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Effects of post-treatment retention interval and context on neophobia and conditioned taste aversion
Behavioural Processes 63 (2003) 159–170
Effects of post-treatment retention interval and context on neophobia and conditioned taste aversion夽 L.G. De la Casa a,∗ , E. Diaz a , R.E. Lubow b a
Department of Experimental Psychology, Faculty of Psychology, University of Seville, C Camilo Jose Cela sn, Sevilla 41018, Spain b Department of Psychology, Tel-Aviv University, Tel Aviv, Israel Received 6 March 2003; received in revised form 21 April 2003; accepted 22 April 2003
Abstract We have repeatedly observed that a delay between acquisition and test, and the nature of the context in which the delay is spent, modulates latent inhibition (LI) of conditioned taste aversion (CTA; e.g. [Anim. Learn. Behav. 28 (2000) 389; Anim. Learn. Behav. 30 (2002) 112]). The present paper analysed the effects of delayed testing and treatment context after flavor exposure on the recovery of neophobia (Experiment 1) and on extinction after simple conditioning (Experiment 2). Two experiments were conducted with the same factorial design (2 × 2: 1 day versus 21 days of delay between first and second stage, and home versus experimental cages as place of experimental treatment). There were independent effects of both variables on habituation of neophobia and conditioning strength as measured on extinction trials. The long delay produced a reduction of neophobia (Experiment 1) and an increase in conditioning (Experiment 2). In addition, more of the flavored solution was consumed when the experimental treatment was conducted in the home cage than in the experimental cage (Experiment 1), and there was stronger conditioning when the delay period took place in the experimental cages than in the home cages (Experiment 2). The implications of these results for LI, as well as their relevance for experiments that use the CTA paradigm, are discussed. © 2003 Elsevier Science B.V. All rights reserved. Keywords: Neophobia; Conditioned taste aversion; Retention interval; Latent inhibition; Habituation
Conditioned taste aversion (CTA) has proven to be a popular and useful tool for studying associative learning. Although there have been debates as to whether CTA represents normative classical conditioning, primarily because it alone tolerates long intervals between CS and US, there are also certain procedural idiosyncrasies that warrant examination (e.g. see Klosterhalfen and Klosterhalfen, 1985). 夽 Part of this paper was presented at the XIV Congress of the Spanish Society of Comparative Psychology (Seville, Spain, September 2002). ∗ Corresponding author. Tel.: +34-9-545-576-82; fax: +34-9-545-517-84. E-mail address: [email protected] (L.G. De la Casa).
For example, CTA and other flavor-based experiments, with the exception of those in which context is a variable, almost always are conducted entirely in the home cage (excluding the brief period in which the animals are removed for the purpose of administering the US). This, of course, is a result of the fact that most of the experimental manipulations, and the testing of their effects, are easily accomplished within the confines of the home environment, a situation that is very different from other preparations, in which special apparatus is required to administer the protocol. The possible consequences of such differences are particularly apparent in studies that are designed to study the effects of retention interval, a topic that
0376-6357/03/$ – see front matter © 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0376-6357(03)00080-9
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has received much attention, particularly in regard to retrieval theories of latent inhibition (LI) and extinction (e.g. Bouton, 1993; Bouton et al., 1999; Miller et al., 1986). We have recently shown, as described below, that the relationship of the context in which the animal spends the retention interval to those contexts in which the other phases of the experiment are conducted, such as stimulus pre-exposure, conditioning, extinction, and testing, has profound effects on test phase performance. A number of studies have reported that LI of CTA is attenuated when a long delay is introduced between the conditioning and test sessions (Aguado et al., 1994, Experiment 1; Aguado et al., 2001, Experiment 2; Bakner et al., 1991, Experiment 2; Ishii et al., 2002, Experiments 1 and 2). In these studies, the experimental manipulations, including the delay periods, were conducted in the animals’ home cages. However, when the pre-exposure, conditioning and test stages of an LI experiment are conducted in a context that is different from that of the home cage, and the delay is spent in the home cage, then, instead of attenuated LI, there is a super-LI effect (De la Casa and Lubow, 2000, 2002; Lubow and De la Casa, 2002). One explanation for these apparently contradictory results appeals to the preservation or extinction of a hypothetical context–[CS-nothing] association that is established during the pre-exposure stage. Specifically, during the course of pre-exposures to the flavor, an association is formed between the flavor and the absence of a consequence. Furthermore, this association is specific to the context in which pre-exposure is conducted. At the time of test, if the test context is the same as the stimulus pre-exposure context, then this association is retrieved, resulting in higher levels of flavored fluid consumption than in a control group conditioned without previous exposure to the flavor (i.e. LI). However, when a long delay is introduced between conditioning and test stages, the test context either maintains or loses its capacity to elicit the context–[CS-nothing] association, depending on whether the delay takes place in a different or same context from pre-exposure and conditioning (De la Casa and Lubow, 2000, 2002). When the interval context is the “same,” the higher order association is extinguished, and LI is attenuated (e.g. Aguado et al., 1994, 2001). When the interval context is “different,” the context–[CS-nothing] association is protected from extinction.
Given that the direction of the delay-induced LI effects are critically dependent on the relationship of delay context to those of the other experimental stages, the question arises as to whether other CTA and related taste-aversion effects may not also be affected by this long-ignored procedural variable. In this regard, two classes of experimental phenomena are of particular interest, both in their own right and as a means to understand the processes that modulate LI: the recovery of habituated neophobia (e.g. Aguado et al., 1994; Best et al., 1978) and the retention interval effect (RIE; e.g. Batsell and Best, 1992a,b). The former refers to the delay-induced recovery of a habituated avoidance response to a novel flavor, and the latter to a delay-induced increase in conditioned aversion to a flavor. In both cases, the relationship of the delay context to that of the preceding treatment context and to the subsequent testing context has important theoretical consequences, both for theories that claim that retention interval and context change effects are additive (e.g. Bouton et al., 1999) and for theories that account for certain learning effects on the basis of associations between the nominal target stimulus and the context (e.g. Wagner, 1981). In summary, experiments that use flavored fluids or foods as stimuli are typically conducted entirely in the home cage. Thus, when there is a manipulation of a retention interval, the interval is spent in the same context as the other stages. In other preparations, as for example conditioned suppression, the CS and US must be administered outside the home cage. Thus, the delay interval is spent in a context that is different from that of the other stages. In previous CTA experiments, we have shown that the direction and magnitude of LI and spontaneous recovery are dependent on the relationship between the interval context and the remaining treatment contexts. This relationship may well influence other flavor-based delay-induced effects. Indeed, there is some independent evidence concerning the roles of context and delay on habituation of neophobia (e.g. Bonardi et al., 1991; Honey et al., 1992), and on CTA (e.g. Batsell and Best, 1994; Swank, 2000). However, the interaction between the context and delay variables, already shown to be critical for predicting the direction of LI effects, has not been explored for habituation of neophobia and CTA. The present paper addresses this issue.
