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Context dependency of conditioned aversions to familiar and novel fluids
Learning and Motivation 37 (2006) 113–130 www.elsevier.com/locate/l&m
Context dependency of conditioned aversions to familiar and novel Xuids 夽 Kiyoshi Ishii a,¤, Yoshio Iguchi a, Kosuke Sawa b b
a Department of Psychology, Nagoya University, Japan Japan Society for Promotion of Science, Nagoya University, Japan
Received 25 November 2004; received in revised form 11 April 2005 Available online 19 July 2005
Abstract Using a context discrimination procedure and rats as the subjects, the formation of contextdependent aversions to novel and familiar Xuids was investigated. Experiment 1 revealed that context dependency could be established to a novel Xuid (saccharin) after three cycles of context discrimination training and that the acquired context dependency was revealed also to a second familiar Xuid (water) presented in the following test. Experiment 2 showed that the formation of the context-dependent aversion and its transfer to a second Xuid was not aVected by whether Xuid presented during discrimination was novel (saccharin) or familiar (water). Experiment 3 demonstrated that when the same water was given both in the two training contexts and in the home cages of the subjects during discrimination, the context-dependent aversion formed was speciWc to it. These Wndings can be explained in terms of a simple summation eVect of Xuid-nausea and context-nausea associations. © 2005 Elsevier Inc. All rights reserved. Keywords: Context dependency; Conditioned aversion; Occasion setting; Rat
夽 This research was supported by Grant-in-Aid for ScientiWc Research, 15530469, from Japanese Ministry of Education, Culture, Sports and Technology to the Wrst author. * Corresponding author. Fax: +81 52 789 2223. E-mail address: [email protected] (K. Ishii).
0023-9690/$ - see front matter © 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.lmot.2005.04.002
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It is now widely acknowledged that responses acquired through a Pavlovian conditioning procedure can become context-dependent (e.g., Bouton & King, 1983; Bouton & Swartzentruber, 1986; Hall & Honey, 1990). This is also true for a response established in the conditioned taste aversion paradigm. For example, the aversive response acquired to a taste attenuates when tested in a context diVerent from the one in which it was conditioned (Bonradi, Honey, & Hall, 1990). Furthermore, after the conditioned taste aversion has been extinguished in a diVerent context, it is renewed when the subject is returned to the original conditioning context (e.g., Archer, Sjoden, & Nilsson, 1985; Holder, 1988). The context dependency of conditioned aversion is also demonstrated in the procedure of context discrimination training. In this paradigm, subjects are repeatedly given paired presentations of a Xuid and nausea-inducing substance (usually lithium chloride: LiCl) in one “conditioned” context, while presented the same Xuid alone in another “neutral” context. After receiving several cycles of such context discrimination training, subjects come to avoid consuming the Xuid more in the former context than in the latter. In most of the studies that showed successful formation of context-dependent aversion (e.g., Boakes, Westbrook, & Barnes, 1992; Boakes, Westbrook, Elliott, & Swinbourne, 1997; Puente, Cannon, Best, & Carrell, 1988), the acquired context dependency was speciWc to the Xuid given during context discrimination training. In the following test, the amount of consumption of a second Xuid that had not been paired with LiCl did not diVer between the two contexts. This fact seems to suggest that the contextual cues did not directly become associated with nausea but rather acquired the property of an “occasion-setter” (Holland, 1983) or a discriminative cue that determines the meaning of the Xuid presented in it. Boakes et al. (1997) found that the Xuid-speciWc context dependency of aversion was established only when the Xuid was preexposed or familiar to the animals. When a novel Xuid was given, on the other hand, subjects revealed no evidence of context discrimination. Thus, they argued that a latent inhibition eVect (Lubow, 1973, 1989) is responsible for the successful formation of context-dependent aversion: When a preexposed Xuid is given, animals still consume a substantial amount of it safely in the neutral context, even after they received the initial paired presentations of the Xuid and LiCl in the conditioned context. When the Xuid is novel, on the other hand, animals come to consume little amount of it in the neutral context due to rapid acquisition of aversion to that Xuid, and thus the discrimination between the two contexts is hard to establish. In other words, Boakes et al. (1997) assumed that only the Xuid become associated with nausea, with the rate of development of this association determining whether or not the context can acquire the function of an occasion setter. However, it should be possible to establish a context-dependent aversion to even a novel Xuid, if the rate of development of its association with nausea is the crucial condition for it. The associability of a stimulus is reduced not only by its preexposure but also by decreasing its salience (here it means physical intensity). When a novel but not so salient Xuid is presented during discrimination training, then, it might be expected that subjects would continue consuming some amount of it in the neutral context, and thus eventually show context-dependent aversion.
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In fact, Loy, Alvarez, Rey, and Lopez (1993) demonstrated that context-dependent aversion could be established to novel sucrose. However, they also found that the established context-dependent aversion was revealed to a second Xuid (coVee) presented in the following test. This Wnding seems to suggest that the context did not acquire the property of an occasion-setter but rather become associated directly with nausea. When considering the nature of the Xuid given in the experiments by Loy et al. (1993), it seems that whether the Xuid given during context discrimination is novel or familiar determines the Xuid-speciWcity of the acquired context dependency. As Boakes et al. (1997) pointed out, however, the methods of the experiments that showed the Xuid-speciWc context dependency of aversion diVered also in some other aspects from that used by Loy et al. (1993). Among these diVerences was the Xuid that was supplied daily in the home cages of the subjects during discrimination training. In most of the studies that showed Xuid-speciWc context dependency of aversion, the Xuid was the same as that presented during context discrimination (e.g., water or saline in Puente et al., 1988, Experiment 2; saccharin in Boakes et al., 1997, Experiment 2; but see also the Wndings in Experiment 3 by Boakes et al., 1997, which are discussed later). In the experiments by Loy et al., on the other hand, animals were given water in their home cage. It is known that acquisition of aversion to a context is apparently “potentiated” (e.g., Durlach & Rescorla, 1980, but see also, e.g., Symonds & Hall, 1999) when subjects receive a Xuid with a novel taste, or even water, during conditioning (e.g., Best, Brown, & Sowell, 1984; Boakes et al., 1992; Mitchell & Heyes, 1996). However, daily consumption of the same Xuid safely in the home cage during context discrimination might function as additional extinction trials and thus retard the acquisition of aversion to that Xuid. Then the ability of the Xuid to potentiate the context-nausea association would also be reduced, if the potentiation is interspersed with within-compound (i.e., Xuid-context) association (see e.g., Durlach & Rescorla, 1980, Experiment 4). Consequently, apparent discrimination might be revealed only when both contextual cues and Xuid, each of which acquires only a weak association with nausea, are presented simultaneously. The implication is that the Xuid-speciWc context dependency of aversion found in most of the previous studies can be explained in terms of a simple summation of the associative strength acquired by each of these two events, if some threshold is assumed for the aversive behavior to be apparent. The aim of the present study was to investigate the process of the formation of context-dependent aversion to both novel and familiar Xuids, and to compare the properties acquired by the context. If successful formation of context-dependent aversion depends solely on the subjects’ experience of consuming some amount of the Xuid in the neutral context during discrimination training, it should be possible to condition to even a novel Xuid, if it is not too salient. Novelty of the Xuid might determine whether or not the acquired context dependency is speciWc to the Xuid given during context discrimination. Furthermore, Xuid-speciWc context dependency of aversion might also be evident when, the Xuid presented in both of the two contexts is also given in the subjects home cage during discrimination training. These predictions were examined in three experiments.
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The conventional single-bottle test was adopted in the present experiments, to compare the Wndings with those in the many previous studies that have also used this method.
