Effects of context novelty vs. familiarity on latent inhibition with a conditioned taste aversion procedure

Behavioural Processes 86 (2011) 242–249

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Effects of context novelty vs. familiarity on latent inhibition with a conditioned taste aversion procedure E. Quintero a , E. Díaz a , J.P. Vargas a , N. Schmajuk b , J.C. López a , L.G. De la Casa a,∗ a b

Department of Experimental Psychology, University of Seville, 41018 Seville, Spain Department of Psychology and Neuroscience, Duke University, Durham, NC 27708, United States

a r t i c l e

i n f o

Article history: Received 18 September 2010 Received in revised form 17 December 2010 Accepted 20 December 2010 Key words: Latent inhibition Home cage Novelty Context change

a b s t r a c t The latent inhibition phenomenon is observed when a conditioned stimulus is preexposed without any consequence before conditioning. The result of this manipulation is a reduction in conditioned response intensity to such a stimulus. In this study, we analyse the role of context novelty/familiarity on LI modulation by changing the context using a three-stage conditioned taste aversion procedure. Experiment 1 revealed that, similar to other learning procedures, a context change between preexposure and conditioning/testing (but not between preexposure/conditioning and testing) resulted in LI attenuation when the experimental contexts were novel. Experiment 2, using animals’ home cages as one of the contexts, revealed a different pattern of results, with an unexpected increase in LI magnitude when the context change was introduced between conditioning and test stages. The Schmajuk et al. (1996) computational model explains these results in terms of the increased novelty of the conditioned stimulus during preexposure, conditioning, and testing. © 2011 Elsevier B.V. All rights reserved.

1. Introduction Although latent inhibition (LI) was first described over 50 years ago (Lubow and Moore, 1959), the phenomenon continues to attract the attention of researchers worldwide (see, for a recent review, Lubow and Weiner, 2010). The techniques necessary to produce the effect in the laboratory are quite simple. The to-be conditioned stimulus (CS) is presented repeatedly by itself, and after subsequent pairing with the unconditioned stimulus (US), the conditioned response (CR) will be weaker than if the CS had not been preexposed. Despite the simplicity of the procedure, the processes underlying the LI effect have shown themselves to be quite complex, to the point that LI has become a crucial phenomenon for testing the validity of the associative learning theories that have emerged ˜ in recent decades (see, for example, De la Casa and Pineno, 2010). One possible source that has led to mixed experimental results, and hindered an adequate explanation of LI, involves the peculiarity of the procedures typically used in classical conditioning research. The conditioned taste aversion (CTA) procedure, in particular, offers several sources of confusion in LI studies (Lubow, 2008). However,

∗ Corresponding autor at: Dpt. Psicologia Experimental, Facultad de Psicología, C/Camilo Jose Cela, s/n, 41018 Sevilla, Spain. Tel.: +34 954557682; fax: +34 954551784. E-mail address: [email protected] (L.G. De la Casa). 0376-6357/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.beproc.2010.12.011

we will focus on the fact that many CTA-LI experiments have carried out the experimental manipulations in the animals’ home cages, while in other studies, the animals were transferred to different rooms and/or cages for one or more of the three experimental stages, and returned to the home cages during the periods when the experimental treatment was not applied. This source of variability is of great significance, considering that LI is highly sensitive to contextual manipulations (Lubow and De la Casa, 2005). In this study, we examine the effects of manipulating context in which the various experimental stages are conducted. We aim to identify to what extent a context change during a three-stage LI experiment with a CTA procedure affects LI, when all the experimental contexts are different from the home cage (Experiment 1) or one of the experimental contexts is the home cage (Experiment 2). We expect that changing the context across stages of a CTA procedure (preexposure, conditioning, and test) will affect LI in the same manner as prior studies have found when using other procedures, whether appetitive in nature (e.g., De la Casa et al., 2009) or aversive (e.g., De la Casa et al., 2005). In addition, we examine whether this context change effect can be modulated by the use of rats’ home cages as an experimental context. Changing the experimental context is of special interest, because the literature on the contextual specificity of LI in the CTA paradigm contains contradictory findings. Some experiments suggest that contextual changes reduce LI (Hall and Channell, 1986; Manrique et al., 2004), but others suggest LI remains intact (Best and Meachum, 1986; Chamizo, 1996; Kurz and Levitsky, 1982).

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As Lubow (2008, p. 45) stated in a recent review of the CTA-LI literature: Clearly, there is a need to determine why CTA-LI is, at best, only weakly global-context-specific. Furthermore, the sources of any putative global context effect, as well as of the better established local context effects, must be identified. Whether they are consequences of the relationship between the preexposure and conditioning contexts or between the preexposure and test contexts, or both, has important implications for theories of learning in general, and for LI specifically.