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1. Experiment 1 Habituation is usually defined as the waning of a stimulus-induced response as a consequence of repeated presentations of that stimulus, at least when such reduction cannot be accounted for by simple fatigue or sensory adaptation (Thompson and Spencer, 1966). Importantly, there is a distinction between short- and long-term habituation (e.g. Sharpless and Jasper, 1956). The latter has been frequently treated as an example of learning. Of particular interest has been the claim that long-term habituation is based on the acquisition of stimulus–context associations (Wagner, 1979; but see Marlin and Miller, 1981). Irrespective of any specific theory of habituation, the fact that it may survive retention intervals in the order of weeks (e.g. Harding and Rundle, 1969; Leaton, 1974) would, indeed, support a learning interpretation. The relationship between retention intervals and the context in which they occur has played an important role in testing Wagner’s model of associative learning as applied to long-term habituation. If such habituation depends on the formation of stimulus–context associations, then exposing the animal to the context after the repeated stimulus presentations in that same context should result in extinction of the stimulus–context association, and therefore it should interfere with the expression of the habituated response. On the other hand, if the intervals are spent in a different context from that in which the repeated stimulus presentations occurred, then habituation should be intact, or at least not as attenuated as in the same context condition. The delayed-testing procedure as applied to habituation of taste aversion usually focuses on neophobia. It is well documented that upon first presentation of a novel flavor, the rat, and other omnivores, will drink or eat considerably less than on subsequent presentations of the same flavor (e.g. Domjan, 1976; Siegel, 1974). The difference in the amount of the novel flavor consumed on the first trial and the amount consumed on the trial at which asymptotic consumption is reached defines the magnitude of the neophobic response. By interpolating a delay interval between the last trial of the exposure stage and a test trial, one can assess the effects of time on the habituated neophobic response. In general, an increase in the retention interval, at least up to 24 h, reduces neophobia (e.g. Bonardi et al., 1991; Bond and Westbrook, 1982; Green and Parker,
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1975; but see Kasprow and Schachtman, 1993). However, the present paper focuses on relatively long retention intervals, primarily because most studies of the effects of retention interval on LI, extinction, and recovery from extinction use long intervals, and our aim is to develop a common theoretical framework for these disparate experimental paradigms. A number of studies have indicated that the length of the delay period between exposure and test does not affect recovery of the habituated neophobic response. This appears to be true when the exposure, delay, and test phases are all conducted in the same context (Aguado et al., 1994, Experiment 2; Kaye et al., 1988, Experiments 1–3; Kraemer and Roberts, 1984, Experiments 3 and 4; Siegel, 1974), as well as when the delay context is different from that of the other stages (Best et al., 1978; Miller et al., 1990, Experiment 1; Steinert et al., 1980). We choose to continue this line of investigation with the same exact parameter values that we have used to modulate delay-induced LI, producing attenuated LI when the retention interval context was identical to the pre-exposure, acquisition, and testing contexts, and super-LI when the retention interval context was different from the other contexts. Thus, the main aim of Experiment 1 was to examine the effects of delayed testing (1 day versus 21 days) and place of experimental treatment (home cages versus experimental cages) on the habituation and recovery of neophobia. To this end, after four trials of mere exposure to a saccharin solution, intended to obtain habituation of neophobia, a test trial was conducted 1 or 21 days after exposure. For half of the animals, all experimental treatments were conducted in a familiar context (home cages). For the other half, all experimental treatments, except for the delay, were conducted in a different, non-familiar context (experimental cages).1 The experimental design is summarized in Table 1. We predicted an Exposure × Delay × Context interaction. The stimulus exposed group that 1 The context manipulation confounds familiar/non-familiar with home/experimental cages. Elsewhere, we have presented the rationale for the contention that the critical element for producing super-LI is the uniqueness of the delay context relative to the training contexts, and not its familiarity (Lubow and De la Casa, 2002). We chose the same procedure here in order to reproduce the conditions that produced the super-LI effect in previous experiments (De la Casa and Lubow, 2000, 2002; Lubow and De la Casa, 2002).
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Table 1 Designs for Experiment 1 (upper section) and Experiment 2 (lower section) Group
Place
Exposure
Conditioning
Delay (days)
Test
Experiment 1 EX/HOME/1 EX/EXP/1 EX/HOME/21 EX/EXP/21 NEX/HOME/1 NEX/EXP/1 NEX/HOME/21 NEX/EXP/21
Home Exp. Home Exp. Home Exp. Home Exp.
Sacch Sacch Sacch Sacch Water Water Water Water
– – – – – – – –
1 1 21 21 1 1 21 21
Sacch Sacch Sacch Sacch Sacch Sacch Sacch Sacch
Experiment 2 HOME/1 EXP/1 HOME/21 EXP/21
Home Exp. Home Exp.
