Chem. Senses 27: 153-158,
2002
© Oxford University Press 2002
Parabrachial Unit Activities After the Acquisition of Conditioned Taste Aversion to a Non-preferred HCl Solution in Rats
Department of Behavioral Physiology, Graduate School of Human Sciences, Osaka University, 1-2 Yamadaoka, Suita, Oaka 565-0871, Japan
Correspondence to be sent to: Tsuyoshi Shimura, PhD, Department of Behavioral Physiology, Graduate School of Human Sciences, Osaka University, 1-2 Yamadaoka, Suita, Oaka 565-0871, Japan. e-mail: shimura{at}hus.osaka-u.ac.jp
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Abstract |
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In a behavioral experiment, rats reliably acquired a taste aversion to non-preferred 0.01 M HCl that had been previously paired with intraperitoneal injection of 0.15 M LiCl. These rats showed aversions to other acidic solutions such as malic acid and tartaric acid. In a neurophysiological experiment, the neuronal activities of the parabrachial nucleus (PBN) were recorded after the acquisition of conditioned taste aversion (CTA) to 0.01 M HCl in urethane-anesthetized rats. Neuronal responses to the conditioned stimulus (CS) did not change on the whole but decreased in the dorsal region to the brachium conjunctivum. The proportion of HCl-best to NaCl-best units was lower in the CTA group than in controls. The spontaneous firing rate was lower in the CTA group than in controls. Correlation coefficients between the HCl CS and normally preferred tastes (sucrose and NaCl) were more negative and those between HCl and quinine were more positive in the CTA group than in the controls. These results may be explained by the notion that gustatory responses of PBN neurons are concerned with alterations in taste hedonics after the acquisition of conditioned taste aversions.
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Introduction |
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TopAbstractIntroductionExperiment 1Experiment 2References |
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When consumption of a taste substance is followed by visceral malaise, animals avoid ingesting this substance on future occasions. This behavior is based on a biologically salient learning called a conditioned taste aversion (CTA), and plays an important part for the animal's survival (Bures et al., 1998
).
Several lines of evidence have shown that the pontine parabrachial nucleus
(PBN), the second gustatory relay in rodents, is critically involved in the
formation of CTA. Bilateral electrolytic
(Di Lorenzo, 1988;
Spector et al., 1992;
Reilly et al., 1993;
Sakai and Yamamoto, 1998) or
ibotenic acid lesions (Scalera et
al., 1995; Yamamoto
et al., 1995; Grigson et al.,
1997b,
1998) thoroughly disturbed the
acquisition of CTA. Intracerebral injections of several chemicals
(Ivanova and Bures, 1990;
Bielavska and Krivanek, 1994;
Sacchetti and Bielavska, 1998;
Gallo et al., 1999)
in the PBN impaired the formation of CTA. Although these results suggest that
the integrity of the PBN is required for the acquisition of CTA, it is still
unclear how taste information is processed in the PBN for the establishment of
CTA. Previously, we reported that PBN neuronal responses are more salient to
the conditioned stimulus (CS) in conditioned animals than in unconditioned
control animals (Shimura et al.,
1997b). Several studies also reported a similar modification in
the responsiveness to the CS in other gustatory areas
(Aleksanyan et al.,
1976; Buresova et al.,
1979; Chang and Scott,
1984; Di Lorenzo,
1985; Yamamoto et
al., 1989; Yasoshima
et al., 1995;
Yasoshima and Yamamoto, 1998).
However, it should be noted that the CS used in those studies were normally
preferred taste solutions such as saccharin or NaCl. It is believed that the
taste quality seems to contribute to its adequacy as a cue for a learned taste
aversion (Kalat and Rozin,
1970; Nowlis et al.,
1980). In fact, it has been documented that the aversion is much
stronger to a nonpreferred CS than to a preferred CS
(Etscorn, 1973;
Massey and Calhoun, 1977). In
contrast, it was reported that rats failed to acquire an aversion to
non-preferred citric acid as the CS
(Brackbill et al.,
1971). These results indicate that the neural mechanisms
underlying the CTA may be different between naturally preferred and
non-preferred tastes. To examine the possibility, we examined the
characteristics of CTA to a non-preferred sour taste using a behavioral
experiment, then compared the firing patterns of PBN neurons in response to
various taste stimuli in rats previously conditioned to non-preferred HCl with
those of unconditioned control rats. |
Experiment 1 |
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TopAbstractIntroductionExperiment 1Experiment 2References |
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Materials and methods
Twelve male Wistar rats (230-260 g) were used. They were divided into two groups and habituated to a schedule with access to one bottle of fluid for 15 min in a test box for 5 days. On day 6, each rat in the experimental group (n = 6) was given 20-min access to 0.01 M HCl (CS) in the home cage and then injected with 0.15 M LiCl (2% of body wt, i.p.). The other rats (n = 6) were given 20-min access to distilled water in the home cage and then injected with saline (2% of body wt, i.p.). On day 7, all the rats were retrained to drink distilled water for 15 min in the test box. On days 8-10, 15 taste solutions and distilled water were randomly presented for 10 s to each rat in the test box and the number of licks to each solution was counted. We used 15 different taste stimuli, four of which were prototypes of the putative basic taste [0.5 M sucrose, sweet; 0.1 M NaCl, salty; 0.01 M HCl, sour (the CS); 0.01 M quinine hydrochloride (QHCl), bitter]. The remaining 10 were NaNO3 (0.01 M), a mixture of 0.1 M monosodium glutamate and 0.01 M inosine 5'-monophosphate, HCl (0.003, 0.006, 0.03 and 0.06 M), malic acid (0.01 M), tartaric acid (0.01 M), KCl (0.1 M), MgCl2 (0.03 M) and NH4Cl (0.1 M).