2. Experiment 1 Previous studies examining the role of context in LI using experimental preparations other than CTA have shown that LI generally is attenuated when the preexposure context differs from the conditioning and test contexts (e.g., Hall and Honey, 1989; Hall and Minor, 1984; Westbrook et al., 2000). However, within the CTA paradigm, as we mentioned earlier, there is limited evidence of contextual specificity of LI. Furthermore, most CTA-LI experiments have been conducted in familiar home cages rather than in novel contexts. Moreover, the available data are contradictory. For instance, Hall and Channell (1986; Experiment 3) found, using contexts other than the home cage and a 3-stage procedure, that a contextual change between the preexposure stage and the conditioning/test stages (ABB, being A the preexposure context and B conditioning and testing contexts, respectively) reduced LI. This mirrors findings from other paradigms in which this manipulation was performed. However, in other CTA studies, a similar context manipulation had no effect on LI (Chamizo, 1996; Kurz and Levitsky, 1982). In Kurz and Levitsky (1982), contextual control was perhaps not observed because of their particular procedure. During preexposure and test, they presented the animals with two bottles, one containing water and the other containing the flavour to be conditioned. However, during conditioning, the animals only had access to the flavoured bottle (CS). Although all other stimuli in the conditioning and test contexts were the same, the bottle difference could constitute a contextual change that perhaps reduced LI in the preexposed group, which would explain the observed lack of contextual specificity. In the study by Chamizo (1996), it is possible that there was a lack of contextual control because the animals were exposed to the preexposure context prior to the preexposure stage of the experiment. Therefore, familiarity with the preexposure context presumably increased, hindering any contextual specificity effect (see McLaren et al., 1994). Given the aforementioned issues, the present experiment studied the contextual specificity of LI using experimental contexts that were completely new to the experimental subjects. To analyse the effect of context change on LI, in addition to the usual LI group in which all the experimental stages occur in the same context (Group AAA), we used additional groups that experienced a contextual change. Specifically, as it has been demonstrated to be the most effective procedure for establishing the contextual specificity of LI in other preparations, we examined the effect of using different contexts in the preexposure and the conditioning/test stages (Group ABB). We also examined the effect of changing the context from the preexposure/conditioning stages to the test stage (Group AAB). Although other paradigms have not revealed any effect of this manipulation on the contextual control of LI (e.g., Lovibond et al., 1984; Westbrook et al., 2000), to our knowledge, this manipulation has not been employed within the CTA paradigm in contexts other than the home cage.

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2.1. Methods 2.1.1. Subjects Forty-eight adult male Wistar rats (University of Seville) were used. Mean weight before the experiment was 329 g. Animals were individually housed in plastic cages in a controlled temperature (21 ◦ C) room on a 12:12-h light–dark cycle. Standard rat food was available continuously. All procedures were conducted in agreement with the guidelines established by the Directive 86/609/CEE of the European Community Council, and the Spanish R.D. 223/1988. 2.1.2. Apparatus and materials Two different contexts, A and B, were used in this experiment. Context A was established in a 1 × 1 m room different from the vivarium, illuminated by a single 75 W red light, and kept at a temperature of 21 ◦ C. The floor and the walls of the experimental boxes used in context A were made of Plexiglas, and the ceiling was made of a red aluminium grating. The dimensions of the boxes were 40 × 20 × 19 cm, and the floor was layered with cardboard. Context B was located in a different room measuring 2.5 m2 . The room was illuminated by a florescent white light, and the temperature was kept at 21 ◦ C. The experimental boxes used in context B were similar to those used in context A (40 × 20 × 19 cm), except that the floor in context B was covered with a plastic green grating. The solutions were presented in 150 ml graduated glass bottles with fitted stainless steel spouts. The bottles were attached to the front of each cage during liquid presentation. The amount of fluid consumed was calculated as the difference between bottle weight before and after consumption. The taste used as CS was a 0.04% saccharin solution. The US was an intraperitoneal injection of LiCl (0.4 M, 0.5% bodyweight). All experimental sessions started at 10:00 a.m. 2.1.3. Procedures One week before the start of the experiment, the rats were randomly assigned to six experimental groups (n = 8), they were handled for 4 days, and the water bottles were removed from the home cages, initiating a 23.30 h water deprivation programme that was maintained through the duration of the experiment. On the experimental treatment days, each animal had 25 additional minutes when they could access water in the home cage after each session in the experimental box. The experiment involved three phases: preexposure, conditioning, and testing. Context was counterbalanced across groups, so that half the animals in each group were preexposed to context A, and the other half were preexposed to context B. The preexposure phase lasted 4 days. During this stage, the non-preexposed (NPE) groups (NPE-AAA, NPE-ABB, and NPE-AAB) received 5 min when they could access water, while the preexposed (PE) groups (PE-AAA, PE-ABB, and PE-AAB) received 5 min of access to the saccharin solution. Each preexposure trial began with a 10-min period in the experimental box in which there was no programmed activity, to allow the rats to adapt to the new context. Afterwards, the rats received 5 min when they could access the flavour in the experimental bottles (saccharin or water). After this 5-min period, the bottles were removed, and the rats remained in the context an additional 5 min before being returned to their home cages. The conditioning stage comprised a single session in which all the animals were allowed to access the saccharin solution for 5 min, followed immediately by an intraperitoneal LiCl injection. The animals in groups AAA and AAB underwent conditioning in the same context as that of the preexposure, while the animals in group ABB underwent conditioning in the other context. As in the preexposure stage, the conditioning session began with a 10-min waiting period in the experimental boxes. Next, the saccharin was presented for