– – – –
Sacch–US Sacch–US Sacch–US Sacch–US
1 1 21 21
Sacch Sacch Sacch Sacch
Abbreviations: home, home cages; exp., experimental cages; and sacch, saccharine
spent the delay in the same context where the experimental treatment was conducted should show recovery of neophobia, thus drinking less of the flavored solution, due to extinction of the context–flavor association (Wagner, 1981), as compared to the group in which the delay context was different from the treatment context, which should show a decrease of the neophobic response after the delay (e.g. Bonardi et al., 1991). This prediction relates to the super-LI effect (e.g. De la Casa and Lubow, 2000), because the enhancement of LI that is observed after a delay that is spent in a context different than the context of the experimental treatment could be mediated, at least in part, by the expected decrease in the neophobic response. 1.1. Method 1.1.1. Subjects Fifty-six male adult Wistar rats (n = 7 per group) participated in the experiment (mean weight 329 g, range 302–383 g). The animals were individually housed in 40 cm×20 cm×24 cm Plexiglas cages, with wood shavings as bedding, on a 12:12 h light:dark cycle. Standard rat food was continuously available. Tap water was supplied from bottles with stainless steel spouts. 1.1.2. Apparatus For animals in the experimental cage condition, exposure and test were conducted in an isolated room,
different from the colony room. For all sessions in this condition, animals were transported to the experimental room and placed in individual 30 cm × 18 cm × 18 cm Plexiglas cages, with wood shavings as bedding, where exposure and test trials took place. For those animals in the home cage condition, all experimental manipulations were conducted in the home cages. All liquid rations were provided at room temperature in 150-ml graduated plastic bottles, fitted with stainless steel spouts, similar to those used for normal rations. The bottles were attached to the fronts of the cages during liquid presentations. The amount of fluid consumed was calculated as the difference between bottle weight before and after each liquid presentation. The fluids during the pre-exposure session were a 0.04% sodium saccharin solution for the Exposed subjects, and tap water for the Non-exposed subjects. 1.1.3. Procedure After 7 days on a 23.5 h water-deprivation schedule, the exposure phase was initiated. For half of the animals, all experimental manipulations were conducted in the home cages (HOM condition); for the other half, exposure and test were conducted in the experimental cages, but the delay was spent in the home cage (EXP condition). During this phase, half of the animals had access to the saccharin solution for 4 days, 5 min per day (EX condition). The remaining animals consumed water for the same period (NEX condition). On each of the exposure days, the 5 min availability of liquid was
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followed immediately by 25 min of water to complete the daily 30 min ration. The test phase, similar for all animals, consisted of a single 5 min exposure of saccharin. This phase was initiated 1 day after exposure for half of the animals (1-day condition) and 21 days after exposure for the other half (21-day condition). To equate deprivation levels at the time of testing for both delay conditions, animals in the 21-day condition received ad libitum water from days 13 to 20. On day 21, the water-deprivation schedule was reinstated. Test trials for animals in the 21 day of delay condition were conducted on day 32. Fluid consumption during all experimental sessions was computed. 1.2. Results and discussion 1.2.1. Pre-exposure phase A 2 × 2 × 4 mixed ANOVA (Exposure, Context, and Trials) was conducted on mean amount of fluid consumed by the four groups. There was a significant main effect of Context [F(1, 52) = 15.93, P < 0.001], with subjects exposed in the home cages drinking more than those exposed in the experimental cages (9.84 ml, S.D. = 1.42 and 8.37 ml, S.D. = 1.32, respectively). The main effect of Exposure (saccharin versus water) and the Context × Exposure interaction were not significant (Ps > 0.75). For the within-subject analyses, there was a significant effect of Trials [F(3, 156) =
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9.38, P < 0.001], with fluid consumption increasing across trials. The Trials × Context and Trials × Exposure interactions were significant [F(3, 156) = 2.94, P < 0.05, and F(3, 156) = 2.73, P < 0.05]. The Trials×Context interaction reflects an increase of fluid consumption across trials for subjects in the home cages, but not for those in the experimental cages. The Trials × Exposure interaction reflects the expected increase in saccharin consumption across trials (habituation of neophobia). The remaining interactions with Trials were not significant (Ps > 0.15). 1.2.2. Test phase Fig. 1 shows mean amount of saccharin consumed on the test day as a function of Exposure and Delay for those subjects in the home cage condition (Panel A) and the experimental cage condition (Panel B). As can be seen, EX groups consumed more saccharin solution than NEX groups; 21-day delay groups drank more than 1-day delay groups; and home cage groups drank more than experimental cage groups. These observations were confirmed by a 2 × 2 × 2 ANOVA (EX-NEX, Delay, and Context). The three between-group effects were significant [F(1, 48) = 8.76, P < 0.01; F(1, 48) = 4.38, P < 0.05; F(1, 48) = 14.05, P < 0.001, for Exposure, Delay and Context factors, respectively]. None of the interactions was significant (F s < 1).
Fig. 1. Mean amount of saccharin consumption as a function of delay between pre-exposure and test stages (1 and 21 days) on test trial for home cage condition and experimental cage condition. Error bars represent S.E.M.s.
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The fact that the NEX groups, which received saccharin for the first time in test, consumed less saccharin than the EX groups, which received saccharin for the fifth time, clearly revealed the neophobia effect. Importantly, although animals drank more saccharin in the home cage than in the experimental cage, and more after a 21-day delay than a 1-day delay, there was no significant interaction with the Exposure variable. These results indicate the expected habituation of neophobia. As shown by the significant main effect of exposure in the test stage, a neophobic response was present on the first exposure trial. However, the results are different from those predicted from associative learning models of habituation (e.g. Wagner, 1981). Thus, group EX/HOM/21, which spent the delay in the same context where pre-exposure took place, consumed a similar amount of saccharin on the test trial as group EX/EXP/21, which spent the delay in a context different from exposure [F(1, 13) < 1]. From an associative view, post-habituation exposure to the context in the absence of saccharin should have resulted in extinction of the context–flavor association acquired in the exposure stage. As a result, a recovery of the habituated neophobia would be expected for the EX/HOM/21 group but not for the EX/EXP/21 group, a difference that was not obtained (also see Fig. 1), thereby suggesting that super-LI is not affected by factors related to the modulation of neophobia.