Results
Figure 1 shows the mean lick numbers for 10 s to the 15 taste stimuli and distilled water in the experimental and control groups. Two-way analysis of variance (ANOVA) with repeated measures (Group x Stimulus) detected a significant main effect of Group [F(1,10) = 12.13, P < 0.01] and Stimulus [F(15,150) = 21.49, P < 0.001], and a Group x Stimulus interaction [F(15,150) = 2.91, P < 0.001]. Post-hoc comparisons using the Fisher's least significant difference test indicated that licks to 0.01, 0.03 and 0.06 M HCl, malic acid, and tartaric acid were lower in the experimental group than in the control group.
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Discussion
These results clearly demonstrated that the rats in the experimental group
acquired a strong aversion to the 0.01 M HCl CS. As the aversion generalized
to 0.03 and 0.06 M HCl, malic acid and tartaric acid but not to the other
solutions, the acquired aversion seems to be specific to acidic tastes.
Although it was reported that non-preferred tastes were inadequate as a cue
for a CTA (Brackbill et al.,
1971), the present results support previous reports that rats can
acquire an aversion to normally non-preferred sour tastes
(Fitzgerald and Burton, 1981;
Smith and Theodore, 1984;
Grigson et al.,
1997a). Therefore, in experiment 2 we examined firing
characteristics of PBN neurons in rats who had previously acquired an aversion
to 0.01 M HCl.
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Experiment 2 |
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TopAbstractIntroductionExperiment 1Experiment 2References |
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Materials and methods
Forty-eight male Wistar rats (200-350 g) were used. They were divided into
two groups and acclimated to a schedule with access to one bottle of fluid for
20 min in the morning (10:00) and 60 min in the afternoon (17:30). The 20 min
morning period was the training and testing session during which all
experimental manipulations were performed. The afternoon session was always a
distilled water presentation and allowed for adequate hydration of the
animals. After baseline responses to water during 20 min/day were established,
the CTA group (n = 26) received three conditioning trials on
alternate days; each rat was given 20-min access to 0.01 M HCl (CS) in the
home cage and then injected with 0.15 M LiCl [2% of body wt, i.p.;
unconditoned stimulus (US)] in each trial. The control animals (n =
22) were similarly treated except that they were given physiological saline
instead of LiCl after the CS. At least 24 h after the last injection of LiCl
or saline, each rat was anesthetized with urethane (1.3 g/kg body wt, i.p.).
The body temperature was maintained at 
36.8°C using an infrared lamp.
Neuronal activity was recorded from the PBN with a glass-insulated tungsten
electrode (Z = 1.5-3 M
at 1 kHz). The electrode was oriented
20° from vertical (tip pointing rostrally) to avoid the transverse sinus.
Neuronal activity was amplified with a conventional method, monitored with a
computer system (CED 1401, Spike2; Cambridge Electronic Design, Cambridge,
UK), and stored on a DAT recorder for offline analysis. After isolating
unitary discharges in the PBN, taste stimuli were presented at room
temperature (23-24°C) into the oral cavity of animals according to a
method described elsewhere in detail
(Shimura et al.,
1997b). Each stimulus trial consisted of a 10 s flow of distilled
water, a 10 s taste stimulus and a 10 s rinse with distilled water. The flow
rate was 0.5 ml/s for all the stimuli, including the rinse. If taste responses
remained after the 10 s post-stimulus rinse with distilled water, we continued
the water rinse until the neural activity returned to the pre-stimulus level.
Ninety seconds were allowed to elapse between the stimuli to avoid the effects
of adaptation. The taste stimuli used were the same as those in experiment 1.
All the stimuli were made with reagent grade chemicals and dissolved in
distilled water.