Experiment 1 Experiment 1 examined whether context-dependent aversion can be established by presenting novel Xuid (0.05% saccharin solution) during discrimination training. Our preliminary investigations showed that in the paradigm of simple conditioned aversion, the rate of acquisition to 0.05% saccharin solution was signiWcantly less than that to 0.1% solution, the concentration that has been used most frequently as the CS in previous studies. It was then tested whether consumption of a second Xuid was also suppressed in the conditioned context. Following the design of Loy et al. (1993), animals were additionally given water daily in their home cage throughout the experiment, but no scent was presented in either the conditioned or neutral context. In addition, tap water was also presented as the second Xuid of the test. Loy et al. used coVee solution that was only preexposed for two days as the test Xuid. To evaluate the degree of aversion acquired by the context itself, however, it would be more reasonable to test with a quite familiar Xuid that evokes no neophobic response. Method Subjects The subjects were 16 male rats of the Wistar strain, about 70–75 days of age at the beginning of the experiment, with a mean free-feeding weight of 252 g (range: 232– 276 g). They were born and reared in the colony room of the Department of Psychology, Nagoya University. Each subject was housed individually in its home cage (31 £ 36 £ 18 cm, with the Xoor covered with wooden chips and a stainless-steel grid roof), which was placed in the colony room that was illuminated on a 12 h light /12 h dark daily cycle. Rats had free access to food. The temperature and humidity of the colony room were maintained at 24 °C and 50%, respectively. Fluids and contexts A 0.05% saccharin solution was presented during context discrimination training. The unconditioned stimulus (US) was an intraperitoneal injection of 0.15 M lithium chloride (LiCl) at 10 ml/kg of body weight. Two kinds of cages and rooms that diVered from each other in the aspects described below were used as the two contexts. Context A consisted of 16 transparent acrylic cages (27 £ 43 £ 20 cm) with a stainless-steel grid roof, placed in an experimental room outside the animal laboratory with dim (0.5 lx) illumination and constant noise (76 dB) produced by a sound stimulator with a loudspeaker. The Xoor of each cage was covered with wooden chips. A stainless-steel spout connected to a graduated cylinder could be inserted in the center of the roof. Context B consisted of 16 opaque polycarbonate cages (31 £ 36 £ 18 cm) with a plain wooden board roof, placed in an experimental room with relatively bright illumination (54 lx). The Xoor of each cage was covered with gravel made by paper, and the same spout as
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used in context A could be inserted into the center of one end wall. The temperature and humidity were kept at 24 °C and 50%, respectively, in both of the two contexts. Procedure For three days before the start of experiment, subjects were on a restricted access to water schedule. They could consume tap water only during two daily sessions of 20 min, initiated at 12:00 and 16:00 in their home cages. Water drinking in the two contexts began the following day, to allow animals to consume saccharin solution in each context from the beginning of context discrimination training. On the Wrst day, animals were placed in Context A at 12:00. Ten minutes later, they were allowed access to water for 10 min. Then they were returned to their home cages. At 16:00 on the same day, subjects were placed in Context B and received the same procedure as given in Context A. On the second day, animals were placed in Context B at 12:00 and in Context A at 16:00. The procedure given in each context was exactly the same as that on the Wrst day. This procedure schedule was performed twice (from Day 1 to Day 4). Context discrimination training (Day 5–16) consisted of three cycles, each containing four daily sessions that began at 12:00. On the Wrst session in each cycle, animals were divided into two subgroups, matched by body weight and the amount of water consumed on Day 4, and placed for 10min in either Context A or Context B. They were then given saccharin solution for 10min. Upon removal of the spout, animals were immediately injected with LiCl. They were then placed back in their home cages. On the second and the fourth days of each cycle, subjects were presented water for 10min in their home cages. A non-conditioning session in the neutral context was given on the third day of each cycle: animals were placed for 10min either in Context B or in Context A. They then had access to the saccharin solution for 10min, without subsequent injection of LiCl. Four test sessions followed the context discrimination training. On the Wrst session (Day 17), half of the subjects in each group were placed in the conditioned context for 10 min, and then were presented water for another 10 min. On the next day (Day 18), they were placed again in the conditioned context but were given saccharin solution for 10 min. On Day 19, these subjects were given water for 10 min in the neutral context. Finally, on Day 20, they were presented saccharin solution for 10 min in the neutral context. The remaining half of the subjects Wrst received two test sessions in the neutral context, followed by another two sessions in the conditioned context. Throughout all drinking training, context discrimination and test sessions, the amount of Xuid consumed was measured to the nearest 0.2 ml. In addition to these daily sessions that began at 12:00, animals were also given water for 10 min at 16:00 in their home cage throughout the experiment, except during the training of water drinking. The spout presented was the same as that used in both of Context A and Context B. Results and discussion The overall mean amount of consumption of water on the last Xuid drinking training in each context which began at 12:00 was 9.80 ml and did not diVer signiWcantly
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between the two contexts (t (14) < 1). Also through the rest of the experiment, no signiWcant subgroup diVerences in the amount of consumption of Xuid were seen. Therefore, the scores of the two subgroups were combined, and a signiWcance level of p < .05 was adopted in this and all subsequent analyses. Fig. 1 depicts the mean amount of saccharin solution consumed in three conditioning and three non-conditioning sessions. It shows that while the amount of consumption in both the Wrst and the second non-conditioning sessions is less than that in the previous conditioning session in each cycle of discrimination training, consumption in the last non-conditioning session is more than that in the last conditioning session. These results indicate that after three cycles rats were able to discriminate the conditioned context from the neutral one. A two-way ANOVA with cycle and context as factors was conducted on the scores shown in Fig. 1. It revealed a signiWcant main eVect of cycle (F (2, 30) D 111.66) and an interaction between the two factors (F (2, 30) D 35.64). Subsequent analyses of the interaction showed that the simple main eVect of cycle was signiWcant only in the conditioned context: Amount of consumption decreased gradually as a function of cycles. The simple main eVect of context was found in all three cycles: Both during the Wrst and second cycle, the amount of consumption was more in the conditioned context than in the neutral context. During the third cycle, on the other hand, it was less in the conditioned context than in the neutral context. Fig. 2 shows the mean amount of saccharin solution and water consumed in the test sessions. It is obvious that both consumption of saccharin solution and of water were less in the conditioned context than in the neutral context, suggesting that not only saccharin solution but also water was avoided more in the former. Consumption of water was more than that of saccharin in both conditioned and neutral contexts, indicating less aversion to water than to saccharin despite the fact that the test to the former preceded that to the latter.
Fig. 1. Experiment 1: mean consumption of saccharin solution during three cycles of the discrimination stage. Each cycle consisted of a conditioning session (C) in one context and an extinction session (E) in another context.
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Fig. 2. Experiment 1: mean consumption of saccharin and water in each of the two contexts on the test.
Statistical analyses also supported these observations. A two-way ANOVA revealed that both the main eVect of context (F(1,15)D41.16) and that of test Xuid (F(1,15)D18.66) were signiWcant, but that the interaction of these two factors was not signiWcant. The procedure of Experiment 1 was essentially the same as that for the experimental group (“Group D”) in the study by Loy et al. (1993) that showed successful contextdependent aversion for a novel Xuid, except that no distinct scent was presented in the conditioned or the neutral context. Therefore, the successful formation of context discrimination shown in the present experiment seems hard to attribute to simple conditioned aversion to some odor cue (see also the results of Group C in Experiment 2). Thus, it is suggested that a context-dependent aversion was established even when the Xuid given during context discrimination was novel to the animals. Moreover, it seems also reasonable to assume tentatively that a direct association of the conditioned context with nausea underlies the acquired context-dependent aversion, since on the test even the familiar water (i.e., given daily in the home cage of the subjects) was consumed less in the conditioned context than in the neutral context (see the general discussion later).
Experiment 2 The aim of Experiment 2 was to directly investigate the eVect of the familiarity of the Xuid presented during conditioning on the establishment of the context-dependent aversion. Thus either water (familiar Xuid) or saccharin solution (novel Xuid) was presented during discrimination training for the corresponding two groups
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(Group W and Group S). A control group (Group C) that was not given Xuid during discrimination was also included, to examine the possibility that in Experiment 1 discrimination was formed on some uncontrollable cue such as undetectable odor in the context: If such a cue associates with nausea, apparent context discrimination would be formed also in Group C. In addition, two non-conditioning sessions were included in each cycle of the context discrimination training, to examine the possibility that the failure in the study by Boakes et al. (1997) to show successful context dependency to the novel Xuid was caused by their procedure in which they gave two non-conditioning sessions in each cycle. All the subjects were given a third Xuid (0.6% NaCl solution), both in the two contexts during drinking training sessions and as a daily Xuid supplement in their home cage. The eVect of the presentations of NaCl solution in the home cage could be estimated by testing the amount of consumption in Group S and comparing it indirectly with the results of Experiment 1, in which subjects were given water in the home cage. Method Subjects The subjects were 24 male rats of the Wistar strain, about 70 days of age with a mean weight of 260 g (range: 232–280 g) at the beginning of the experiment. Fluids and contexts The Xuids given in discrimination training were 0.05% saccharin and tap water. The US was the same dose of LiCl as used in Experiment 1. The two contexts, one conditioned and the other neutral, were also the same as those used in Experiment 1. Procedure The procedure of Experiment 2 was essentially the same as that of Experiment 1, except for the following. Animals were presented 0.6% NaCl solution instead of water in: (1) the 3-day Xuid restriction period before the start of the experiment, (2) the 4-day Xuid drinking training sessions in each context, and (3) the daily 10 min presentations of Xuid in the home cage, which started at 16:00, during both context discrimination and the test period. Subjects were divided into three groups, S, W, and C (Ns D 8), based on the body weight and the amount of consumption of Xuid on the last day of drinking training sessions in the two contexts. As in Experiment 1, the context discrimination training period consisted of three cycles, each containing four daily sessions. However, since the experiment included Group W in which water was used as the target Xuid, two non-conditioning sessions were conducted on the third and fourth days in each cycle, to match the procedure in the Wrst experiment by Boakes et al. (1997). During discrimination training, subjects in Group S were given 0.05% saccharin solution, while animals in Group W received presentation of tap water. Subjects in Group C were not allowed to consume any Xuid during discrimination but were simply placed in each context.
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During the Wrst session of the test phase that followed the context discrimination phase, half of the subjects in Group S were given water in the conditioned context. Then they were given water in the neutral context during the second session and given saccharin solution on the third (in conditioned context) and fourth (in neutral) sessions. The remaining half of the animals received a test with water in the neutral context on the Wrst session and in the conditioned context on the second session. Tests with saccharin followed these two sessions, Wrst in the neutral and then in the conditioned context. Subjects in Group W were tested Wrst with the saccharin solution and then with water, with the order of the context counterbalanced across the animals. For Group C, both the Xuid and the context presented in each test session were counterbalanced across subjects. Results and discussion The mean amount of consumption of NaCl solution on the last Xuid drinking training session, which began at 12:00, was 12.43 ml in Group S, and 12.83 ml in Group W. These scores did not diVer from each other (t (14) < 1) but were signiWcantly larger than the mean amount of Xuid consumed on the Wrst conditioning session (8.93 ml in Group S; 7.20 ml in Group W), indicating that 0.6% NaCl solution was preferred to both the saccharin solution and tap water (see, e.g., Rowland & Fregly, 1988). Fig. 3 depicts the mean amount of consumption of Xuid during the context discrimination phase. During both the Wrst and the second cycle, the amount of consumption in the conditioning session was more than that in the two non-conditioning sessions and Group S drank less than Group W in non-conditioning sessions. During the third cycle, on the other hand, group diVerences disappeared, and the amount of
Fig. 3. Experiment 2: mean Xuid consumption during three cycles of the discrimination stage. Each cycle consisted of a conditioning session (C) and two extinction sessions (E) given in each of the two contexts, respectively.
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consumption in the conditioning session was less than that in either of the two subsequent non-conditioning sessions in both groups. Statistical analyses supported these Wndings. A three-way ANOVA with group (2), cycle (3), and session in each cycle (3) as factors was conducted on the scores shown in Fig. 3. It showed a signiWcant main eVect of cycle (F (2, 28) D 21.47). In addition, interactions between cycle and session (F (4, 56) D 22.84) and between group and session (F (2, 28) D 6.38) were also signiWcant, whereas the main eVect of groups was not signiWcant. Analyses of simple main eVect of session revealed that in the Wrst cycle the amount of consumption of Xuid was more in the conditioning session (C1) than in either of the two non-conditioning sessions (E1, E2). In the second cycle, it was more in the conditioning session (C2) than in the Wrst non-conditioning session (E3). In the third cycle, on the other hand, the amount of consumption was less in the conditioning session (C3) than in the second non-conditioning session (E6). The simple main eVect of cycle was signiWcant only in the conditioning session: The amount of consumption in the third cycle was less than that in either the Wrst or the second cycle. On the other hand, this eVect was not found in either of the two non-conditioning sessions. These analyses indicated that the suppression of consumption of Xuid in the conditioned context was the cause of the successful context discrimination which was formed during the third cycle. In both of the two non-conditioning sessions, amount of consumption of Xuid was less in Group S than in Group W. This result suggests that the rate of acquisition of simple aversion to saccharin was more than that to water. Fig. 4 shows the mean amount of consumption of saccharin (A) and water (panel B) during the test sessions. Group C revealed little diVerence between the conditioned and neutral context. For Group S and Group W, on the other hand, the amount of consumption of saccharin and of water in the conditioned context was less than in
Fig. 4. Experiment 2: (A) indicates mean consumption of saccharin whereas (B) shows that of water in each of the two contexts on the test.