2. Experiment 2 The same design used to assess the effects of retention intervals and delay context on the recovery of habituated neophobia was used to evaluate the modulation of conditioning strength. In the present experiment, stage 1 consisted of a single CS–US pairing (saccharin–LiCl) instead of the CS-nothing presentations. A number of studies have reported that CTA is stronger after long than short post-conditioning delays, a phenomenon that has been labeled the RIE (e.g. Batsell and Best, 1992a,b, 1993, 1994; Batsell and Pritchett, 1995), and which is independent of a reinstatement of neophobia (e.g. Batsell and Best, 1992a,b). Although the size of the effect does not increase beyond the first few days of delay (Batsell and Best, 1992b), RIE has been demonstrated with
intervals ranging from 3 to 21 days (Batsell and Best, 1993, 1994; Biederman et al., 1974). However, a number of studies have not found potentiation of conditioned aversion with long delays (Dragoin et al., 1973; Klein et al., 1977; Steinert et al., 1980). This also is the case in many studies that have RIE-relevant groups that serve as controls in LI experiments (e.g. Aguado et al., 1994; Bakner et al., 1991; Rosas and Bouton, 1996, Experiment 3). In our own studies (De la Casa and Lubow, 2000, 2002; Lubow and De la Casa, 2002), with delays of 1 and 21 days, we typically find that the long delay control (NPE) group exhibits greater CTA than the short-delay control group, but not significantly. The only obvious difference between groups in the Batsell and Best RIE experiments and the NPE groups in the LI experiments is that the NPE groups, unlike the RIE groups, are pre-exposed to the conditioning context. However, for CTA, the distinction between apparatus pre-exposure and non-pre-exposure would appear to be nominal since all procedures usually are carried out in the home cage. In short, we are unable to account for the absence of RIE in the NPE groups in LI studies with long delays. Nevertheless, if we accept that RIE is a valid reflection of an increase in conditioning performance after a long compared to a short post-conditioning delay, then we must also note that, with one exception, the experiments that reported RIE were conducted such that all stages, conditioning, interval, and test, were in the home cages. Batsell and Best (1992a, Experiment 6) specifically compared the effects of retention interval (1 and 6 days) when the intervals were spent in contexts different than or the same as the other experimental stages. RIE was present in the latter, but not in the former, condition. To confirm this latter finding, but using the parameter values with which we have produced super-LI and failed to produce significant RIE, we conducted an experiment that examined the effects of retention interval and retention interval context on the modulation of CTA. A summary of the procedure and 2 × 2 design is provided in Table 1. Consumption of saccharin solution was paired with the US (LiCl), following which animals were tested after either a 1- or 21-day delay. For half of the animals all of the treatments (conditioning, delay, and test) were conducted in the home cage (HOM). For the other half,
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conditioning and test were conducted in a chamber that was different from the home cage (EXP), and the delay was spent in the home cage.
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experimental session, animals had access to water in the home cage for 25 min. 2.2. Results and discussion
2.1. Method 2.1.1. Subjects Forty-eight male adult Wistar rats (n = 12 per group) participated in this experiment (mean weight 392 g, range 332–448 g). The animals were fed and housed as described in Experiment 1. 2.1.2. Apparatus As described in Experiment 1, for those animals in the home cage condition all experimental manipulations were conducted in the home cages. For those animals in the experimental cage condition, conditioning and testing were conducted in experimental chambers located in an isolated room, but the delay was spent in the home cages. Apparatus and fluids were the same as those described in Experiment 1. For the conditioning trial, each animal was injected (i.p.) with a 0.4 M LiCl solution (0.5% body weight). 2.1.3. Procedure After 7 days on a 23.5 h water-deprivation schedule, the conditioning trial was presented. For half of the animals, all experimental manipulations took place in the home cages (HOM condition); for the other half, conditioning and testing were conducted in experimental chambers located in an isolated room, but the delay was spent in the home cage (EXP condition). During this phase, all animals had access to the saccharin solution for a single trial (5 min). Immediately after saccharin consumption, LiCl was injected. The test phase was similar for all animals. Each subject was given access to the saccharin solution for 5 min on each of six successive days. This phase was initiated one day after conditioning for half of the animals (1-day condition) and 21 days after conditioning for the other half (21-day condition). To equate deprivation level at the time of testing for both delay conditions, animals in the 21-day condition received ad libitum water from days 9 to 20. The first test trial for those animals in the 21-day delay condition was conducted on day 29. All fluid consumptions during experimental sessions were recorded. As in Experiment 1, after completing each
2.2.1. Conditioning trial The mean amount of saccharin solution consumed by the animals in the HOM and EXP conditions was 9.10 (S.D. = 2.73) and 7.98 (S.D. = 1.51), respectively, a difference that was very similar to that obtained on the first pre-exposure trial of Experiment 1. However, the difference was not significant [F(1, 46) = 3.03, P > 0.08]. 2.2.2. Test phase Fig. 2 shows mean saccharin consumption across the six extinction trials for the four groups. As can be seen, there were main effects of Delay and Context, and interactions of both variables with trials. The mean amount of saccharin solution consumed on test days was subjected to a 2 × 2 × 6 mixed ANCOVA (Delay, Context of treatment, and Trials), with amount of saccharin consumed on the conditioning trial as a covariate. There was a significant main effect of Context of delay [F(1, 43) = 17.42, P < 0.001], with the HOM cage groups drinking more saccharin than the EXP cage groups (5.40 ml, S.D. = 2.47 and 3.06 ml, S.D. = 1.51, respectively). The main effect of Delay also was significant [F(1, 43) = 8.61, P < 0.01], with the 1-day groups drinking more than the 21-day groups (5.02 ml, S.D. = 2.38 and 3.36 ml, S.D. = 2.00, respectively). The Context × Delay interaction was not significant [F(1, 43) < 1]. The main effect of Trials was significant [F(5, 215) = 140.9, P < 0.001]. Extinction was faster for the 1-day delay groups than for the 21-day delay groups. In addition, irrespective of Delay, extinction was faster for the HOM groups than for the EXP groups. These observations were supported by significant Trials × Delay and Trials × Context interactions [F(5, 215) = 4.14, P < 0.001 and F(5, 215) = 7.67, P < 0.001, respectively]. The three-way interaction was not significant [F(5, 215) < 1]. In summary, Experiment 2 produced a strong RIE, with CTA being stronger after a 21-day delay than a 1-day delay. Furthermore, CTA was stronger when the conditioning and test stages were conducted in a context other than the delay context (home cage) as
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Fig. 2. Mean amount of saccharin solution consumed in the test stage as a function of delay between conditioning and test stages (1 and 21 days) and context of treatment (HOMe cages and EXPerimental cages). Error bars represent S.E.M.s.
