermore, correlation coefficients between sucrose
(most palatable) and QHCl (most aversive) were low (0.138) in the AM,
which was statistically not different from those (0.03 and 0.019) in
the PBN (two-tailed t test after Fisher’s
Z-transformation, P > 0.05). These results
strongly suggest a difference in taste coding between the PBN and AM,
e.g., taste quality vs. palatability. Hypothalamic neuronal responses.
Recordings were made from 421 neurons (215 in control rats; 206 in
repeated cold-stressed rats) in the LHA. The spontaneous neuronal
activity of the LHA neurons ranged from 0.7 to 62.9 spikes/s
(n = 215) under control conditions and from 2.8 to 53.3
(n = 206) during stress. The mean spontaneous neuronal
activity during stress (mean ± SEM, 17.0 ± 0.72) was 34% higher than the mean spontaneous neuronal activity under
control conditions (12.6 ± 0.66) (Student’s t test,
P < 0.01) (Fig. 3A1
). Each neuron was tested during CTS and subsequent ingestion of four
amino acids (lysine, MSG, arginine and glycine), NaCl and distilled
water. Of these 421 neurons tested, 135 (62.8%, 135 of 215) under
control conditions and 150 (72.8%, 150 of 206) during stress responded
to one or more phases of the task (responsive neurons).
|
shows an example of LHA neuronal responses in a control rat. The
inhibitory responses during the presentation of CTS (2350 Hz tone) in
preextinction trials (Fig. 3B1
) disappeared in successive
extinction trials (Fig. 3B2
) and reattained preextinction
levels during the relearning trials (Fig. 3B3
). It should be emphasized that several of the neuronal responses noted in stressed rats differed from those observed in control rats. First, responses of some LHA neurons to CTS in stressed rats were enhanced rather than decreased during extinction trials (data not shown). Second, some LHA neurons displayed opposite responses to CTS and corresponding unconditioned stimuli compared with those in control rats (e.g., in stressed rats, excitatory and inhibitory responses to conditioned and unconditioned stimuli, respectively; data not shown). Such unusual responses were not observed in control rats.
In the MHA, recordings were made from 127 neurons (67 in control rats, 60 in repeated cold-stressed rats). The spontaneous neuronal activity ranged from 1.3 to 19.1 spikes/s (n = 67) under control conditions and from 1.1 to 8.9 (n = 60) during stress. The mean spontaneous neuronal activity in stressed rats (mean ± SEM, 3.12 ± 0.22) was 36% lower than the mean spontaneous activity in control rats (4.87 ± 0.42) (P < 0.01). In the MHA, fewer neurons responded to CTS and/or licking, in contrast to those in the LHA. Of the 127 MHA neurons recorded, 9 (13.4%, 9 of 67) in the control setting and 3 (5.0%, 3 of 60) during stress responded similarly to various CTS and taste solutions (nondifferential neurons). No neurons that discriminated the various CTS and taste solutions were observed in the MHA.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONSUMMARYREFERENCES |
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In the present sample, QHCl-best neurons constituted 37.7% of the
gustatory responsive cells, almost equivalent to the sucrose-best
subset. This preferential coding of aversive stimuli such as bitter
taste in the gustatory modality in this study is consistent with
recent, human neuropsychologic studies in which preferential coding of
aversive or negative stimuli in gustatory (Zald et al. 1998
), visual (Adolph et al. 1995
) and olfactory
(Zald and Pardo 1997
) modalities was reported in the AM.
Analyses using correlation coefficients suggest that in the AM, taste
encoding is based on the palatability of the sapid chemicals. Results
of behavioral studies, however, conflict with such a conclusion;
lesions of the central nucleus of the AM appear to have little effect
on the responsiveness to the four standard sapid stimuli
(Galaverna et al. 1993
, Kiefer and Grijalva 1980
). In fact, basic oromotor responsiveness to gustatory
stimuli is nearly normal in chronically decerebrated rats (Grill and Norgren 1978a
and 1978b
). Lesions of the central nucleus of
the AM do alter the relationship between oromotor responses to taste
and the actual consumption of the stimuli (Seeley et al. 1993
). Larger lesions of the AM attenuate behavioral responses
to both preferred and aversive sapid stimuli, and alter conditioned
taste aversion (Kemble and Schwartzbaum 1969
,
Yamamoto et al. 1995
). Finally, fiber-sparing
lesions of the AM in monkeys reportedly change their food preferences
(Murray et al. 1996
). Thus, gustatory sensory activity
reaches the AM, and this information may be used in the ongoing process
of evaluation. The strong reciprocal connections between the central
nucleus of the AM and the brainstem taste nuclei imply that, whatever
the information is that is being added in the AM, it is likely to be
involved in modifying ascending gustatory neuronal activity.