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Table 1 Section A (Exp. 1): mean fluid consumption along preexposure trials as a function of preexposure taste (NPE: water vs. PE: saccharin) for Experiment 1. SEMs appear between brackets. Section B (Exp. 2): mean fluid consumption at preexposure trials as function of taste (NPE: water vs. PE: saccharine) and preexposure context (H: home cage vs. A: experimental cage) for Experiment 2. SEMs appear between brackets. A: Exp. 1

Trial 1

Trial 2

Trial 3

Trial 4

NPE PE

4.97 (0.60) 4.74 (0.37)

5.53 (0.57) 7.42 (0.38)

7.59 (0.40) 7.56 (0.44)

7.81 (0.46) 8.58 (0.40)

B: Exp. 2 NPE-H PE-H NPE-A PE-A

8.57 (0.78) 6.08 (0.52) 6.87 (1.06) 6.16 (0.85)

8.97 (0.35) 9.17 (0.40) 8.11 (1.45) 8.65 (0.75)

9.63 (0.44) 9.47 (0.35) 8.28 (0.37) 9.79 (0.37)

9.87 (0.37) 10.55 (0.34) 9.04 (0.52) 8.90 (1.14)

8

Mean Sac Consumption (ml)

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2.2. Results and discussion The upper section of Table 1 shows mean fluid consumption across preexposure trials as a function of the Preexposure condition. An analysis conducted on this data (mixed 4 × 2 ANOVA, with trials and preexposure: PE vs. NPE, as main factors) revealed a significant main effect of trials, F(3,138) = 35.03, p < .01, due to a general increase of fluid consumption across trials, probably reflecting a general habituation of neophobia effect. The main effect of preexposure was non-significant, F(1,46) = 1.44, p > .20. However, the trials × preexposure interaction was also significant, F(3,138) = 3.80, p < .05, reflecting a higher increase in consumption across trials for the PE groups as compared to the NPE groups. A 2 × 3 ANOVA (preexposure × context change condition) conducted on mean consumption on the conditioning day revealed no significant main effects and no interaction (all ps > .10). Fluid consumption ranged from 6.80 ml to 9.18 ml. Fig. 1 depicts mean consumption collapsed across trials as a function of preexposure and context change condition for the test stage. These data reveal a LI effect for the no context change condition (Group AAA), and for the condition that received preexposure and conditioning in the same context. However, when testing in a different context (Group AAB), the PE group drank more saccharin (i.e., less taste aversion conditioning) than the NPE group. Conversely, the LI effect was abolished when the preexposure context was different from the context at conditioning and testing (Group ABB), due to a decrease in consumption in the PE group. These impressions were confirmed for the statistical analyses. Specifically, a 2 × 3 ANOVA (preexposure × context change condition), conducted on mean saccharin intake collapsed across test trials, revealed a significant main effect of preexposure, F(1,42) = 19.99, p < .01, and a main effect of context change condition, F(2.42) = 3.41, p < .05. Post-hoc tests (Tukey, p < .05) were performed to identify differences between conditions. The main

PE

6 5 4 3 2 1 0

5 min. Then, the rats were injected with LiCl, after which they remained in the experimental boxes another 5 min before being returned to the home cage. The test stage lasted 2 days. During each test day, all the animals had access to the saccharin solution for 5 min. In the AAA groups, the test stage occurred in the same context as the preexposure and conditioning stages; in the ABB groups, the test stage occurred in the same context as conditioning; in the AAB groups, the test stage occurred in a context that was different from the two previous stages. The sequence of events in the test stage was similar to that of the previous stages: 10 min of adaptation, 5 min of flavour presentation, and a 5-min period in the experimental context before being returned to the home cage.

NPE

7

AAA

ABB

AAB

Context Change Condition Fig. 1. Mean saccharin consumption collapsed across test trials, as a function of Preexposure and experimental contexts. NPE: non-preexposed, PE: preexposed, AAA: preexposure, conditioning and test stages conducted at the same experimental context, ABB: preexposure conducted at experimental context A but conditioning and test at experimental context B, AAB: preexposure and conditioning conducted at experimental context A and test at experimental context B. Error bars represent SEMs.