All data analyses were based on the neuronal activity in 5 s samples. Spontaneous activity and responses to pre-stimulus water were calculated from multiple samples. The spontaneous rate was determined during the periods just before the pre-stimulus water rinse. Water and taste responses were calculated during the first 5 s period after the onset of stimulation with pre-stimulus water or a taste solution. An adjusted score (a net response rate) was employed for data analyses, which was obtained by subtracting the mean raw water responses from the raw taste responses. A response to taste stimulus was considered to be significant if the neuronal activity increased or decreased at least 2 SD from the mean of the spontaneous activity of the neuron. After the recording sessions, electrolytic lesions were made in the final recording sites (20 µA for 20 s, electrode positive). The rats were perfused intracardially with phosphate-buffered saline and 10% formalin. The location of each recording site was histologically examined.
Results
The CTA animals acquired a strong aversion to the CS (0.01 M HCl), because the intake of the CS significantly decreased across trials [F(2,50) = 77.81, P < 0.05].
Taste-responsive neurons in the CTA and control groups were found both
above and below the brachium conjunctivum in the area that has been described
previously as the pontine taste area
(Norgren and Pfaffmann, 1975).
As illustrated in Figure 2, there was no fundamental difference in the distribution of recording sites
between the CTA and control groups. A total of 95 taste-responsive neurons
were recorded from the PBN: 49 from the CTA and 46 from the control groups.
All the neurons showed excitatory responses to at least one of the four basic
tastes (sucrose, NaCl, HCl or QHCl). The mean spontaneous firing rate in the
CTA group was 2.53 ± 0.29 (mean ± SE). It was significantly
lower than that of the control group (4.27 ± 0.59) (t = 2.69,
P < 0.01).
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Figure 3 illustrates the
response profiles of PBN taste neurons to the four standard taste stimuli of
both groups. On the basis of their largest response to the four basic taste
stimuli, we classified PBN neurons as follows: one sucrose-best (2%), 39
NaCl-best (80%) and nine HCl-best (18%) in the CTA group; three sucrose-best
(6%), 28 NaCl-best (61%) and 15 HCl-best (33%) in the control group. Taste
neurons are ordered by best-stimulus category and, within categories, by
response magnitude. As shown in the figure, the proportion of HCl-best to
NaCl-best neurons was significantly smaller in the CTA group than in the
control group (one-tailed 
2 test, P < 0.05). In
addition, the proportion of HCl-best to NaCl-best units tended to be higher in
the dorsal than in the ventral PBN in controls (83.3 versus 35.3%), but not in
the CTA group (23.1 versus 16.7%). The number of HCl-best units was smaller in
the CTA group than in controls regardless of the recording sites.
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Figure 4A shows the mean responses of all PBN neurons to the 15 taste stimuli in both groups. Two-way analysis of variance (ANOVA) with repeated measures (Group x Stimulus) revealed a significant main effect of Stimulus [F(14,1302) = 62.88, P < 0.001]. However, a main effect of Group and a Group x Stimulus interaction were not significant [F(1,93) = 1.276, F(14,1302) = 0.889, respectively]. Figure 4B-D indicate the mean responses of PBN neurons to taste stimuli recorded from the area dorsal to, within, and ventral to the brachium conjunctivum, respectively. A three-way ANOVA with repeated measures (Group x Region x Stimulus) detected a main effect of Stimulus [F(14,1246) = 56.22, P < 0.001] and a Group x Region x Stimulus interaction [F(28,1246) = 1.72, P < 0.05]. Other main effects and interactions were not significant. Post-hoc analyses of these data using the Fisher's least significant difference test indicated that responses to 0.01, 0.03 and 0.06 M HCl and malic acid were higher in the control group than in the CTA group in the dorsal PBN. Responses to NaCl and NaNO3 were higher in the control group than in the CTA group in the dorsal and ventral PBN, and lower in the control group than in the CTA group in the brachium conjunctivum (Ps < 0.05).
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To investigate how similarly the neurons responded to the four basic taste stimuli, we calculated Pearson product—moment correlation coefficients between the 0.01 M HCl CS and other three basic tastes (sucrose, NaCl and QHCl). As shown in Figure 5, the correlation coefficients between the HCl CS and normally preferred tastes (sucrose and NaCl) were more positive in the control group than in the CTA group except for neurons recorded ventral to the brachium conjunctivum. In contrast, when calculated from all the neurons, the correlation coefficient between HCl and QHCl was higher in the CTA group than in controls (Figure 5A). The tendency was more prominent in neurons recorded dorsal to the brachium conjunctivum (Figure 5B).