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the neutral context. That simple paired presentations of the conditioned context and LiCl, alternately with the presentations of neutral context alone did not cause any context-dependent aversion to the Xuid eliminated the possibility that the successful discrimination shown in Group S and Group W was a consequence of association of some uncontrollable cue with nausea. Consumption of water in the conditioned context was less in Group W than in Group S. On the other hand, these two groups showed little diVerence in their amount of consumption of saccharin solution in the conditioned context. In addition, consumption of saccharin in the neutral context was slightly less in Group S than in Group W. These Wndings were substantiated by statistical analyses. For test with the saccharin solution, a two-way ANOVA showed the signiWcant main eVect of group (F (2, 21) D 42.00) and context (F (1, 21) D 96.96), as well as a signiWcant interaction of these factors (F (2, 21) D 20.80). Subsequent multiple comparisons using the LSD method showed that for both Group S and Group W, the amount of consumption in the conditioned context was less than that in the neutral context. However, no diVerence was found in Group C. Amount of consumption in the conditioned context did not diVer between Group S and Group W, and both of the two groups consumed less than Group C. In the neutral context, the amount of consumption was less in Group S than in both Group W and Group C, which did not diVer from each other. For the test with water, an ANOVA revealed signiWcant main eVects of group (F (2, 21) D 23.68) and of context (F (1, 21) D 37.89), and their interaction was also signiWcant. Subsequent multiple comparisons showed that for both Group S and Group W, the amount of consumption in the conditioned context was less than that in the neutral context. No diVerence between the two contexts was found in Group C. In the conditioned context, the amount of consumption was less in Group W than in either Group S or Group C, and it was less in Group S than in Group C. In the neutral context, on the other hand, the amount of consumption did not diVer among groups. These Wndings suggest that the familiarity of the Xuid given during context discrimination training essentially did not aVect the process of the acquisition of context-dependent aversion. Although the consumption of Xuid during its initial presentations in the neutral context was more suppressed in Group S than in Group W, this diVerence did not aVect the eventual formation of a discrimination. Moreover, acquired context-dependent aversion generalized to the other Xuid, water for Group S and saccharin for Group W, suggesting that in both of them the conditioned context was directly associated with nausea. Together with the formation of successful discrimination shown in Experiment 1, the results of Group S also suggested that when a novel Xavor was presented as the target, whether or not the test Xuid (water) was given in the home cage during discrimination did not aVect the results. In addition, it was established irrespective of whether the number of the non-conditioning sessions given in each cycle was one or two. The Wnding that Group C did not show successful context discrimination indicates not only that the presentation of some Xuid was necessary for the establishment of an
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apparent context-dependent aversion, but also that the successful context-dependent aversions shown in Experiment 1 and Experiment 2 were not a consequence of the association of some uncontrollable cue with nausea.
Experiment 3 The results obtained from the previous two experiments seem to suggest that a direct association of the context with nausea underlies the formation of contextdependent aversion, irrespective of whether the Xuid given during discrimination training was novel or familiar. Experiment 3 aimed to investigate the eVects of the Xuid given in the home cage during the context discrimination phase and the eVects of the Xuid presented in the two contexts during the drinking training phase. For all of the following three groups of subjects, water was the target Xuid given in context discrimination. Subjects in Group WW were given water both in the two contexts during the drinking training phase and in their home cages during the context discrimination phase. Animals in Group WN were presented water in the two contexts during the drinking training sessions but were given 0.6% NaCl solution in their home cages during the context discrimination phase. Subjects in Group NN received NaCl solution during both of the two phases. Thus the procedure given to this group was identical to that to Group W in Experiment 2. If consumption of the same Xuid in both contexts and in the home cage during context discrimination is necessary for the formation of a context dependency that is speciWc to that Xuid, only Group WW would show it. If, on the other hand, preexposure to the Xuid during the drinking training phase causes the formation of the Xuid-speciWc context dependency, it should be evident in both Group WW and Group WN. Method Subjects The subjects were 24 male rats of the Wistar strain, about 70 days of age at the start of the experiment, with a mean weight of 255 g (range: 224–278 g). Fluids and contexts Tap water was used as the Xuid presented during discrimination training, and 0.6% NaCl solution was assigned as the Xuid given to some groups of animals as described below. In addition, a 0.05% saccharin solution was used as the test Xuid. The US was a 0.15 M, 10 ml/kg injection of LiCl. The two contexts presented during context discrimination were identical to those used in the previous experiments. Procedure The procedure of the experiment mirrored that of Experiment 2, except for the Xuid presented to the subjects. After a 3-day Xuid restriction period in which all the subjects were given 0.05% saccharin solution for 10 min both at 12:00 and at 16:00 in
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their home cages, they were divided into three groups (WW, WN, and NN, Ns D 8). During the 6-day drinking training sessions, subjects in Group WW, and Group WN were given water, whereas animals in Group NN were presented NaCl solution in both of the two contexts (note that they were not given any Xuid in the home cage during this phase). Through the context discrimination phase, animals in Group WW were given tap water while subjects in Group NN and Group WN were presented NaCl solution in their home cages. After three cycles of discrimination training, all the animals were tested with both the saccharin solution and water in the same manner as that for Group W in Experiment 2. Results and discussion Fig. 5 depicts the mean amount of consumption of water during context discrimination sessions. On the Wrst non-conditioning session of the Wrst cycle, there was less consumption in Group NN than in either Group WW or Group WN. Group WW and Group WN showed about the same amount of consumption throughout the Wrst cycle. During the second cycle, the amount of consumption on both of the non-conditioning sessions appeared more in Group WW than in either Group NN or Group WN. In both Group NN and Group WN, the amount of consumption on the conditioning session of the third cycle was less than that in either of the following two nonconditioning sessions. In Group WW, on the other hand, the amount of consumption did not vary among the sessions. A three-way ANOVA conducted on the scores from Figure 5 showed signiWcant main eVects of group (F (2, 21) D 13.77), cycle (F (2, 42) D 5.32), and session (F (2, 42) D 5.26); interaction between group and session (F (4, 42) D 5.85) and that between cycle and session (F (8, 84) D 2.45) were also signiWcant. In addition, interaction among the three factors (F (8, 84) D 2.45) was also signiWcant. Therefore, only
Fig. 5. Experiment 3: mean water consumption during three cycles of the discrimination stage. Each cycle consisted of a conditioning session (C) and two extinction sessions (E) given in each of the two contexts, respectively.
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signiWcant diVerences that were shown in the subsequent analyses by the LSD method and that are relevant to the discussion are described below. As for the group diVerences, it was revealed that on both of the conditioning and the Wrst non-conditioning sessions during the Wrst cycle, the amount of consumption of Xuid was less in Group NN than in either Group WN or WW, though WN and WW did not diVer from each other. This Wnding suggests that presentations of NaCl during drinking training sessions reduced the palatability of water. During the third cycle, however, more water was drunk by Group WW than by either Group NN or Group WN; though NN and WN did not diVer from each other. On the other hand, the amount of consumption on the second non-conditioning session did not diVer among the groups in either the Wrst or the third cycle. In all three groups, the amount of consumption of water on the conditioning session was less in the third cycle than in the second cycle. In both Group WN and Group NN, more was drunk in the conditioning session than in the following two non-conditioning sessions in the second cycle; in the third cycle less was drunk in the conditioning session than in the two non-conditioning sessions. In Group WW, on the other hand, the amount of consumption did not diVer among the three sessions through the three cycles. These Wndings indicate that during the third cycle of context discrimination training, the context-dependent aversion to water was apparent in Group WN and Group NN but not in Group WW. Fig. 6 shows the mean amount of consumption of water (panel A) and saccharin solution (panel B) during the test sessions. All three groups showed context dependency of aversion in the test with water: The amount of consumption was less in the conditioned context than in the neutral context. Group WW did not show evidence
Fig. 6. Experiment 3: (A) indicates mean consumption of water whereas (B) shows that of saccharin in each of the two contexts on the test.
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of context-dependent aversion during the discrimination training phase but revealed clear discrimination in the test. As a similar Wnding was reported by Boakes et al. (1997, Experiment 3), this would imply that it was during the third cycle of discrimination training that the context-dependent aversion developed and was apparent at the test. Amount of consumption of saccharin solution was less in the conditioned context than in the neutral context, for both Group NN and Group WN. On the other hand, it did not diVer between the two contexts in Group WW. A two-way ANOVA conducted on the test scores with water revealed that only the main eVect of context was signiWcant (F (1, 21) D 60.87). The same ANOVA conducted on the test to saccharin, on the other hand, showed that the main eVects of group (F (2, 21) D 20.77) and context (F (1, 21) D 33.26) and the interaction of these two factors (F (2, 21) D 9.46) were signiWcant. Post hoc comparisons showed that for both Group NN and Group WN the amount of consumption in the conditioned context was less than that in the neutral context. In contrast, the amount of consumption in Group WW did not diVer between the two contexts. In the conditioned context, the amount of consumption was more in Group WW than in either Group NN or Group WN, whereas no group diVerences were found in the neutral context. These Wndings suggest that in Experiment 3 the supplement of water in the home cage during context discrimination was responsible for the Xuid-speciWc context dependency of aversion. It is possible that this context dependency was a consequence of the summation of the two eVects, preexposure to water and a supplement of it in the home cage during discrimination training. However, it would be more reasonable to suppose that consumption of water in the home cage during context discrimination was, at the very least, the main cause of the Xuid-speciWc context dependency of aversion shown in the test, since Group WN failed to show the Xuid-speciWc aversion.