effect of preexposure was due to an overall LI effect, with the preexposed animals drinking more saccharin than the non-preexposed. As for the effect of context change condition, the differences between AAA and ABB were significant, with higher fluid consumption in the former than in the latter. However, there were no significant differences between ABB and AAB, and none between the AAA and AAB conditions. As predicted, the preexposure × context change condition interaction was statistically significant, F(2,42) = 3.322, p < .05, indicating that LI was affected by the context change only in the ABB condition. To fully justify this statement, we ran separate 2 × 2 ANOVAs (NPE/PE vs. AAA/ABB and NPE/PE vs. AAB/ABB) on mean saccharin intake collapsed across test trials. The first ANOVA (NPE/PE vs. AAA/ABB) revealed significant main effects of preexposure, F(1,28) = 10.68, p < .01, due to the overall LI effect, and context change condition, F(1,28) = 6.04, p < .05, due to a higher consumption in the AAA as compared to the ABB condition. The preexposure × context change condition interaction was statistically significant, F(1,28) = 6.04, p < .05. To identify the source of the interaction, we ran simple effects analyses. There were differences between PE and NPE groups in the AAA condition, F(1,14) = 12.94, p < .01. However, the LI effect was abolished in the ABB condition, F(1,14) < 1. The PE groups in the AAA and ABB conditions were significantly different, F(1,14) = 7.44, p < .05. The NPE groups did not differ between them, F(1,14) < 1. The second ANOVA (NPE/PE vs. AAB/ABB) revealed a significant main effects of preexposure, F(1,28) = 7.71, p < .01, and context change condition, F(1,28) = 4.21, p = .05, due to the general LI effect and due to the greater consumption in the AAB as compared to the ABB condition. The preexposure × context change condition interaction was close to the standard levels of significance, F(1,28) = 3.45, p = .07. Simple effect analyses revealed significant differences between NPE and PE groups (i.e., the LI effect) for the AAB condition, F(1,14) = 10.12, p < .01, but not for the ABB condition, F(1,14) < 1. The difference between the PE groups was significant, F(1,14) = 5.91, p < .05. There were no significant differences between the NPE groups, F(1,14) < 1. In summary, the results showed that conditioned aversion to saccharin was reduced when it was preexposed, conditioned, and tested in the same context (AAA condition), and when preexposure and conditioning were conducted in the same context, but testing

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took place in a different one (AAB condition). This LI effect was mitigated when the preexposure stage (ABB condition) was carried out in a context different from that of the other stages. When we focus on this condition, it can be seen that group PE-ABB consumed significantly less than the standard group PE-AAA. The combination of this result and the lack of LI observed in group PE-ABB, when compared with the corresponding NPE group, demonstrate contextual specificity. These results indicate that, as it is with other experimental preparations (Hall and Honey, 1989; Hall and Minor, 1984; Kaye et al., 1987; Lovibond et al., 1984; Westbrook et al., 2000), CTA-LI is context-specific. The results for the group in which the contextual change occurred in the test stage (PE-AAB), showing a LI effect in spite of the context change introduced between preexposure/conditioning phases and testing stage, are not completely surprising considering that, as mentioned in the introduction, similar results have been found in prior studies performing this manipulation with other experimental preparations (e.g., Lovibond et al., 1984; Westbrook et al., 2000).

3. Experiment 2 Prior studies have shown LI to be more prominent when familiar contexts are used (e.g., Hall and Channell, 1985; Hall and Minor, 1984). Moreover, the use of a familiar context during preexposure may promote the transfer of LI to other situations (e.g. Hall and Channell, 1986; McLaren et al., 1994). The findings of Hall and Channell (1986), with a CTA procedure, are particularly relevant to the present study. They found that when the preexposure context was the animals’ home cage, a change in context between preexposure and conditioning/test stages did not affect LI, but when the change in context involved two experimental boxes different from the home cage, LI was affected. To determine whether the contextual specificity of LI depends on the familiarity–novelty dimension of the preexposure context, in this experiment, we examined the effect of contextual changes on LI using the home cage of the animals as the familiar context. Like Experiment 1, this experiment used the standard LI groups in which all the experimental phases occur in the same context. In this case, this context was the home cage (groups PE-HHH and NPE-HHH). The manipulations performed in the contextual change groups were similar to those of Experiment 1. Thus, the contextual change was introduced either between the preexposure stage and the conditioning/test stages (groups PE-HAA and NPE-HAA), or between the preexposure/conditioning stages and the test stage (groups PE-AAH and NPE-AAH). We selected the AAH condition, instead of the HHA condition that would have been more rational in relation to the logic of Experiment 1, because it will allow us a cross-experiment comparison with the AAB groups from Experiment 1, and a direct test of a possible interaction between context change and the effect of conducting preexposure vs. testing in the home cage. Based on prior findings (e.g., Hall and Channell, 1985; Lubow et al., 1976; McLaren et al., 1994), we expected that context familiarity would favour LI. Therefore, we expected a strong CS preexposure effect in group PE-HHH, which had the home-cage context across experimental stages. Group PE-HAA should also display LI despite the contextual change, as the familiarity of the preexposure context should allow LI to transfer to the other context. Regarding group PE-AAH, such LI transfer should not occur, given the non-familiarity of the preexposure context. However, because prior studies did not find this manipulation to determine LI (e.g. Lovibond et al., 1984; Westbrook et al., 2000), we did not have a firm prediction for this group.