Responses in the hypothalamus.
In this study, mean spontaneous neuronal activity increased in the LHA,
whereas it decreased in the MHA. Several lines of evidence suggest that
LHA and VMH neurons play a reciprocal role in the regulation of various
physiologic functions. Previous behavioral and neurophysiologic results
suggest that the LHA and VMH control feeding behavior in opposite
manners (Oomura et al. 1967
and 1969
, Shimizu et al. 1987
; Winn et al. 1984
). Chronic recording
of LHA and VMH neurons reveal that the activity of the majority of LHA
neurons increases during electroencephalogram arousal and decreases
during slow-wave sleep; the activity of a significant number of VMH
neurons that respond during feeding is reciprocal to that of LHA
neurons (Shibata et al. 1987
).
Shimizu et al. (1989a
and 1989b)
reported that the
activity of 80% of LHA neurons is inhibited by immobilization stress,
acting via inhibitory serotonergic activity (which may increase in LHA
during immobilization). Might such a mechanism account for
immobilization-induced anorexia? In this study, LHA neuronal
activity increased during stress. Furthermore, serotonin levels
decreased in several brain areas, including hypothalamus, during
repeated cold stress (Hata et al. 1991
). The discrepancy
between our results and those of other studies (Shimizu et al. 1989a
and 1989b
) might be explained by the different stressors
employed, i.e., repeated cold stress is a mild and chronic stress model
associated with hyperphagia (Kondoh et al. 1996
),
whereas immobilization stress is characterized by anorexia in
association with a severe and acute stress (Shimizu et al. 1989b
). In general, the results of both previous and current
studies are consistent with the idea that the LHA is an important
feeding center.
In this study, the responses of some neurons to conditioned stimuli
were enhanced during extinction, and the response direction to
conditioned and unconditioned stimuli were opposite in stressed rats.
It has been reported in nonstressed, normal rats that neuronal
responses to conditioned stimuli readily disappear after several
extinction trials, and that the direction of neuronal responses (i.e.,
excitation or inhibition) to conditioned stimuli is the same as that of
the responses to corresponding unconditioned stimuli in the LHA as well
as the AM. This phenomenon might constitute a neural basis for
appetitive behaviors (Muramoto et al. 1993
, Ono et al. 1986
). Conceivably, the abnormal responses of the LHA
neurons in stressed rats might be related to alterations in feeding
behaviors during stress (Antelman et al. 1976
,
Kondoh et al. 1996
, Martí et al. 1994
, Vaswani et al. 1983
).
Role of the hypothalamus and amygdala in feeding behavior during stress.
Anatomically, the hypothalamus is one of the main recipients of AM
efferents (Amaral et al. 1992
). It has been reported
that inactivation of the AM alters the spontaneous firing rates of LHA
neurons, and that LHA neuronal responses to conditioned stimuli
associated with reward depend on intact AM function (Fukuda et
al. 1987
, Nakamura et al. 1987
). The AM
has been reported to play a pivotal role in the manifestation of
various stress symptoms (Merali et al. 1998
, Pich et al. 1995
). Such findings suggest that increased spontaneous
firing rates and abnormal responses of LHA neurons in stressed rats can
be attributed to altered AM functions due to stress (though AM neuronal
responses were not recorded in stressed rats in this study). Taken
together, the hypothalamus and AM might work as a functional unit to
modulate feeding behavior.
|
SUMMARY |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONSUMMARYREFERENCES |
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), and both
regions send descending projections to the NTS and PBN (van der Kooy et al. 1984
, Veening et al. 1984
). These results strongly suggest that
these forebrain areas may be higher centers that modulate feeding
behavior.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 Supported in part by the Japanese Ministry of
Education, Science and Culture Grants-in-Aid for Scientific Research
(08408036, 08279105, 10680762, 10164219), and by Funds for
Comprehensive Research on Aging and Health.
4 Abbreviations used: AM, amygdala; CTS,
conditioned tone stimuli; EMG, electromyogram; ICSS, intracranial
self-stimulation; LHA, lateral hypothalamic area; MHA, medial
hypothalamic area; MSG, monosodium glutamate; NTS, nucleus of the
solitary tract; PBN, pontine parabrachial nucleus; QHCl, quinine
hydrochloride; VMH, ventromedial hypothalamic nucleus.
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