compared to when all stages, including delay, were in the same context (home cage). Nevertheless, as indicated by the absence of a significant Delay × Context interaction, the RIE was not affected by the different context conditions. Although many studies have reported RIE when all the experimental stages, including the delay period, were conducted in the home cage (e.g. Batsell and Best, 1992a,b, 1994), there have been a number of failures to produce RIE when the delay context was different from that of conditioning/test (Batsell and Best, 1992a, Experiment 6; Kraemer et al., 1988; Miller et al., 1990, Experiment 1; Steinert et al., 1980). The present study is the first to demonstrate that RIE survives such a manipulation. Fig. 2 suggests that the discrepancy between the results of the present study and those that failed to produce RIE may be due to differences in the number of test trials. As can be seen, RIE develops more rapidly in the HOM group than the EXP group. Indeed, there does not appear to be any evidence for RIE in the HOM group until trial 3. It is therefore noteworthy that the two studies with the same delays as the present one, namely 1 and 21 days, that failed to obtain RIE, used only one 30-min test trial (Kraemer et al., 1988; Miller et al., 1990).
3. General discussion The reported experiments clearly demonstrate the relevance of retention interval and context in which the experimental treatment is conducted for neophobia and conditioning. Specifically, Experiment 1 revealed, not surprisingly, that when a flavored solution is presented in a familiar context (home cage) consumption is higher than when it is presented in a non-familiar context (experimental cages). Relatedly, Honey et al.8 1992) reported that intake of a novel liquid increased with number of presentations, but fell when afterwards it was presented in a different context. This decline in consumption did not occur when the test context was familiarized independently of the flavor presentations. In addition, in our Experiment 1, when a long delay was introduced between flavor exposure and test, there was an increase in saccharin consumption, reflecting attenuation of the neophobic response as opposed to its recovery (for similar results, see Bonardi et al., 1991; Green and Parker, 1975). Experiment 2 revealed a RIE for conditioning that was opposite to that found for neophobia: flavored fluid consumption decreased (i.e. an increase in conditioning) when the test was conducted 21 days after
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conditioning as compared to 1 day after conditioning. This RIE was evident in both home cage and experimental cage conditions. Furthermore, extinction proceeded faster for those groups conditioned and tested in a familiar home cage than for those conditioned and tested in the unfamiliar experimental cage. 3.1. Effects of retention interval The effects of retention intervals interpolated between various procedural stages of a variety of paradigms have become the subject of much theoretical interest, as seen in studies of extinction (e.g. Brooks and Bouton, 1993), counter-conditioning (e.g. Bouton and Peck, 1992), and LI (e.g. Aguado et al., 1994, 2001; De la Casa and Lubow, 2000, 2002). To explain these effects, Bouton (1993; Bouton et al., 1999) has proposed that extended passages of time result in, or are equivalent to, a context change. Lubow and De la Casa (2002) have suggested that such delay-induced changes specifically modulate the recovery of first associations (see below). If one accepts that elicitation of a habituated response in a particular context depends on the prior formation of a stimulus–context association in that same context (Wagner, 1979), then a time-induced context change between exposure and test also would result in the recovery of the neophobia that otherwise would have appeared as habituated. On the other hand, a context change should not affect CTA, since an excitatory conditioned response is relatively context-independent (e.g. Bouton, 1994). Clearly, our results do not support these hypotheses. Increases in retention interval reduced neophobic response and increased CTA. However, there is a potentially important difference between the procedures described in the present study and those usually employed to analyze Retention interval effects in extinction, counter-conditioning, and LI experiments. The latter typically require three stages, with the retention interval introduced between the second and test stages. The neophobia and conditioning experiments of the present study consisted of two phases, with the retention interval interpolated between the first and test stages. As a consequence, the two sets of procedures differ in terms of the number of hypothetical associations that are acquired before the test (one association for neophobia and simple
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conditioning, and two associations for extinction, counter-conditioning, and LI). Recently, we have proposed that long as compared to short retention intervals potentiate proactive interference, that is, the association that was acquired first gains in strength relative to the second association as the interval increases (Lubow and De la Casa, 2002). Specifically, the effects of a retention interval would critically depend on the acquisition of two or more sequentially learned associations in the same context. Under these circumstances, linking the same contextual cues to the memories of the two (or more) conditioning episodes (Bouton, 1993) provides the basis for interference effects, with an increase in retention interval potentiating the contribution of the first-learned association. In the present experiments, in spite of the absence of significant interactions with context of delay, the passage of time by itself potently affected behavior. The neophobic response was significantly less after the 21-day as compared to the 1-day retention interval. The decline in neophobia with time has an adaptive advantage. After flavor consumption, long intervals without an aversive consequence would signify increased certainty as to the safety of that flavor. This “learned safety” proposal (Kalat and Rozin, 1973) would be fully compatible with the habituation of neophobia observed in the 1-day group and the reduction in neophobia after 21 days in Experiment 1. Whether this effect is long-lasting, or restricted to relatively short intervals remains an open question. Although a decrease of the neophobic response has been obtained after a 24 h retention interval (Bonardi et al., 1991; Green and Parker, 1975) but not after 30 days (Domjan, 1977), the potentiating effect of a retention interval on the expression of CTA has not been consistently obtained (Batsell and Best, 1992a,b, 1993, 1994; Batsell and Pritchett, 1995; Dragoin et al., 1973; Klein et al., 1977; Steinert et al., 1980). On the basis of the Rescorla–Wagner model (1972), one might expect a Retention interval × Context interaction in Experiment 2, with RIE in the EXP condition but not in the HOM condition, due to extinction of the Context–US association during the long delay in the HOM condition (with animals spending the delay in the same context as conditioning) but not in the EXP condition (with animals spending the delay in a different context from conditioning). However, we