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3.1. Methods 3.1.1. Subjects Forty-eight adult male Wistar rats (University of Seville) were used. Mean weight was 329 g before the start of the experiment. Each animal was individually housed in Plexiglas cages in a controlled temperature (21 ◦ C) room on a 12:12-h light–dark cycle. Standard rat food was available continuously. All procedures were conducted in agreement with the guidelines established by the Directive 86/609/CEE of the European Community Council, and the Spanish R.D. 223/1988. 3.1.2. Apparatus and materials Two contexts were used in this experiment: the animals’ home cages and an experimental context (context A). The home cages (35 × 20 × 14 cm) were located in the colony room (2.5 × 3.5 m). The floor and walls of these cages were made of Plexiglas, with wood shavings as bedding. The colony room was illuminated by four 100 W bulbs. Context A was the same described for Experiment 1. The solutions were presented in 150 ml graduated glass bottles with fitted stainless steel spouts. The bottles were attached to the front of each cage during liquid presentation. The amount of fluid consumed was calculated as the difference between bottle weight before and after consumption. The taste used as CS was a 0.04% saccharin solution. The US was an intraperitoneal injection of LiCl (0.4 M, 0.5% bodyweight). All experimental sessions were conducted at 10:00 a.m. 3.1.3. Procedures The rats were randomly assigned into six groups (n = 8). They entered a handling phase that lasted 4 days. One week before the experiment began, the water bottles were removed, and a 23.30 h deprivation programme was introduced. The deprivation programme was maintained throughout all the experimental stages. The experiment consisted of three stages: preexposure, conditioning, and test. The trials in context A followed the same sequence as described in Experiment 1: the animals were transferred to their corresponding experimental boxes and entered a 10-min waiting period with no programmed activity, for the purpose of adapting to the new context. Then they received the flavour of the corresponding experimental bottles (saccharin or water) for 5 min, after which the bottles were removed and the rats remained in the context for another 5 min before being returned to their home cages. The preexposure stage lasted 4 days. During this stage, the nonpreexposed groups (NPE-HHH, NPE-HAA and NPE-AAH) received 5 min of water in the experimental bottles. The preexposed groups (PE-HHH, PE-HAA and PE-AAH) received 5 min of saccharine solution in the experimental bottles. The groups differed in terms of the preexposure context. Preexposure occurred in the home cage for groups HHH and HAA, while it occurred in context A for groups AAH. The conditioning stage consisted of a single session. During this session, all the animals had access to the saccharin solution for 5 min, followed immediately by an intraperitoneal injection of LiCl. The conditioning stage occurred in context H for the HHH groups, while it occurred in context A for the HAA and AAH groups. The test stage began 1 day after conditioning, and lasted for 2 days. During this stage, all animals had access to the saccharin solution for a period of 5 min. For the HHH and AAH groups, the test occurred in context H, while for the HAA group, the test occurred in context A. 3.2. Results and discussion The bottom section of Table 1 depicts mean consumption at preexposure across trials as a function of Preexposure (PE vs. NPE) and

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Mean Sac Consumption (ml)

8 NPE

7

PE

6 5 4 3 2 1 0

HHH

HAA

AAH

Context Change Condition Fig. 2. Mean saccharin consumption collapsed across test trials as a function of preexposure and experimental contexts. NPE: non-preexposed, PE: preexposed, HHH: preexposure, conditioning and test stages conducted in home cages, HAA: preexposure conducted in home cages but conditioning and test in experimental cages, AAH: preexposure and conditioning conducted in experimental cages and test in home cages. Error bars represent SEMs.

Preexposure context (Home vs. Experimental). A 4 × 2 × 2 mixed ANOVA (trials × preexposure × preexposure context) revealed a significant main effect of trials, F(3,132) = 33.63, p < .01, reflecting a general increase in fluid consumption probably resulting from habituation of neophobia. No other main effect was significant (ps > .05). The trials × preexposure interaction was also significant, F(3,132) = 6.28, p < .01, due to the greater increase in consumption of saccharin across trials for the PE groups, as compared to water consumption for the NPE animals. No more interaction was significant (ps > .05). To analyse consumption on the conditioning day, a 2 × 3 ANOVA (preexposure × context change condition) was conducted. The analysis revealed significant main effects of preexposure and context change condition, F(1,42) = 13.68, p < .01, and F(2,42) = 10.14, p < .001, respectively. Post-hoc analyses (Tukey tests, p < .05) revealed higher fluid consumption for the preexposed as compared to the non-preexposed groups, and significant differences between HHH and HAA conditions and HHH and AAH conditions. There were no differences between conditions HAA and AAH. In order to minimize the effect of these differences, we introduced mean consumption on conditioning trial as a covariate in subsequent analyses. Finally, the preexposure × context change condition was non-significant, F(2,42) = 1.58, p > .21. Fig. 2 shows mean consumption collapsed across tests trials as a function of preexposure and context change condition. As can be seen, the LI effect, greater consumption (i.e., less conditioning) for the PE as compared to the NPE group, appeared in those groups that had been preexposed, conditioned, and tested in the home cages (HHH condition). The LI effect was reduced for the HAA condition, but the LI appeared, and it was even more intense, for the AAH condition. These impressions were confirmed by the statistical analyses. A 2 × 3 ANCOVA (preexposure × context change condition), with consumption at conditioning as a covariate, conducted on mean consumption collapsed across tests trials, revealed main effects of preexposure and context change condition, F(1,41) = 27.98; p < .001, and F(2,41) = 6.0, p < .01, respectively. The main effect of preexposure reflects a greater general consumption for the preexposed as compared to the non-preexposed groups. The context change condition effect was due to significant differences in consumption between groups in HHH vs. AAH condition, and HAA vs. AAH conditions.