General discussion The Wndings obtained in the present three experiments demonstrate that contextdependent aversion can be established to both a novel Xuid (saccharin solution) and familiar water. Moreover, the established context dependency was not speciWc to the initial Xuid; it was revealed also when a second Xuid was given at the test, and the Xuid supplied in the home cages of the subjects diVered from that presented in context discrimination training. Fluid-speciWc context dependency was shown only when the same Xuid was given both in the two contexts and in the home cages of the subjects during the context discrimination. In addition, the context dependency established to saccharin was also revealed to water presented in the test, suggesting that whether the Xuid given in the home cage was the same as (Experiment 1) or diVerent from (Experiment 2) the test Xuid did not aVect the results of the test. Therefore, it is hard to attribute these results to the enhancement of a neophobic response in the conditioned context, when considering the familiarity of water for these subjects, especially that in Experiment 1.
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More importantly, the results of Experiment 2 clearly demonstrated that novelty of the Xuid had little eVect on the process of establishment of context-dependent aversion: Not only Group S that received novel saccharin during context discrimination but also Group W that was given water established context-dependent aversion and transferred it to another Xuid. These Wndings contradict the prediction that novelty of the Xuid given during context discrimination training determines whether or not the established context-dependent aversion is speciWc to it. Rather, the Wndings obtained from the present Experiments 1 and 2 agree with the simple assumption that both the Xuid, even water (e.g., Revusky & Parker, 1976), and the context associated directly with nausea during context discrimination training, and the Xuid-nausea association generalized to the second Xuid presented in the test. In Experiment 3, two groups (NN and WN) of rats that were given water in context discrimination training while they were supplied NaCl solution in the home cage showed the acquired context-dependent aversion to a second Xuid (saccharin solution). On the other hand, Group WW, to which water was given both in the two contexts and in the home cage, failed to show context-dependent aversion to the second Xuid. These Wndings seem to indicate that the context acquired an occasion setting property rather than a direct association with nausea only in Group WW (e.g., Puente et al., 1988; Boakes et al., 1997; but see also, e.g., Symonds et al., 1998). However, these Wndings could also be explained in terms of simple summation and generalization decrement. For the subjects in Group WW, presenting water in the home cage could be regarded as additional extinction trials. Consequently, the association of water with nausea would develop slower in this group than in the other two groups (Group NN and Group WN) that did not receive water in their home cages. In addition, the development of a context-nausea association would also be retarded in Group WW, if the water-context association potentiated it. The failure to show an indication of the acquisition of an aversion in this group during context discrimination training, shown in Fig. 5, supports this explanation. The results of the test shown in Group WW could be explained by assuming that aversive behavior was apparent only when the two events (water and contextual cues), each of which had not acquired substantial association with nausea, were presented together. Conversely, presentation the second Xuid would not be enough to result in apparent aversive behavior in the conditioned context because of the generalization decrement of the association acquired to water. On the other hand, the subjects in both Group NN and Group WN acquired a relatively more substantial association to water and to the conditioned context, since no additional water was given in the home cage. Then, the aversion to a second Xuid should be more evident in the conditioned context, which had been strongly associated with nausea. It might still be possible to assume that in Group WW the context acquired the property of an occasion setter. However, such an explanation does not explain why presenting the same Xuid in the home cage during context discrimination resulted in the acquisition of the occasion setting property by the context. For example, it has been shown that the property of occasion setting is acquired by a stimulus or context
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that has relatively lower salience than that of the conditioned stimulus (e.g., Holland, 1989; Holland & Hass, 1993). But, there seems little reason to assume that the context was less salient in Group WW than in Group NN or Group WN. Rather, the additional presentations of water in the home cage should reduce its salience (e.g., Wagner, 1981) and thus increase the relative salience of the context in Group WW. Another possible interpretation is that in all of the present experiments the context acquired the property of occasion setter and the Wndings simply reXect the direct generalization of aversion acquired to the original Xuid presented during context discrimination, an argument derived from the criticism that the Xuid consumption test does not provide unequivocal evidence of context-illness association (e.g., Symonds & Hall, 1997; Lopez & Cantora, 2003). However, the Wnding in Experiment 1 that the context dependency established to novel saccharin generalized to water is hard to explain as the direct generalization of aversion between the two Xuids, since the same water was also given daily and safely in the home cages throughout the experiment (and, in addition, through the life history of the subjects after weaning). Further, water had no chance to be associated with either nausea or the conditioned context (see Bills, Smith, Myers, & Schachtman, 2003). In fact, amount of consumption of water given in the home cage of the subjects on the days following each conditioning (overall mean: 10.7 ml) did not decrease through the experiment, suggesting that little generalization of aversion if any occurred. It would be more reasonable to assume that the apparent aversion to water shown in the test reXected the direct association between the conditioned context and nausea, rather than the direct generalization between the two Xuids. The results of the third experiment by Boakes et al. (1997) that showed the XuidspeciWc context dependency of aversion do not agree with the explanation described above, since the Xuid given in the home cage (water) was not the same as that presented during context discrimination training (sucrose). However, subjects in this experiment were preexposed to sucrose before being given context discrimination training, and two extinction test sessions were replicated for both sucrose and the test Xuid (saline) in each of the two contexts. Then, the averaged test scores might simply reXect a relatively weak association of sucrose with nausea and thus little generalization of it to the saline, and the fact that context-dependent aversion was apparent only to the sucrose would be explainable in terms of the simple summation of aversion acquired to sucrose and that to the contextual cues. For the present, therefore, explanation in terms of a summation eVect of associations acquired to Xuid, and to the contextual cues seems more parsimonious than explanation in terms of acquisition of an occasion setting function to the context, at least when the Xuid given during context discrimination training is not so salient.
References Archer, T., Sjoden, P.-O., & Nilsson, L. G. (1985). Contextual control of taste-aversion conditioning and extinction. In P. D. Balsam & A. Tomie (Eds.), Context and learning (pp. 225–271). Hillsdale, NJ: Erlbaum.
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Best, M. R., Brown, E. R., & Sowell, M. K. (1984). Taste-mediated potentiation of non-ingestional stimuli in the rats. Learning and Motivation, 15, 244–258. Bills, C., Smith, S., Myers, N., & Schachtman, T. R. (2003). EVects of context exposure during conditioning on conditioned taste aversions. Learning and Behavior, 31, 369–377. Boakes, R. F., Westbrook, R. F., & Barnes, B. W. (1992). Potentiation by a taste of toxicosis-based context conditioning: EVects of varying the test Xuid. Quarterly Journal of Experimental Psychology, 45B, 303–325. Boakes, R. A., Westbrook, R. F., Elliott, M., & Swinbourne, A. L. (1997). Context dependency of conditioned aversions to water and sweet tastes. Journal of Experimental Psychology: Animal Behavior Processes, 23, 56–67. Bonradi, C., Honey, R. C., & Hall, G. (1990). Context speciWcity of conditioning in Xavor-aversion learning: Extinction and blocking tests. Animal Learning and Behavior, 18, 229–237. Bouton, M. E., & King, D. A. (1983). Contextual control of the extinction of conditioned fear: Test for the associative value of the context. Journal of Experimental Psychology: Animal Behavior Processes, 12, 4–15. Bouton, M. E., & Swartzentruber, D. (1986). Analysis of the associative and occasion-setting properties of contexts participating in a Pavlovian discrimination. Journal of Experimental Psychology: Animal Behavior Processes, 12, 333–350. Durlach, P. D., & Rescorla, R. A. (1980). Potentiation rather than overshadowing in Xavor aversion learning: An analysis in terms of within-compound associations. Journal of Experimental Psychology: Animal Behavior Processes, 6, 175–187. Hall, G., & Honey, R. C. (1990). Context-speciWc conditioning in the conditioned-emotional–response procedure. Journal of Experimental Psychology: Animal Behavior Processes, 16, 271–278. Holder, M. D. (1988). Possible role of confounded taste stimuli in conditioned taste aversions. Animal Learning and Behavior, 16, 231–234. Holland, P. C. (1983). Occasion-setting in Pavlovian feature positive discrimination. In M. L. Commonds, R. J. Herrnstein, & A. R. Wagner (Eds.), Quantitative analyses of behavior: Discrimination processes (Vol. 4, pp. 183–206). New York: Ballinger. Holland, P. C. (1989). Occasion setting with simultaneous compounds in rats. Journal of Experimental Psychology: Animal Behavior Processes, 15, 183–193. Holland, P. C., & Hass, M. L. (1993). The eVects of target salience in operant feature positive discriminations. Learning and Motivation, 24, 119–140. Lopez, M., & Cantora, R. (2003). Associative interference with taste aversions after contextual discrimination learning. Learning and Motivation, 34, 372–388. Loy, I., Alvarez, R., Rey, V., & Lopez, M. (1993). Context-US associations rather than occasion-setting in taste aversion learning. Learning and Motivation, 24, 55–72. Lubow, R. E. (1973). Latent inhibition. Psychological Bulletin, 79, 398–407. Lubow, R. E. (1989). Latent inhibition and conditioned attention theory. Cambridge: Cambridge University Press. Mitchell, C., & Heyes, C. (1996). Simultaneous overshadowing and potentiation of taste and contextual cues by a second taste in toxicosis conditioning. Learning and Motivation, 27, 58–72. Puente, G. P., Cannon, D. S., Best, M. R., & Carrell, L. E. (1988). Occasion setting of Xuid ingestion by contextual cues. Learning and Motivation, 19, 239–253. Revusky, S., & Parker, L. A. (1976). Aversions to unXavored water and cup drinking produced by delayed sickness. Journal of Experimental Psychology: Animal Behavior Processes, 4, 342–353. Rowland, N. E., & Fregly, M. J. (1988). Sodium appetite: Species and strain diVerences and role of reninangiotensin-aldosterone system. Appetite, 11, 143–178. Symonds, M., & Hall, G. (1997). Contextual conditioning with lithium-induced nausea as the US: Evidence from a blocking procedure. Learning and Motivation, 28, 200–215. Symonds, M., & Hall, G. (1999). Overshadowing not potentiation of illness-based contextual conditioning by a novel taste. Animal Learning and Behavior, 27, 379–390. Symonds, M., Hall, G., Lopez, M., Loy, I., Ramos, A., & Rodriguez, M. (1998). Is Xuid consumption necessary for the formation of context-illness associations. An evaluation using consumption and blocking tests. Learning and Motivation, 29, 168–183. Wagner, A. R. (1981). SOP: A model for automatic memory processing in animal behavior. In N. E. Spear & R. R. Miller (Eds.), Information processing in animals: Memory mechanisms (pp. 5–47). Hillsdale, NJ: Erlbaum.