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obtained RIE in both HOM and EXP conditions, thereby not supporting the Rescorla–Wagner hypothesis. Our results are compatible with the retrieval disruption hypothesis of RIE. As proposed by Batsell and Best (1994), the reduced conditioning observed after a short delay is the result of a retrieval failure produced by the non-associative changes generated by a recent surprising US. If time-induced changes in conditioned response magnitude are produced by non-associative post-US effects (Batson and Best, 1982), then RIE should not be affected by the context of delay. 3.2. Effects of context of treatment The role of context in habituation has been amply recognized (e.g. Honey et al., 1992). From an associative point of view, habituation depends on the capacity of the context to elicit a representation of the stimulus in short-term memory (Wagner, 1979). Thus, the first time the stimulus is presented it is actively processed and it evokes the corresponding orienting/neophobic response. However, after repeated stimulus presentations in a particular context, that context acquires the capacity to retrieve the stimulus representation from long-term memory, thereby preventing active processing and reducing orienting/neophobic responses. However, the results of Experiment 1 are consistent with a non-associative model of habituation, one that proposes that the response decrement is generated to all elements of the the training situation. From this view, the greater the exposure to the complex stimulus (context plus stimulus), the greater the response decrement (Korn and Moyer, 1966; Marlin and Miller, 1981). In our design, the novelty of the experimental context would have contributed to the reduction in saccharin consumption observed in the EXP condition. Similarly, exposure to the saccharin flavor would result in increased consumption at testing as compared to NPE groups. Thus, neophobia would be the result of a summation of stimulus and context novelty, with novel/novel producing the highest levels of neophobia and familiar/familiar the lowest levels. The effects of place of conditioning and testing in CTA procedures has received little attention in previous research. To the best of our knowledge, only one study has examined the effects of Home versus Experimental contexts on simple CTA. Swank (2000) reported a trend towards greater aversion when the con-
ditioning episode was conducted in a novel context as compared with a familiar home context. Similarly, we found that conditioning was stronger when the CS–US pairing occurred in the experimental/unfamiliar context than in the home/familiar context. In summary, our results indicate that a set of conditions traditionally ignored in CTA and flavor neophobia procedures play an important role in determining consummatory behavior and learning. The place of the experimental treatment (home versus experimental cages) and the interval between the conditioning and testing episodes are variables that unmistakably modulate learning/expression of flavor–consequence and flavor–no consequence associations. The independent effects of place of exposure/conditioning and delay on neophobia and CTA, and the fact that they do not interact, have implications for the understanding of both phenomena, and for developing an explanation of the super-LI effect. It appears that one can reject explanations of the super-LI effect (De la Casa and Lubow, 2000, 2002; Lubow and De la Casa, 2002) based on either the interaction of passage of time and place of training on neophobia or on CTA. The absence of a Retention interval × Place interactions in Experiments 1 and 2 suggests that the direction of modulated LI with the passage of time, super- or attenuated LI, is the result of a triple interaction between two conflicting associations, training context and retention interval, the exact nature of which remains to be revealed.
Acknowledgements This research was supported by DGES (Spanish government) BSO2000-0323-C02-01 and BSO200201136 grants. References Aguado, L., Symonds, M., Hall, G., 1994. Interval between preexposure and test determines the magnitude of latent inhibition: implications for an interference account. Anim. Learn. Behav. 22, 188–194. Aguado, L., de Brugada, I., Hall, G., 2001. Tests for inhibition after extinction of a conditioned stimulus in the flavour aversion procedure. Q. J. Exp. Psychol. 54B, 201–217. Bakner, L., Strohen, K., Nordeen, M., Riccio, D.C., 1991. Postconditioning recovery from the latent inhibition effect in conditioned taste aversion. Physiol. Behav. 50, 1269–1272.
L.G. De la Casa et al. / Behavioural Processes 63 (2003) 159–170 Batsell, W.R., Best, M.R., 1992a. Variations in the retention of taste aversions: evidence for retrieval competition. Anim. Learn. Behav. 20, 146–159. Batsell, W.R., Best, M.R., 1992b. Investigation of replacement fluids and retention-interval effects in taste-aversion learning. Bull. Psychon. Soc. 30, 414–416. Batsell, W.R., Best, M.R., 1993. One bottle too many? Method of testing determines the detection of overshadowing and retention of taste aversions. Anim. Learn. Behav. 21, 154–158. Batsell, W.R., Best, M.R., 1994. The role of US novelty in retention interval effect in single-element taste-aversion learning. Anim. Learn. Behav. 22, 332–340. Batsell, W.R., Pritchett, K.P., 1995. Retention of rotationally induced taste aversions. Physiol. Behav. 58, 815–818. Best, M.R., Domjan, M., Haskins, W.L., 1978. Long-term retention of flavor familiarization: effects of number and amount of prior exposures. Behav. Neural Biol. 23, 95–99. Biederman, G.B., Milgram, N.W., Heighington, G.A., Stockman, S.M., O’Neill, W., 1974. Memory of conditioned food aversion follows a U-shape function in rats. Q. J. Exp. Psychol. 26, 610–615. Bonardi, C., Guthrie, D., Hall, G., 1991. The effect of a retention interval on habituation of the neophobic response. Anim. Learn. Behav. 19, 11–17. Bond, N.W., Westbrook, R.F., 1982. The role of amount consumed in flavor preexposure effects and neophobia. Anim. Learn. Behav. 10, 511–515. Bouton, M.E., 1993. Context, time, and memory retrieval in the interference paradigms of Pavlovian learning. Psychol. Bull. 114, 80–99. Bouton, M.E., 1994. Conditioning, remembering, and forgetting. J. Exp. Psychol. Anim. Behav. Process. 20, 219–231. Bouton, M.E., Peck, C.A., 1992. Spontaneous recovery in cross-motivational transfer (counterconditioning). Anim. Learn. Behav. 20, 313–321. Bouton, M.E., Nelson, J.B., Rosas, J.M., 1999. Stimulus generalization, context change, and forgetting. Psychol. Bull. 125, 171–186. Brooks, D.C., Bouton, M.E., 1993. A retrieval cue for extinction attenuates spontaneous recovery. J. Exp. Psychol. Anim. Behav. Process. 19, 77–89. De la Casa, L.G., Lubow, R.E., 2000. Super-latent inhibition with conditioned taste aversion testing. Anim. Learn. Behav. 28, 389–399. De la Casa, L.G., Lubow, R.E., 2002. An empirical analysis of the super-latent inhibition effect. Anim. Learn. Behav. 30, 112–120. Domjan, M., 1976. Determinants of the enhancement of flavored water intake by prior exposure. J. Exp. Psychol. Anim. Behav. Process. 2, 17–27. Domjan, M., 1977. Attenuation and enhancement of neophobia for edible substances. In: Barker, L.M., Best, M.R., Domjan, M. (Eds.), Learning Mechanisms in Food Selection. Baylor University Press, Waco, TX, pp. 151–179. Dragoin, W., Hughes, G., Devine, M., Bentley, J., 1973. Long-term retention of conditioned taste aversions: effects of gustatory interference. Psychol. Rep. 33, 511–514. Green, K.F., Parker, L.A., 1975. Gustatory memory: incubation and interference. Behav. Biol. 13, 359–367.