As expected, the preexposure × context change condition interaction was significant, F(2,41) = 7.24, p < .01. In order to explore the source of the interaction, and to identify the differences between groups, we ran analyses of simple effects. There were significant differences between NPE and PE groups for the HHH and the AAH conditions, F(1,13) = 8.50, p < .05, and F(1,13) = 12.55, p < .01. For the HAA conditions, the differences between NPE and PE groups were non-significant, F(1,13) = 3.77, p > .07. In addition, there was no significant difference between the NPE groups in any condition (all Fs[2,20] < 1). Finally, comparisons between PE groups revealed that the PE-AAH group was significantly different from the PE-HHH, F(1,13) = 5.29, p < .05, and from the PE-HAA, F(1,13) = 11.19, p < .01. There was no difference between these latter groups, F(1,13) < 1. In summary, the results indicate a clear LI effect in the group that performed all the experimental phases in the highly familiar context of the home cage (groups HHH). On the other hand, the LI effect was not observed in the group for which the context changed between the preexposure and the conditioning/test stages (HAA), despite the familiarity of the preexposure context. A perhaps more surprising result was found for the group for which the context changed between preexposure/conditioning and test (AAH). Not only was the LI effect not reduced, but it actually increased. The lack of additional control groups to compare with the AAH condition makes it difficult to identify the source of greater LI in condition AAH as compared to condition HHH. It would be important to run additional experiments, including more appropriate controls to identify the source of the LI enhancement observed in the AAH condition. The lack of LI transfer in the HAA groups may be, in part, due to the difference in consumption between groups PE-HAA and NPEHAA during the conditioning stage. Thus, the lower consumption of group NPE-HAA may have resulted in a lower degree of conditioning, which in turn, would have masked the LI effect in group PE-HAA. However, this difference in consumption also occurred in the AAH groups, yet they showed the opposite LI result, a fact that allows us to reject the aforementioned explanation regarding the HAA groups. A more plausible explanation is that the reduction of the LI effect seen in group PE-HAA in relation to its control group, NPE-HAA, as compared to the LI effect observed in PE-HHH in relation to NPEHHH, indicates the contextual specificity of LI, and the absence of differences between PE-HAA and PE-HHH groups resulting from the familiarity of the preexposure context of the former contributes to reduced contextual specificity.

4. General discussion Overall, the results indicate that introducing a context change with a conditioned taste aversion procedure weakens LI when the change occurs between preexposure and conditioning/test, but not when it is introduced between preexposure/conditioning and test (Experiment 1). Therefore, it appears that contextual effects depend on the novelty of the context and the position of the context change (between preexposure and conditioning vs. between conditioning and testing). In Experiment 2, a change from a familiar to a novel context (HAA) reduced LI, but a change from a novel to a familiar context (AAH) produced a super-LI effect. Most theories handling LI have incorporated, in some form or other, mechanisms that account for the role of contextual cues in LI. For example, Wagner’s (1981) SOP model assumes that context–CS associations, formed during preexposure, reduce the rate of acquisition during conditioning, and reduce the rate of expression during testing, of the CS–US associations. According to this model, a contextual change occurring between preexposure and conditioning will decrease the prediction of the CS (Group ABB in Experiment