Context dependency of conditioned aversions to familiar and novel Xuids 夽 Kiyoshi Ishii a,¤, Yoshio Iguchi a, Kosuke Sawa b b
a Department of Psychology, Nagoya University, Japan Japan Society for Promotion of Science, Nagoya University, Japan
Received 25 November 2004; received in revised form 11 April 2005 Available online 19 July 2005
Abstract Using a context discrimination procedure and rats as the subjects, the formation of contextdependent aversions to novel and familiar Xuids was investigated. Experiment 1 revealed that context dependency could be established to a novel Xuid (saccharin) after three cycles of context discrimination training and that the acquired context dependency was revealed also to a second familiar Xuid (water) presented in the following test. Experiment 2 showed that the formation of the context-dependent aversion and its transfer to a second Xuid was not aVected by whether Xuid presented during discrimination was novel (saccharin) or familiar (water). Experiment 3 demonstrated that when the same water was given both in the two training contexts and in the home cages of the subjects during discrimination, the context-dependent aversion formed was speciWc to it. These Wndings can be explained in terms of a simple summation eVect of Xuid-nausea and context-nausea associations. © 2005 Elsevier Inc. All rights reserved. Keywords: Context dependency; Conditioned aversion; Occasion setting; Rat
夽 This research was supported by Grant-in-Aid for ScientiWc Research, 15530469, from Japanese Ministry of Education, Culture, Sports and Technology to the Wrst author. * Corresponding author. Fax: +81 52 789 2223. E-mail address: [email protected] (K. Ishii).
0023-9690/$ - see front matter © 2005 Elsevier Inc. All rights reserved. doi:10.1016/j.lmot.2005.04.002
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It is now widely acknowledged that responses acquired through a Pavlovian conditioning procedure can become context-dependent (e.g., Bouton & King, 1983; Bouton & Swartzentruber, 1986; Hall & Honey, 1990). This is also true for a response established in the conditioned taste aversion paradigm. For example, the aversive response acquired to a taste attenuates when tested in a context diVerent from the one in which it was conditioned (Bonradi, Honey, & Hall, 1990). Furthermore, after the conditioned taste aversion has been extinguished in a diVerent context, it is renewed when the subject is returned to the original conditioning context (e.g., Archer, Sjoden, & Nilsson, 1985; Holder, 1988). The context dependency of conditioned aversion is also demonstrated in the procedure of context discrimination training. In this paradigm, subjects are repeatedly given paired presentations of a Xuid and nausea-inducing substance (usually lithium chloride: LiCl) in one “conditioned” context, while presented the same Xuid alone in another “neutral” context. After receiving several cycles of such context discrimination training, subjects come to avoid consuming the Xuid more in the former context than in the latter. In most of the studies that showed successful formation of context-dependent aversion (e.g., Boakes, Westbrook, & Barnes, 1992; Boakes, Westbrook, Elliott, & Swinbourne, 1997; Puente, Cannon, Best, & Carrell, 1988), the acquired context dependency was speciWc to the Xuid given during context discrimination training. In the following test, the amount of consumption of a second Xuid that had not been paired with LiCl did not diVer between the two contexts. This fact seems to suggest that the contextual cues did not directly become associated with nausea but rather acquired the property of an “occasion-setter” (Holland, 1983) or a discriminative cue that determines the meaning of the Xuid presented in it. Boakes et al. (1997) found that the Xuid-speciWc context dependency of aversion was established only when the Xuid was preexposed or familiar to the animals. When a novel Xuid was given, on the other hand, subjects revealed no evidence of context discrimination. Thus, they argued that a latent inhibition eVect (Lubow, 1973, 1989) is responsible for the successful formation of context-dependent aversion: When a preexposed Xuid is given, animals still consume a substantial amount of it safely in the neutral context, even after they received the initial paired presentations of the Xuid and LiCl in the conditioned context. When the Xuid is novel, on the other hand, animals come to consume little amount of it in the neutral context due to rapid acquisition of aversion to that Xuid, and thus the discrimination between the two contexts is hard to establish. In other words, Boakes et al. (1997) assumed that only the Xuid become associated with nausea, with the rate of development of this association determining whether or not the context can acquire the function of an occasion setter. However, it should be possible to establish a context-dependent aversion to even a novel Xuid, if the rate of development of its association with nausea is the crucial condition for it. The associability of a stimulus is reduced not only by its preexposure but also by decreasing its salience (here it means physical intensity). When a novel but not so salient Xuid is presented during discrimination training, then, it might be expected that subjects would continue consuming some amount of it in the neutral context, and thus eventually show context-dependent aversion.
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In fact, Loy, Alvarez, Rey, and Lopez (1993) demonstrated that context-dependent aversion could be established to novel sucrose. However, they also found that the established context-dependent aversion was revealed to a second Xuid (coVee) presented in the following test. This Wnding seems to suggest that the context did not acquire the property of an occasion-setter but rather become associated directly with nausea. When considering the nature of the Xuid given in the experiments by Loy et al. (1993), it seems that whether the Xuid given during context discrimination is novel or familiar determines the Xuid-speciWcity of the acquired context dependency. As Boakes et al. (1997) pointed out, however, the methods of the experiments that showed the Xuid-speciWc context dependency of aversion diVered also in some other aspects from that used by Loy et al. (1993). Among these diVerences was the Xuid that was supplied daily in the home cages of the subjects during discrimination training. In most of the studies that showed Xuid-speciWc context dependency of aversion, the Xuid was the same as that presented during context discrimination (e.g., water or saline in Puente et al., 1988, Experiment 2; saccharin in Boakes et al., 1997, Experiment 2; but see also the Wndings in Experiment 3 by Boakes et al., 1997, which are discussed later). In the experiments by Loy et al., on the other hand, animals were given water in their home cage. It is known that acquisition of aversion to a context is apparently “potentiated” (e.g., Durlach & Rescorla, 1980, but see also, e.g., Symonds & Hall, 1999) when subjects receive a Xuid with a novel taste, or even water, during conditioning (e.g., Best, Brown, & Sowell, 1984; Boakes et al., 1992; Mitchell & Heyes, 1996). However, daily consumption of the same Xuid safely in the home cage during context discrimination might function as additional extinction trials and thus retard the acquisition of aversion to that Xuid. Then the ability of the Xuid to potentiate the context-nausea association would also be reduced, if the potentiation is interspersed with within-compound (i.e., Xuid-context) association (see e.g., Durlach & Rescorla, 1980, Experiment 4). Consequently, apparent discrimination might be revealed only when both contextual cues and Xuid, each of which acquires only a weak association with nausea, are presented simultaneously. The implication is that the Xuid-speciWc context dependency of aversion found in most of the previous studies can be explained in terms of a simple summation of the associative strength acquired by each of these two events, if some threshold is assumed for the aversive behavior to be apparent. The aim of the present study was to investigate the process of the formation of context-dependent aversion to both novel and familiar Xuids, and to compare the properties acquired by the context. If successful formation of context-dependent aversion depends solely on the subjects’ experience of consuming some amount of the Xuid in the neutral context during discrimination training, it should be possible to condition to even a novel Xuid, if it is not too salient. Novelty of the Xuid might determine whether or not the acquired context dependency is speciWc to the Xuid given during context discrimination. Furthermore, Xuid-speciWc context dependency of aversion might also be evident when, the Xuid presented in both of the two contexts is also given in the subjects home cage during discrimination training. These predictions were examined in three experiments.
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The conventional single-bottle test was adopted in the present experiments, to compare the Wndings with those in the many previous studies that have also used this method.