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Harding, G.B., Rundle, G.R., 1969. Long-term retention of modality- and nonmodality-specific habituation of the GSR. J. Exp. Psychol. 82, 390–392. Honey, R.C., Pye, C., Lightbown, Y., Rey, V., Hall, G., 1992. Contextual factors in neophobia and its habituation: the role of absolute and relative novelty. Q. J. Exp. Psychol. 45B, 327–347. Ishii, K., Yamada, Y., Hishimura, Y., Haga, Y., 2002. The effects of preexposure-test and conditioning-test intervals on the magnitude of latent inhibition. Jpn. Psychol. Res. 44, 51–56. Kalat, J.W., Rozin, P., 1973. “Learned safety” as a mechanism in long-delay taste-aversion learning in rats. J. Comp. Physiol. Psychol. 83, 198–207. Kasprow, W.J., Schachtman, T.R., 1993. Differential effects of distractor stimuli and the interval between flavor exposures on neophobia and latent inhibition. Psychol. Rec. 43, 25–37. Kaye, H., Gambini, B., Mackintosh, N.J., 1988. A dissociation between one-trial overshadowing and the effect of a distractor on habituation. Q. J. Exp. Psychol. 40B, 31–47. Klein, S.B., Mikulka, P.J., Domato, G.C., Hallstead, C., 1977. Retention of internal experiences in juvenile and adult rats. Physiol. Psychol. 5, 63–66. Klosterhalfen, S.Y., Klosterhalfen, W., 1985. Conditioned taste aversion and traditional learning. Psychol. Res. 47, 71–94. Korn, J.H., Moyer, K.E., 1966. Habituation of the startle response and of heart rate in the rat. Can. J. Psychol. 20, 183–190. Kraemer, P.J., Roberts, W.A., 1984. The influence of flavor preexposure and test interval on conditioned taste aversion in the rat. Learn. Motiv. 15, 259–278. Kraemer, P.J., Lariviere, N.A., Spear, N.E., 1988. Expression of a taste aversion conditioned with an odor-taste compound: overshadowing is relatively weak in weanlings and decreases over a retention interval in adults. Anim. Learn. Behav. 16, 164–168. Leaton, R.N., 1974. Long-term retention of the habituation of lick suppression in rats. J. Comp. Physiol. Psychol. 87, 1157–1164. Lubow, R.E., De la Casa, L.G., 2002. Super-latent inhibition and spontaneous recovery: differential effects of pre- and post-conditioning CS-alone presentations after long delays in different contexts. Anim. Learn. Behav. 30, 376–386. Marlin, N.A., Miller, R.R., 1981. Associations to contextual stimuli as a determinant of long-term habituation. J. Exp. Psychol. Anim. Behav. Process. 7, 313–333. Miller, R.R., Kasprow, W.J., Schachtman, T.R., 1986. Retrieval variability: sources and consequences. Am. J. Psychol. 99, 145– 218. Miller, J.S., Jagielo, J.A., Spear, N.E., 1990. Alleviation of short-term forgetting: effects of the CS and other conditioning elements in prior cueing or as context during test. Learn. Motiv. 21, 96–109. Rescorla, R.A., Wagner, A.R., 1972. A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. In: Black, A.H., Prokasy, W.F. (Eds.), Classical Conditioning: II. Current Research and Theory. Appleton-Century-Crofts, New York, pp. 64–99. Rosas, J.M., Bouton, M.E., 1996. Spontaneous recovery after extinction of a conditioned taste aversion. Anim. Learn. Behav. 24, 341–348.