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1), thereby facilitating the formation of the CS–US association, and decreasing LI. Similarly, when the contextual change occurs between conditioning and testing (Group AAB in Experiment 1), presenting the CS during the test without the preexposure context, should increase the rate of response and decrease LI. Therefore, in line with the results of Experiment 1, LI is expected to be stronger in Group AAA than in Group ABB or Group AAB. However, for the same reasons, the SOP model wrongly expects LI to be stronger in Group HHH than in Group AAH in Experiment 2. The Pearce and Hall (1980) model does not give explicitly contextual cues a role in LI and, therefore, the model is not able to describe the absence of LI in group ABB and its presence in group AAA, which can be attributed to a contextual change between preexposure and conditioning. Some theories have suggested the possibility that context modulates the expression of the associations between CS and no consequences, and between CS and US, formed during preexposure and conditioning, respectively (e.g., Bouton, 1993). According to this hypothesis, if the contextual change occurs between the preexposure stage and the conditioning/test stages, then, since the test occurs in the same context as that of conditioning, the CS–US association will be recovered during the test. Similarly, when the contextual change occurs between the preexposure/conditioning stages and the test stage, presenting the CS during the test without the preexposure context should hinder recovery of the CS–no consequences association, and favour recovery of the CS–US association. The results of Experiment 1 are in line with these predictions. However, the increased LI found when the home cage was used as the test context (AAH) in Experiment 2 is problematic for this perspective. Another theory, which assumes that context directly impacts LI is known as the comparator hypothesis, proposed by Miller and his associates (e.g., Grahame et al., 1994; Miller et al., 1986; Miller and Matzel, 1988). This hypothesis assumes that during preexposure, when there are no consequences for the to-be-CS, an association develops between the to-be-CS and the context in which it appears. In the conditioning stage, two additional associations are formed: CS–US, and context–US. During the test, CR intensity in response to the CS depends on a comparison of the US representation activated directly by the CS, and the US representation activated indirectly by the CS–context and context–US associations. The reduced CR, which defines the LI results because it presents the CS, during the test and in the same context as that of preexposure and conditioning, promotes (i) a directly activated US representation, stemming from the CS–US association established during conditioning; and (ii) an indirectly activated US representation, stemming from the CS–context association created during preexposure and the context–US association formed during conditioning. The comparison of the two US representations produces a weak CR, interpreted as LI (Grahame et al., 1994). The result that we observed when changing the context between the preexposure stage and the conditioning/test stages accords with this hypothesis. On the other hand, as with the previous theory, the comparator hypothesis has difficulty explaining the results of group, PE-AAH. If the contextual change occurs between the preexposure/conditioning stage and the test stage, the comparator hypothesis would predict that, in the absence of contextual associations at the time of the test, only the directly activated US representation (in response to the CS) should be recovered, leading to a fully intense CR (a reduced LI). Perhaps any procedure performed in a familiar context like the home cage has a different effect than the same procedure performed in a novel context. When preexposure and conditioning are carried out in the home cage, the potential for the context to become associated with any event will be reduced by virtue of prior experience in which that context was repeatedly preexposed without

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consequences. Hall and Symonds (2006) provided evidence along these lines by preexposing a context before pairing it with the US (LiCl). Their results showed that both four and eight 30-min exposures to the context, in isolation, blocked later association of this context with the US. Based on these results, it appears that when the home cage is used, context familiarity hinders the modulating role, which contextual cues play during the preexposure stage. The association established during the preexposure stage will not be expressed unless a cue is presented that recovers the association. Thus, LI should be weakened when the home cage is used as the preexposure context. This hypothesis explains the results of group HAA, but like the other theories, it cannot explain the results of group AAH. Regarding the familiarity of the home cage, another possibility is that it functions as a safety signal, given that the animals receive food and water in this context and do not generally experience aversive events. From this perspective, and applying the proposal developed by Bouton (1993), we can explain the results of group AAH. During the preexposure and conditioning stage, perhaps the animals formed a CS–no-consequence association and a CS–US association, respectively, modulated by context A. During the test stage, when the CS appeared in the home cage, the “safety” of the context led to a stronger recovery of the CS–no consequences association relative to the CS–aversive US association. Although this possibility can explain why LI would hold, it does not quite explain why it actually increased. Undoubtedly, a more detailed study is needed on the modulating role of the familiarity/safety of the home-cage context when the conditioned taste aversion procedures are conducted in its presence. An alternative to the aforementioned theories, which also addresses the role of context in LI, is the Schmajuk, Lam and Gray (SLG) model (Schmajuk et al., 1996), an attentional-associative model of classical conditioning. The SLG network incorporates (a) a mechanism that modulates attention to the conditioned stimuli (CSs) in proportion to the total novelty detected in the environment, and (b) a network that forms CS–CS and CS–unconditioned stimulus (US) excitatory and inhibitory associations, according to a real-time competitive rule. The model assumes that total novelty increases when (a) a predicted CS or predicted US is absent, or (b) an unpredicted CS or unpredicted US is present. In the model, presentation of a CS activates a short-term memory trace, TCS , which is combined with the prediction of that CS, BCS , by other CSs or the context (CX). The combined input (TCS + BCS ) becomes associated through attention zCS with the novelty detected in the environment. Notice that novelty increases when the CS is not well predicted by itself, by other CSs, or by the context (as in Wagner’s SOP model, 1981) and when the CS is not a good predictor of the US (as in the Pearce and Hall, 1980 model), other CSs, or the context. As novelty increases, the strength of the CS representation increases. The representation of the CS, XCS ∼ zCS (TCS + BCS ), becomes associated with the US through association VCS–US . Changes in VCS–US are proportional to a common error term (US − BUS ), which reflects the difference between the predicted, BUS , and the real value of the US, and to an individual error term, (1 − VCS–US ), which limits the association that a CS can gain with the US. Finally, the conditioned response, CR, is a non-linear function of BUS . Notice that the strength of the CS representation, XCS , determines not only the magnitude of its association with the US, but also the magnitude of the resulting CR. According to the SLG model, LI occurs because, after preexposure of the to-be CS in a given context, novelty and the strength of the CS representation are low, thereby hindering the formation of the CS–US association in the same context. However, if the context changes between the preexposure and the conditioning stage, novelty increases because the new context does not fully predict the CS and because the CS predicts the old context. Consequently, the