Experiment 1 Experiment 1 examined whether context-dependent aversion can be established by presenting novel Xuid (0.05% saccharin solution) during discrimination training. Our preliminary investigations showed that in the paradigm of simple conditioned aversion, the rate of acquisition to 0.05% saccharin solution was signiWcantly less than that to 0.1% solution, the concentration that has been used most frequently as the CS in previous studies. It was then tested whether consumption of a second Xuid was also suppressed in the conditioned context. Following the design of Loy et al. (1993), animals were additionally given water daily in their home cage throughout the experiment, but no scent was presented in either the conditioned or neutral context. In addition, tap water was also presented as the second Xuid of the test. Loy et al. used coVee solution that was only preexposed for two days as the test Xuid. To evaluate the degree of aversion acquired by the context itself, however, it would be more reasonable to test with a quite familiar Xuid that evokes no neophobic response. Method Subjects The subjects were 16 male rats of the Wistar strain, about 70–75 days of age at the beginning of the experiment, with a mean free-feeding weight of 252 g (range: 232– 276 g). They were born and reared in the colony room of the Department of Psychology, Nagoya University. Each subject was housed individually in its home cage (31 £ 36 £ 18 cm, with the Xoor covered with wooden chips and a stainless-steel grid roof), which was placed in the colony room that was illuminated on a 12 h light /12 h dark daily cycle. Rats had free access to food. The temperature and humidity of the colony room were maintained at 24 °C and 50%, respectively. Fluids and contexts A 0.05% saccharin solution was presented during context discrimination training. The unconditioned stimulus (US) was an intraperitoneal injection of 0.15 M lithium chloride (LiCl) at 10 ml/kg of body weight. Two kinds of cages and rooms that diVered from each other in the aspects described below were used as the two contexts. Context A consisted of 16 transparent acrylic cages (27 £ 43 £ 20 cm) with a stainless-steel grid roof, placed in an experimental room outside the animal laboratory with dim (0.5 lx) illumination and constant noise (76 dB) produced by a sound stimulator with a loudspeaker. The Xoor of each cage was covered with wooden chips. A stainless-steel spout connected to a graduated cylinder could be inserted in the center of the roof. Context B consisted of 16 opaque polycarbonate cages (31 £ 36 £ 18 cm) with a plain wooden board roof, placed in an experimental room with relatively bright illumination (54 lx). The Xoor of each cage was covered with gravel made by paper, and the same spout as
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used in context A could be inserted into the center of one end wall. The temperature and humidity were kept at 24 °C and 50%, respectively, in both of the two contexts. Procedure For three days before the start of experiment, subjects were on a restricted access to water schedule. They could consume tap water only during two daily sessions of 20 min, initiated at 12:00 and 16:00 in their home cages. Water drinking in the two contexts began the following day, to allow animals to consume saccharin solution in each context from the beginning of context discrimination training. On the Wrst day, animals were placed in Context A at 12:00. Ten minutes later, they were allowed access to water for 10 min. Then they were returned to their home cages. At 16:00 on the same day, subjects were placed in Context B and received the same procedure as given in Context A. On the second day, animals were placed in Context B at 12:00 and in Context A at 16:00. The procedure given in each context was exactly the same as that on the Wrst day. This procedure schedule was performed twice (from Day 1 to Day 4). Context discrimination training (Day 5–16) consisted of three cycles, each containing four daily sessions that began at 12:00. On the Wrst session in each cycle, animals were divided into two subgroups, matched by body weight and the amount of water consumed on Day 4, and placed for 10min in either Context A or Context B. They were then given saccharin solution for 10min. Upon removal of the spout, animals were immediately injected with LiCl. They were then placed back in their home cages. On the second and the fourth days of each cycle, subjects were presented water for 10min in their home cages. A non-conditioning session in the neutral context was given on the third day of each cycle: animals were placed for 10min either in Context B or in Context A. They then had access to the saccharin solution for 10min, without subsequent injection of LiCl. Four test sessions followed the context discrimination training. On the Wrst session (Day 17), half of the subjects in each group were placed in the conditioned context for 10 min, and then were presented water for another 10 min. On the next day (Day 18), they were placed again in the conditioned context but were given saccharin solution for 10 min. On Day 19, these subjects were given water for 10 min in the neutral context. Finally, on Day 20, they were presented saccharin solution for 10 min in the neutral context. The remaining half of the subjects Wrst received two test sessions in the neutral context, followed by another two sessions in the conditioned context. Throughout all drinking training, context discrimination and test sessions, the amount of Xuid consumed was measured to the nearest 0.2 ml. In addition to these daily sessions that began at 12:00, animals were also given water for 10 min at 16:00 in their home cage throughout the experiment, except during the training of water drinking. The spout presented was the same as that used in both of Context A and Context B. Results and discussion The overall mean amount of consumption of water on the last Xuid drinking training in each context which began at 12:00 was 9.80 ml and did not diVer signiWcantly
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between the two contexts (t (14) < 1). Also through the rest of the experiment, no signiWcant subgroup diVerences in the amount of consumption of Xuid were seen. Therefore, the scores of the two subgroups were combined, and a signiWcance level of p < .05 was adopted in this and all subsequent analyses. Fig. 1 depicts the mean amount of saccharin solution consumed in three conditioning and three non-conditioning sessions. It shows that while the amount of consumption in both the Wrst and the second non-conditioning sessions is less than that in the previous conditioning session in each cycle of discrimination training, consumption in the last non-conditioning session is more than that in the last conditioning session. These results indicate that after three cycles rats were able to discriminate the conditioned context from the neutral one. A two-way ANOVA with cycle and context as factors was conducted on the scores shown in Fig. 1. It revealed a signiWcant main eVect of cycle (F (2, 30) D 111.66) and an interaction between the two factors (F (2, 30) D 35.64). Subsequent analyses of the interaction showed that the simple main eVect of cycle was signiWcant only in the conditioned context: Amount of consumption decreased gradually as a function of cycles. The simple main eVect of context was found in all three cycles: Both during the Wrst and second cycle, the amount of consumption was more in the conditioned context than in the neutral context. During the third cycle, on the other hand, it was less in the conditioned context than in the neutral context. Fig. 2 shows the mean amount of saccharin solution and water consumed in the test sessions. It is obvious that both consumption of saccharin solution and of water were less in the conditioned context than in the neutral context, suggesting that not only saccharin solution but also water was avoided more in the former. Consumption of water was more than that of saccharin in both conditioned and neutral contexts, indicating less aversion to water than to saccharin despite the fact that the test to the former preceded that to the latter.
Fig. 1. Experiment 1: mean consumption of saccharin solution during three cycles of the discrimination stage. Each cycle consisted of a conditioning session (C) in one context and an extinction session (E) in another context.
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Fig. 2. Experiment 1: mean consumption of saccharin and water in each of the two contexts on the test.
Statistical analyses also supported these observations. A two-way ANOVA revealed that both the main eVect of context (F(1,15)D41.16) and that of test Xuid (F(1,15)D18.66) were signiWcant, but that the interaction of these two factors was not signiWcant. The procedure of Experiment 1 was essentially the same as that for the experimental group (“Group D”) in the study by Loy et al. (1993) that showed successful contextdependent aversion for a novel Xuid, except that no distinct scent was presented in the conditioned or the neutral context. Therefore, the successful formation of context discrimination shown in the present experiment seems hard to attribute to simple conditioned aversion to some odor cue (see also the results of Group C in Experiment 2). Thus, it is suggested that a context-dependent aversion was established even when the Xuid given during context discrimination was novel to the animals. Moreover, it seems also reasonable to assume tentatively that a direct association of the conditioned context with nausea underlies the acquired context-dependent aversion, since on the test even the familiar water (i.e., given daily in the home cage of the subjects) was consumed less in the conditioned context than in the neutral context (see the general discussion later).
Experiment 2 The aim of Experiment 2 was to directly investigate the eVect of the familiarity of the Xuid presented during conditioning on the establishment of the context-dependent aversion. Thus either water (familiar Xuid) or saccharin solution (novel Xuid) was presented during discrimination training for the corresponding two groups
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(Group W and Group S). A control group (Group C) that was not given Xuid during discrimination was also included, to examine the possibility that in Experiment 1 discrimination was formed on some uncontrollable cue such as undetectable odor in the context: If such a cue associates with nausea, apparent context discrimination would be formed also in Group C. In addition, two non-conditioning sessions were included in each cycle of the context discrimination training, to examine the possibility that the failure in the study by Boakes et al. (1997) to show successful context dependency to the novel Xuid was caused by their procedure in which they gave two non-conditioning sessions in each cycle. All the subjects were given a third Xuid (0.6% NaCl solution), both in the two contexts during drinking training sessions and as a daily Xuid supplement in their home cage. The eVect of the presentations of NaCl solution in the home cage could be estimated by testing the amount of consumption in Group S and comparing it indirectly with the results of Experiment 1, in which subjects were given water in the home cage. Method Subjects The subjects were 24 male rats of the Wistar strain, about 70 days of age with a mean weight of 260 g (range: 232–280 g) at the beginning of the experiment. Fluids and contexts The Xuids given in discrimination training were 0.05% saccharin and tap water. The US was the same dose of LiCl as used in Experiment 1. The two contexts, one conditioned and the other neutral, were also the same as those used in Experiment 1. Procedure The procedure of Experiment 2 was essentially the same as that of Experiment 1, except for the following. Animals were presented 0.6% NaCl solution instead of water in: (1) the 3-day Xuid restriction period before the start of the experiment, (2) the 4-day Xuid drinking training sessions in each context, and (3) the daily 10 min presentations of Xuid in the home cage, which started at 16:00, during both context discrimination and the test period. Subjects were divided into three groups, S, W, and C (Ns D 8), based on the body weight and the amount of consumption of Xuid on the last day of drinking training sessions in the two contexts. As in Experiment 1, the context discrimination training period consisted of three cycles, each containing four daily sessions. However, since the experiment included Group W in which water was used as the target Xuid, two non-conditioning sessions were conducted on the third and fourth days in each cycle, to match the procedure in the Wrst experiment by Boakes et al. (1997). During discrimination training, subjects in Group S were given 0.05% saccharin solution, while animals in Group W received presentation of tap water. Subjects in Group C were not allowed to consume any Xuid during discrimination but were simply placed in each context.
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During the Wrst session of the test phase that followed the context discrimination phase, half of the subjects in Group S were given water in the conditioned context. Then they were given water in the neutral context during the second session and given saccharin solution on the third (in conditioned context) and fourth (in neutral) sessions. The remaining half of the animals received a test with water in the neutral context on the Wrst session and in the conditioned context on the second session. Tests with saccharin followed these two sessions, Wrst in the neutral and then in the conditioned context. Subjects in Group W were tested Wrst with the saccharin solution and then with water, with the order of the context counterbalanced across the animals. For Group C, both the Xuid and the context presented in each test session were counterbalanced across subjects. Results and discussion The mean amount of consumption of NaCl solution on the last Xuid drinking training session, which began at 12:00, was 12.43 ml in Group S, and 12.83 ml in Group W. These scores did not diVer from each other (t (14) < 1) but were signiWcantly larger than the mean amount of Xuid consumed on the Wrst conditioning session (8.93 ml in Group S; 7.20 ml in Group W), indicating that 0.6% NaCl solution was preferred to both the saccharin solution and tap water (see, e.g., Rowland & Fregly, 1988). Fig. 3 depicts the mean amount of consumption of Xuid during the context discrimination phase. During both the Wrst and the second cycle, the amount of consumption in the conditioning session was more than that in the two non-conditioning sessions and Group S drank less than Group W in non-conditioning sessions. During the third cycle, on the other hand, group diVerences disappeared, and the amount of
Fig. 3. Experiment 2: mean Xuid consumption during three cycles of the discrimination stage. Each cycle consisted of a conditioning session (C) and two extinction sessions (E) given in each of the two contexts, respectively.
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consumption in the conditioning session was less than that in either of the two subsequent non-conditioning sessions in both groups. Statistical analyses supported these Wndings. A three-way ANOVA with group (2), cycle (3), and session in each cycle (3) as factors was conducted on the scores shown in Fig. 3. It showed a signiWcant main eVect of cycle (F (2, 28) D 21.47). In addition, interactions between cycle and session (F (4, 56) D 22.84) and between group and session (F (2, 28) D 6.38) were also signiWcant, whereas the main eVect of groups was not signiWcant. Analyses of simple main eVect of session revealed that in the Wrst cycle the amount of consumption of Xuid was more in the conditioning session (C1) than in either of the two non-conditioning sessions (E1, E2). In the second cycle, it was more in the conditioning session (C2) than in the Wrst non-conditioning session (E3). In the third cycle, on the other hand, the amount of consumption was less in the conditioning session (C3) than in the second non-conditioning session (E6). The simple main eVect of cycle was signiWcant only in the conditioning session: The amount of consumption in the third cycle was less than that in either the Wrst or the second cycle. On the other hand, this eVect was not found in either of the two non-conditioning sessions. These analyses indicated that the suppression of consumption of Xuid in the conditioned context was the cause of the successful context discrimination which was formed during the third cycle. In both of the two non-conditioning sessions, amount of consumption of Xuid was less in Group S than in Group W. This result suggests that the rate of acquisition of simple aversion to saccharin was more than that to water. Fig. 4 shows the mean amount of consumption of saccharin (A) and water (panel B) during the test sessions. Group C revealed little diVerence between the conditioned and neutral context. For Group S and Group W, on the other hand, the amount of consumption of saccharin and of water in the conditioned context was less than in
Fig. 4. Experiment 2: (A) indicates mean consumption of saccharin whereas (B) shows that of water in each of the two contexts on the test.