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Discussion
The PBN neuronal responses to the CS showed slight but noticeable changes
after the acquisition of CTA to the normally non-preferred HCl CS. As the
animals in the CTA group acquired a robust aversion to the CS, these
alterations in PBN neuronal activities seem to be plastic as suggested in our
previous study (Shimura et al.,
1997b). The present results, however, were somewhat different from
previous ones using a normally preferred taste as the CS. In the previous
study, PBN neuronal responses to the CS increased after the acquisition of CTA
to the NaCl CS compared with those in controls. In contrast, neuronal
responses to the HCl CS in the present study did not change on the whole but
decreased only in the dorsal PBN. In addition, the proportion of HCl-best to
NaCl-best units was lower in the CTA group than in controls in the present
study. There was no difference in the proportion of NaCl-best to HCl-best
units between the CTA and control groups in the previous study. These
comparative results, therefore, suggest that the PBN neuronal mechanisms
underlying the CTA are different between preferred and non-preferred tastes as
the CS. Alternatively, these minor alterations in the firing rates may
indicate that some change in taste hedonics rather than taste quality is
primarily responsible for the acquisition of CTA, because the PBN is thought
to be concerned with processing of not only taste quality but also taste
hedonics (Yamamoto et al.,
1994a,
b).
The spontaneous firing rate was also lower in the CTA group than in controls in the present study. On the other hand, it was not different between the CTA and control groups in the previous study. Our preliminary results indicated that the spontaneous firing rate was lower in rats given three injections of LiCl US without CS than in the control rats. Injections of LiCl US might generally suppress the PBN neuronal activity in the CTA group. However, as we used a net response rate (raw taste response — raw water response) as a taste response for data analyses, lowered spontaneous firing rates in the CTA group might be negligible for responses to each taste.
It was documented that HCl-best units were preferentially located in the
dorsal PBN (Ogawa et al.,
1984,
1987). In line with these
observations, the proportion of HCl-best to NaCl-best units was higher in the
dorsal than in the ventral PBN in controls in the present study. However, the
number of HCl-best units was smaller in the CTA group than in controls
regardless of the recording sites. The lowered proportion of HCl-best units in
the CTA group might reflect an overall decrease in the response magnitude to
HCl in this group. Thus, originally second-best to NaCl units presumably
turned out to be NaCl-best in the CTA group after the acquisition of taste
aversion.
Interstimulus correlation coefficients indicate that the taste similarities
are lower between the HCl CS and normally preferred tastes (sucrose and NaCl),
and higher between normally non-preferred QHCl in the CTA group than in
controls. These results suggest that the hedonics of originally non-preferred
HCl becomes worse after the acquisition of taste aversion to the HCl. Thus,
the PBN appears to be concerned with alterations in taste hedonics induced by
aversion learning. In line with this suggestion, c-fos
immunoreactivity studies (Yamamoto et al.,
1994a,
b) have shown that the PBN is
involved in the processing of taste hedonics as well as taste quality. As the
recipient zone for originally preferred saccharin taste shifts from the dorsal
lateral to external lateral subnucleus after the acquisition of CTA, it is
plausible that the neurons in the lateral portion of the PBN are primarily
responsible for the acquisition of CTA. Behavioral lesion studies
(Sakai and Yamamoto, 1998;
Reilly and Trifunovic, 2000)
also support this notion. Therefore, we could have obtained clearer
alterations in taste responses if the neurons from the lateral PBN were
recorded.
The importance of the PBN in CTA and sodium appetite has been repeatedly
documented (Spector et al.,
1992; Reilly et al.,
1993; Scalera et al.,
1995; Yamamoto et
al., 1995; Grigson et al.,
1997b,
1998;
Sakai and Yamamoto, 1998). We
have shown that PBN neuronal responses to high concentrations of NaCl decrease
in sodium-deprived rats (Shimura et
al., 1997a), which may be favorable for ingestion of an
otherwise unpalatable concentration of NaCl. It is thus accepted that PBN
neuronal responses to NaCl increase when NaCl is aversive in CTA and decrease
when NaCl is preferred in sodium appetite. Although not so robust as shown
above for NaCl responses, we could detect the decrease in responsiveness of
PBN neurons to the HCl CS in the present study. Alterations in the neuronal
activity of PBN neurons may contribute for animals to discriminate, select and
avoid the relevant stimulus selectively.
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Acknowledgments |
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We thank Noritaka Sako and Junko Tamura for their assistance in conducting these experiments. This work was supported by Grant-in-Aid for Scientific Research (nos 11680787 to T.S. and 11557135 to T.Y.) from the Ministry of Education, Science, Sports and Culture of Japan, and by Research for the Future Program (JSPS-RFTF97L00906 to T.Y.) from the Japan Society for the Promotion of Science.
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TopAbstractIntroductionExperiment 1Experiment 2References |
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Accepted October 31, 2001
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