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Fig. 3. Section A: Simulated saccharin consumption in groups AAA, ABB, and AAB. Average consumption over five test trials, following 50 preexposure and 10 conditioning trials. The simulation procedure was identical to that used for Experiment 1, with the exception of two contexts, with a salience of 0.2, which represented the training cages A and B, and a third context, with a salience of 0.3, which represented the generalization between the contexts. In the training cages, a negative five time units (t.u.) US of strength −0.05, represented the appetitive value of the solution. Section B: simulated saccharin consumption in groups HHH, HAA, and AAH. Average consumption over five test trials, following 50 preexposure and 10 conditioning trials (consumption = 0.9 − CR). In the preexposure trials in the PE case, a conditioned stimulus representing the water was presented for 20 t.u. simultaneously with another stimulus representing the flavour; the water CS was presented alone in the NPE case. The intertrial interval (ITI) was 500 t.u. A context with a salience of 0.2 represented the training cages, another context with the same salience represented the home cage, and a third context with a salience of 0.3 represented the common elements between the contexts. A negative, five t.u. US of strength −0.1, represented the appetitive and safety values of the solution when drunk in the home cage, and a weaker US of strength −0.05, represented the appetitive value of the solution when drunk in the training cage. The effect of the aversive LiCl was represented by a positive five t.u. US of strength 1.

strength of the CS representation increases and leads to a strong CS–US association, and in turn, a reduction of LI (see, for example, Schmajuk, 2005). In the case of conditioned taste aversions used in the present paper, the SLG model suggests that novelty increases when the situation changes from the preexposure stage, with an appetitive water-and-saccharin flavoured CS, to conditioning, with the same CS predicting an aversive US (the noxious effects of LiCl). Again, this increase in novelty increases the strength of the CS representation, XCSs , and leads to an increased CR and, therefore, a reduction of LI at testing. In addition to the degree of acquired aversive value of the flavour, fluid consumption and LI are a function of the appetitive value of the water-and-saccharin flavour CS at testing. As can be seen in Fig. 3 (Section A for Experiment 1 and Section B for Experiment 2), computer simulations of the results of our experiments – in which both contexts and the hedonic value of the liquid change – are in line with these principles. Fig. 3 Section A, shows that the SLG model captures well the difference in consumption between the AAA, ABB, and AAB groups in Experiment 1. The model suggests that the reduced LI observed in group PE-ABB is due to the increased novelty produced by changing the context in the conditioning stage. On the other hand, the slight weakening of LI seen in group PE-AAB, the contextual change of which occurred between conditioning and test, would occur because the CS–US association formed during conditioning was weak. In other words, although introducing the new context during the test would intensify the CS representation, it would not activate an intense CR because the CS–US association had a lower magnitude. In contrast to the abovementioned theories, the SLG model can also explain the results of Experiment 2, in which one of the contexts was the home cage of the animals. Fig. 3, Section B, shows that the model captures well the difference in consumption between the HHH, HAA, and AAH groups in Experiment 2. We assumed that preexposure to the saccharin solution and water alone, had a rewarding effect on the thirsty animals and that this rewarding effect was stronger when the water or the solution was dispensed in the home cage and not in another context. Notice that this assumption has some similarities with Revusky (1971) learned safety idea

and De la Casa and Lubow (De la Casa and Lubow, 2002, p.119; see also Wheeler et al., 2004) suggestion that the water has a hedonic value. Therefore, the SLG model is capable of describing the effect of context changes in LI of CTA, even when the home cage is one of those contexts.1 Furthermore, it is tempting to speculate that the deleterious effects of context changes on LI of CTA might be absent because of an increased effect of the hedonic change, which would mask the weaker effect of the context change. Notice that the SLG is unique in predicting contextual changes in all types of LI because it captures the effect of context changes in terms of the increased novelty that follows (a) the weakened prediction of the CS when the context changes between preexposure and conditioning (groups ABB and HAA) or conditioning and testing (AAB), an effect that Wagner’s (1981) SOP model would also predict; and (b) the changes in the hedonic value of the solution previously predicted by the CS (groups AAB vs. AAH), which we propose in this paper. To conclude, it appears that when contexts are novel, the mechanisms that underlie LI are the same when induced with CTA as when induced with other procedures. Changing the context between the preexposure and conditioning stage has been shown to reduce LI in various types of preparations, whether the preparations involved appetitive conditioning, (e.g., De la Casa et al., 2009), conditioned emotional response (e.g., De la Casa et al., 2005), or spatial learning tasks (e.g., De la Casa and Timberlake, 2006). In all these experiments, the contexts were novel for the test subjects at the beginning of the experiment, a fact that likely promoted associations between the context and the stimuli presented during the experiment. However, it appears that a context that is familiar and safe, like the home cage, triggers other mechanisms, or at least it alters the functioning of the usual mechanisms. Therefore, we believe future studies should examine how context properties (e.g., familiarity, safety, and other functional aspects) affect the manner in which the context modulates associative learning phenomena, such as LI.

1 Detailed information on values and results of the simulations can be requested from the authors.

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