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the neutral context. That simple paired presentations of the conditioned context and LiCl, alternately with the presentations of neutral context alone did not cause any context-dependent aversion to the Xuid eliminated the possibility that the successful discrimination shown in Group S and Group W was a consequence of association of some uncontrollable cue with nausea. Consumption of water in the conditioned context was less in Group W than in Group S. On the other hand, these two groups showed little diVerence in their amount of consumption of saccharin solution in the conditioned context. In addition, consumption of saccharin in the neutral context was slightly less in Group S than in Group W. These Wndings were substantiated by statistical analyses. For test with the saccharin solution, a two-way ANOVA showed the signiWcant main eVect of group (F (2, 21) D 42.00) and context (F (1, 21) D 96.96), as well as a signiWcant interaction of these factors (F (2, 21) D 20.80). Subsequent multiple comparisons using the LSD method showed that for both Group S and Group W, the amount of consumption in the conditioned context was less than that in the neutral context. However, no diVerence was found in Group C. Amount of consumption in the conditioned context did not diVer between Group S and Group W, and both of the two groups consumed less than Group C. In the neutral context, the amount of consumption was less in Group S than in both Group W and Group C, which did not diVer from each other. For the test with water, an ANOVA revealed signiWcant main eVects of group (F (2, 21) D 23.68) and of context (F (1, 21) D 37.89), and their interaction was also signiWcant. Subsequent multiple comparisons showed that for both Group S and Group W, the amount of consumption in the conditioned context was less than that in the neutral context. No diVerence between the two contexts was found in Group C. In the conditioned context, the amount of consumption was less in Group W than in either Group S or Group C, and it was less in Group S than in Group C. In the neutral context, on the other hand, the amount of consumption did not diVer among groups. These Wndings suggest that the familiarity of the Xuid given during context discrimination training essentially did not aVect the process of the acquisition of context-dependent aversion. Although the consumption of Xuid during its initial presentations in the neutral context was more suppressed in Group S than in Group W, this diVerence did not aVect the eventual formation of a discrimination. Moreover, acquired context-dependent aversion generalized to the other Xuid, water for Group S and saccharin for Group W, suggesting that in both of them the conditioned context was directly associated with nausea. Together with the formation of successful discrimination shown in Experiment 1, the results of Group S also suggested that when a novel Xavor was presented as the target, whether or not the test Xuid (water) was given in the home cage during discrimination did not aVect the results. In addition, it was established irrespective of whether the number of the non-conditioning sessions given in each cycle was one or two. The Wnding that Group C did not show successful context discrimination indicates not only that the presentation of some Xuid was necessary for the establishment of an
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apparent context-dependent aversion, but also that the successful context-dependent aversions shown in Experiment 1 and Experiment 2 were not a consequence of the association of some uncontrollable cue with nausea.
Experiment 3 The results obtained from the previous two experiments seem to suggest that a direct association of the context with nausea underlies the formation of contextdependent aversion, irrespective of whether the Xuid given during discrimination training was novel or familiar. Experiment 3 aimed to investigate the eVects of the Xuid given in the home cage during the context discrimination phase and the eVects of the Xuid presented in the two contexts during the drinking training phase. For all of the following three groups of subjects, water was the target Xuid given in context discrimination. Subjects in Group WW were given water both in the two contexts during the drinking training phase and in their home cages during the context discrimination phase. Animals in Group WN were presented water in the two contexts during the drinking training sessions but were given 0.6% NaCl solution in their home cages during the context discrimination phase. Subjects in Group NN received NaCl solution during both of the two phases. Thus the procedure given to this group was identical to that to Group W in Experiment 2. If consumption of the same Xuid in both contexts and in the home cage during context discrimination is necessary for the formation of a context dependency that is speciWc to that Xuid, only Group WW would show it. If, on the other hand, preexposure to the Xuid during the drinking training phase causes the formation of the Xuid-speciWc context dependency, it should be evident in both Group WW and Group WN. Method Subjects The subjects were 24 male rats of the Wistar strain, about 70 days of age at the start of the experiment, with a mean weight of 255 g (range: 224–278 g). Fluids and contexts Tap water was used as the Xuid presented during discrimination training, and 0.6% NaCl solution was assigned as the Xuid given to some groups of animals as described below. In addition, a 0.05% saccharin solution was used as the test Xuid. The US was a 0.15 M, 10 ml/kg injection of LiCl. The two contexts presented during context discrimination were identical to those used in the previous experiments. Procedure The procedure of the experiment mirrored that of Experiment 2, except for the Xuid presented to the subjects. After a 3-day Xuid restriction period in which all the subjects were given 0.05% saccharin solution for 10 min both at 12:00 and at 16:00 in
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their home cages, they were divided into three groups (WW, WN, and NN, Ns D 8). During the 6-day drinking training sessions, subjects in Group WW, and Group WN were given water, whereas animals in Group NN were presented NaCl solution in both of the two contexts (note that they were not given any Xuid in the home cage during this phase). Through the context discrimination phase, animals in Group WW were given tap water while subjects in Group NN and Group WN were presented NaCl solution in their home cages. After three cycles of discrimination training, all the animals were tested with both the saccharin solution and water in the same manner as that for Group W in Experiment 2. Results and discussion Fig. 5 depicts the mean amount of consumption of water during context discrimination sessions. On the Wrst non-conditioning session of the Wrst cycle, there was less consumption in Group NN than in either Group WW or Group WN. Group WW and Group WN showed about the same amount of consumption throughout the Wrst cycle. During the second cycle, the amount of consumption on both of the non-conditioning sessions appeared more in Group WW than in either Group NN or Group WN. In both Group NN and Group WN, the amount of consumption on the conditioning session of the third cycle was less than that in either of the following two nonconditioning sessions. In Group WW, on the other hand, the amount of consumption did not vary among the sessions. A three-way ANOVA conducted on the scores from Figure 5 showed signiWcant main eVects of group (F (2, 21) D 13.77), cycle (F (2, 42) D 5.32), and session (F (2, 42) D 5.26); interaction between group and session (F (4, 42) D 5.85) and that between cycle and session (F (8, 84) D 2.45) were also signiWcant. In addition, interaction among the three factors (F (8, 84) D 2.45) was also signiWcant. Therefore, only
Fig. 5. Experiment 3: mean water consumption during three cycles of the discrimination stage. Each cycle consisted of a conditioning session (C) and two extinction sessions (E) given in each of the two contexts, respectively.
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signiWcant diVerences that were shown in the subsequent analyses by the LSD method and that are relevant to the discussion are described below. As for the group diVerences, it was revealed that on both of the conditioning and the Wrst non-conditioning sessions during the Wrst cycle, the amount of consumption of Xuid was less in Group NN than in either Group WN or WW, though WN and WW did not diVer from each other. This Wnding suggests that presentations of NaCl during drinking training sessions reduced the palatability of water. During the third cycle, however, more water was drunk by Group WW than by either Group NN or Group WN; though NN and WN did not diVer from each other. On the other hand, the amount of consumption on the second non-conditioning session did not diVer among the groups in either the Wrst or the third cycle. In all three groups, the amount of consumption of water on the conditioning session was less in the third cycle than in the second cycle. In both Group WN and Group NN, more was drunk in the conditioning session than in the following two non-conditioning sessions in the second cycle; in the third cycle less was drunk in the conditioning session than in the two non-conditioning sessions. In Group WW, on the other hand, the amount of consumption did not diVer among the three sessions through the three cycles. These Wndings indicate that during the third cycle of context discrimination training, the context-dependent aversion to water was apparent in Group WN and Group NN but not in Group WW. Fig. 6 shows the mean amount of consumption of water (panel A) and saccharin solution (panel B) during the test sessions. All three groups showed context dependency of aversion in the test with water: The amount of consumption was less in the conditioned context than in the neutral context. Group WW did not show evidence
Fig. 6. Experiment 3: (A) indicates mean consumption of water whereas (B) shows that of saccharin in each of the two contexts on the test.
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of context-dependent aversion during the discrimination training phase but revealed clear discrimination in the test. As a similar Wnding was reported by Boakes et al. (1997, Experiment 3), this would imply that it was during the third cycle of discrimination training that the context-dependent aversion developed and was apparent at the test. Amount of consumption of saccharin solution was less in the conditioned context than in the neutral context, for both Group NN and Group WN. On the other hand, it did not diVer between the two contexts in Group WW. A two-way ANOVA conducted on the test scores with water revealed that only the main eVect of context was signiWcant (F (1, 21) D 60.87). The same ANOVA conducted on the test to saccharin, on the other hand, showed that the main eVects of group (F (2, 21) D 20.77) and context (F (1, 21) D 33.26) and the interaction of these two factors (F (2, 21) D 9.46) were signiWcant. Post hoc comparisons showed that for both Group NN and Group WN the amount of consumption in the conditioned context was less than that in the neutral context. In contrast, the amount of consumption in Group WW did not diVer between the two contexts. In the conditioned context, the amount of consumption was more in Group WW than in either Group NN or Group WN, whereas no group diVerences were found in the neutral context. These Wndings suggest that in Experiment 3 the supplement of water in the home cage during context discrimination was responsible for the Xuid-speciWc context dependency of aversion. It is possible that this context dependency was a consequence of the summation of the two eVects, preexposure to water and a supplement of it in the home cage during discrimination training. However, it would be more reasonable to suppose that consumption of water in the home cage during context discrimination was, at the very least, the main cause of the Xuid-speciWc context dependency of aversion shown in the test, since Group WN failed to show the Xuid-speciWc aversion.
General discussion The Wndings obtained in the present three experiments demonstrate that contextdependent aversion can be established to both a novel Xuid (saccharin solution) and familiar water. Moreover, the established context dependency was not speciWc to the initial Xuid; it was revealed also when a second Xuid was given at the test, and the Xuid supplied in the home cages of the subjects diVered from that presented in context discrimination training. Fluid-speciWc context dependency was shown only when the same Xuid was given both in the two contexts and in the home cages of the subjects during the context discrimination. In addition, the context dependency established to saccharin was also revealed to water presented in the test, suggesting that whether the Xuid given in the home cage was the same as (Experiment 1) or diVerent from (Experiment 2) the test Xuid did not aVect the results of the test. Therefore, it is hard to attribute these results to the enhancement of a neophobic response in the conditioned context, when considering the familiarity of water for these subjects, especially that in Experiment 1.
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More importantly, the results of Experiment 2 clearly demonstrated that novelty of the Xuid had little eVect on the process of establishment of context-dependent aversion: Not only Group S that received novel saccharin during context discrimination but also Group W that was given water established context-dependent aversion and transferred it to another Xuid. These Wndings contradict the prediction that novelty of the Xuid given during context discrimination training determines whether or not the established context-dependent aversion is speciWc to it. Rather, the Wndings obtained from the present Experiments 1 and 2 agree with the simple assumption that both the Xuid, even water (e.g., Revusky & Parker, 1976), and the context associated directly with nausea during context discrimination training, and the Xuid-nausea association generalized to the second Xuid presented in the test. In Experiment 3, two groups (NN and WN) of rats that were given water in context discrimination training while they were supplied NaCl solution in the home cage showed the acquired context-dependent aversion to a second Xuid (saccharin solution). On the other hand, Group WW, to which water was given both in the two contexts and in the home cage, failed to show context-dependent aversion to the second Xuid. These Wndings seem to indicate that the context acquired an occasion setting property rather than a direct association with nausea only in Group WW (e.g., Puente et al., 1988; Boakes et al., 1997; but see also, e.g., Symonds et al., 1998). However, these Wndings could also be explained in terms of simple summation and generalization decrement. For the subjects in Group WW, presenting water in the home cage could be regarded as additional extinction trials. Consequently, the association of water with nausea would develop slower in this group than in the other two groups (Group NN and Group WN) that did not receive water in their home cages. In addition, the development of a context-nausea association would also be retarded in Group WW, if the water-context association potentiated it. The failure to show an indication of the acquisition of an aversion in this group during context discrimination training, shown in Fig. 5, supports this explanation. The results of the test shown in Group WW could be explained by assuming that aversive behavior was apparent only when the two events (water and contextual cues), each of which had not acquired substantial association with nausea, were presented together. Conversely, presentation the second Xuid would not be enough to result in apparent aversive behavior in the conditioned context because of the generalization decrement of the association acquired to water. On the other hand, the subjects in both Group NN and Group WN acquired a relatively more substantial association to water and to the conditioned context, since no additional water was given in the home cage. Then, the aversion to a second Xuid should be more evident in the conditioned context, which had been strongly associated with nausea. It might still be possible to assume that in Group WW the context acquired the property of an occasion setter. However, such an explanation does not explain why presenting the same Xuid in the home cage during context discrimination resulted in the acquisition of the occasion setting property by the context. For example, it has been shown that the property of occasion setting is acquired by a stimulus or context
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that has relatively lower salience than that of the conditioned stimulus (e.g., Holland, 1989; Holland & Hass, 1993). But, there seems little reason to assume that the context was less salient in Group WW than in Group NN or Group WN. Rather, the additional presentations of water in the home cage should reduce its salience (e.g., Wagner, 1981) and thus increase the relative salience of the context in Group WW. Another possible interpretation is that in all of the present experiments the context acquired the property of occasion setter and the Wndings simply reXect the direct generalization of aversion acquired to the original Xuid presented during context discrimination, an argument derived from the criticism that the Xuid consumption test does not provide unequivocal evidence of context-illness association (e.g., Symonds & Hall, 1997; Lopez & Cantora, 2003). However, the Wnding in Experiment 1 that the context dependency established to novel saccharin generalized to water is hard to explain as the direct generalization of aversion between the two Xuids, since the same water was also given daily and safely in the home cages throughout the experiment (and, in addition, through the life history of the subjects after weaning). Further, water had no chance to be associated with either nausea or the conditioned context (see Bills, Smith, Myers, & Schachtman, 2003). In fact, amount of consumption of water given in the home cage of the subjects on the days following each conditioning (overall mean: 10.7 ml) did not decrease through the experiment, suggesting that little generalization of aversion if any occurred. It would be more reasonable to assume that the apparent aversion to water shown in the test reXected the direct association between the conditioned context and nausea, rather than the direct generalization between the two Xuids. The results of the third experiment by Boakes et al. (1997) that showed the XuidspeciWc context dependency of aversion do not agree with the explanation described above, since the Xuid given in the home cage (water) was not the same as that presented during context discrimination training (sucrose). However, subjects in this experiment were preexposed to sucrose before being given context discrimination training, and two extinction test sessions were replicated for both sucrose and the test Xuid (saline) in each of the two contexts. Then, the averaged test scores might simply reXect a relatively weak association of sucrose with nausea and thus little generalization of it to the saline, and the fact that context-dependent aversion was apparent only to the sucrose would be explainable in terms of the simple summation of aversion acquired to sucrose and that to the contextual cues. For the present, therefore, explanation in terms of a summation eVect of associations acquired to Xuid, and to the contextual cues seems more parsimonious than explanation in terms of acquisition of an occasion setting function to the context, at least when the Xuid given during context discrimination training is not so salient.
References Archer, T., Sjoden, P.-O., & Nilsson, L. G. (1985). Contextual control of taste-aversion conditioning and extinction. In P. D. Balsam & A. Tomie (Eds.), Context and learning (pp. 225–271). Hillsdale, NJ: Erlbaum.
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Best, M. R., Brown, E. R., & Sowell, M. K. (1984). Taste-mediated potentiation of non-ingestional stimuli in the rats. Learning and Motivation, 15, 244–258. Bills, C., Smith, S., Myers, N., & Schachtman, T. R. (2003). EVects of context exposure during conditioning on conditioned taste aversions. Learning and Behavior, 31, 369–377. Boakes, R. F., Westbrook, R. F., & Barnes, B. W. (1992). Potentiation by a taste of toxicosis-based context conditioning: EVects of varying the test Xuid. Quarterly Journal of Experimental Psychology, 45B, 303–325. Boakes, R. A., Westbrook, R. F., Elliott, M., & Swinbourne, A. L. (1997). Context dependency of conditioned aversions to water and sweet tastes. Journal of Experimental Psychology: Animal Behavior Processes, 23, 56–67. Bonradi, C., Honey, R. C., & Hall, G. (1990). Context speciWcity of conditioning in Xavor-aversion learning: Extinction and blocking tests. Animal Learning and Behavior, 18, 229–237. Bouton, M. E., & King, D. A. (1983). Contextual control of the extinction of conditioned fear: Test for the associative value of the context. Journal of Experimental Psychology: Animal Behavior Processes, 12, 4–15. Bouton, M. E., & Swartzentruber, D. (1986). Analysis of the associative and occasion-setting properties of contexts participating in a Pavlovian discrimination. Journal of Experimental Psychology: Animal Behavior Processes, 12, 333–350. Durlach, P. D., & Rescorla, R. A. (1980). Potentiation rather than overshadowing in Xavor aversion learning: An analysis in terms of within-compound associations. Journal of Experimental Psychology: Animal Behavior Processes, 6, 175–187. Hall, G., & Honey, R. C. (1990). Context-speciWc conditioning in the conditioned-emotional–response procedure. Journal of Experimental Psychology: Animal Behavior Processes, 16, 271–278. Holder, M. D. (1988). Possible role of confounded taste stimuli in conditioned taste aversions. Animal Learning and Behavior, 16, 231–234. Holland, P. C. (1983). Occasion-setting in Pavlovian feature positive discrimination. In M. L. Commonds, R. J. Herrnstein, & A. R. Wagner (Eds.), Quantitative analyses of behavior: Discrimination processes (Vol. 4, pp. 183–206). New York: Ballinger. Holland, P. C. (1989). Occasion setting with simultaneous compounds in rats. Journal of Experimental Psychology: Animal Behavior Processes, 15, 183–193. Holland, P. C., & Hass, M. L. (1993). The eVects of target salience in operant feature positive discriminations. Learning and Motivation, 24, 119–140. Lopez, M., & Cantora, R. (2003). Associative interference with taste aversions after contextual discrimination learning. Learning and Motivation, 34, 372–388. Loy, I., Alvarez, R., Rey, V., & Lopez, M. (1993). Context-US associations rather than occasion-setting in taste aversion learning. Learning and Motivation, 24, 55–72. Lubow, R. E. (1973). Latent inhibition. Psychological Bulletin, 79, 398–407. Lubow, R. E. (1989). Latent inhibition and conditioned attention theory. Cambridge: Cambridge University Press. Mitchell, C., & Heyes, C. (1996). Simultaneous overshadowing and potentiation of taste and contextual cues by a second taste in toxicosis conditioning. Learning and Motivation, 27, 58–72. Puente, G. P., Cannon, D. S., Best, M. R., & Carrell, L. E. (1988). Occasion setting of Xuid ingestion by contextual cues. Learning and Motivation, 19, 239–253. Revusky, S., & Parker, L. A. (1976). Aversions to unXavored water and cup drinking produced by delayed sickness. Journal of Experimental Psychology: Animal Behavior Processes, 4, 342–353. Rowland, N. E., & Fregly, M. J. (1988). Sodium appetite: Species and strain diVerences and role of reninangiotensin-aldosterone system. Appetite, 11, 143–178. Symonds, M., & Hall, G. (1997). Contextual conditioning with lithium-induced nausea as the US: Evidence from a blocking procedure. Learning and Motivation, 28, 200–215. Symonds, M., & Hall, G. (1999). Overshadowing not potentiation of illness-based contextual conditioning by a novel taste. Animal Learning and Behavior, 27, 379–390. Symonds, M., Hall, G., Lopez, M., Loy, I., Ramos, A., & Rodriguez, M. (1998). Is Xuid consumption necessary for the formation of context-illness associations. An evaluation using consumption and blocking tests. Learning and Motivation, 29, 168–183. Wagner, A. R. (1981). SOP: A model for automatic memory processing in animal behavior. In N. E. Spear & R. R. Miller (Eds.), Information processing in animals: Memory mechanisms (pp. 5–47). Hillsdale, NJ: Erlbaum.