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Effects of post-treatment retention interval and context on neophobia and conditioned taste aversion夽 L.G. De la Casa a,∗ , E. Diaz a , R.E. Lubow b a
Department of Experimental Psychology, Faculty of Psychology, University of Seville, C Camilo Jose Cela sn, Sevilla 41018, Spain b Department of Psychology, Tel-Aviv University, Tel Aviv, Israel Received 6 March 2003; received in revised form 21 April 2003; accepted 22 April 2003
Abstract We have repeatedly observed that a delay between acquisition and test, and the nature of the context in which the delay is spent, modulates latent inhibition (LI) of conditioned taste aversion (CTA; e.g. [Anim. Learn. Behav. 28 (2000) 389; Anim. Learn. Behav. 30 (2002) 112]). The present paper analysed the effects of delayed testing and treatment context after flavor exposure on the recovery of neophobia (Experiment 1) and on extinction after simple conditioning (Experiment 2). Two experiments were conducted with the same factorial design (2 × 2: 1 day versus 21 days of delay between first and second stage, and home versus experimental cages as place of experimental treatment). There were independent effects of both variables on habituation of neophobia and conditioning strength as measured on extinction trials. The long delay produced a reduction of neophobia (Experiment 1) and an increase in conditioning (Experiment 2). In addition, more of the flavored solution was consumed when the experimental treatment was conducted in the home cage than in the experimental cage (Experiment 1), and there was stronger conditioning when the delay period took place in the experimental cages than in the home cages (Experiment 2). The implications of these results for LI, as well as their relevance for experiments that use the CTA paradigm, are discussed. © 2003 Elsevier Science B.V. All rights reserved. Keywords: Neophobia; Conditioned taste aversion; Retention interval; Latent inhibition; Habituation
Conditioned taste aversion (CTA) has proven to be a popular and useful tool for studying associative learning. Although there have been debates as to whether CTA represents normative classical conditioning, primarily because it alone tolerates long intervals between CS and US, there are also certain procedural idiosyncrasies that warrant examination (e.g. see Klosterhalfen and Klosterhalfen, 1985). 夽 Part of this paper was presented at the XIV Congress of the Spanish Society of Comparative Psychology (Seville, Spain, September 2002). ∗ Corresponding author. Tel.: +34-9-545-576-82; fax: +34-9-545-517-84. E-mail address: [email protected] (L.G. De la Casa).
For example, CTA and other flavor-based experiments, with the exception of those in which context is a variable, almost always are conducted entirely in the home cage (excluding the brief period in which the animals are removed for the purpose of administering the US). This, of course, is a result of the fact that most of the experimental manipulations, and the testing of their effects, are easily accomplished within the confines of the home environment, a situation that is very different from other preparations, in which special apparatus is required to administer the protocol. The possible consequences of such differences are particularly apparent in studies that are designed to study the effects of retention interval, a topic that
0376-6357/03/$ – see front matter © 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0376-6357(03)00080-9
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has received much attention, particularly in regard to retrieval theories of latent inhibition (LI) and extinction (e.g. Bouton, 1993; Bouton et al., 1999; Miller et al., 1986). We have recently shown, as described below, that the relationship of the context in which the animal spends the retention interval to those contexts in which the other phases of the experiment are conducted, such as stimulus pre-exposure, conditioning, extinction, and testing, has profound effects on test phase performance. A number of studies have reported that LI of CTA is attenuated when a long delay is introduced between the conditioning and test sessions (Aguado et al., 1994, Experiment 1; Aguado et al., 2001, Experiment 2; Bakner et al., 1991, Experiment 2; Ishii et al., 2002, Experiments 1 and 2). In these studies, the experimental manipulations, including the delay periods, were conducted in the animals’ home cages. However, when the pre-exposure, conditioning and test stages of an LI experiment are conducted in a context that is different from that of the home cage, and the delay is spent in the home cage, then, instead of attenuated LI, there is a super-LI effect (De la Casa and Lubow, 2000, 2002; Lubow and De la Casa, 2002). One explanation for these apparently contradictory results appeals to the preservation or extinction of a hypothetical context–[CS-nothing] association that is established during the pre-exposure stage. Specifically, during the course of pre-exposures to the flavor, an association is formed between the flavor and the absence of a consequence. Furthermore, this association is specific to the context in which pre-exposure is conducted. At the time of test, if the test context is the same as the stimulus pre-exposure context, then this association is retrieved, resulting in higher levels of flavored fluid consumption than in a control group conditioned without previous exposure to the flavor (i.e. LI). However, when a long delay is introduced between conditioning and test stages, the test context either maintains or loses its capacity to elicit the context–[CS-nothing] association, depending on whether the delay takes place in a different or same context from pre-exposure and conditioning (De la Casa and Lubow, 2000, 2002). When the interval context is the “same,” the higher order association is extinguished, and LI is attenuated (e.g. Aguado et al., 1994, 2001). When the interval context is “different,” the context–[CS-nothing] association is protected from extinction.
Given that the direction of the delay-induced LI effects are critically dependent on the relationship of delay context to those of the other experimental stages, the question arises as to whether other CTA and related taste-aversion effects may not also be affected by this long-ignored procedural variable. In this regard, two classes of experimental phenomena are of particular interest, both in their own right and as a means to understand the processes that modulate LI: the recovery of habituated neophobia (e.g. Aguado et al., 1994; Best et al., 1978) and the retention interval effect (RIE; e.g. Batsell and Best, 1992a,b). The former refers to the delay-induced recovery of a habituated avoidance response to a novel flavor, and the latter to a delay-induced increase in conditioned aversion to a flavor. In both cases, the relationship of the delay context to that of the preceding treatment context and to the subsequent testing context has important theoretical consequences, both for theories that claim that retention interval and context change effects are additive (e.g. Bouton et al., 1999) and for theories that account for certain learning effects on the basis of associations between the nominal target stimulus and the context (e.g. Wagner, 1981). In summary, experiments that use flavored fluids or foods as stimuli are typically conducted entirely in the home cage. Thus, when there is a manipulation of a retention interval, the interval is spent in the same context as the other stages. In other preparations, as for example conditioned suppression, the CS and US must be administered outside the home cage. Thus, the delay interval is spent in a context that is different from that of the other stages. In previous CTA experiments, we have shown that the direction and magnitude of LI and spontaneous recovery are dependent on the relationship between the interval context and the remaining treatment contexts. This relationship may well influence other flavor-based delay-induced effects. Indeed, there is some independent evidence concerning the roles of context and delay on habituation of neophobia (e.g. Bonardi et al., 1991; Honey et al., 1992), and on CTA (e.g. Batsell and Best, 1994; Swank, 2000). However, the interaction between the context and delay variables, already shown to be critical for predicting the direction of LI effects, has not been explored for habituation of neophobia and CTA. The present paper addresses this issue.
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1. Experiment 1 Habituation is usually defined as the waning of a stimulus-induced response as a consequence of repeated presentations of that stimulus, at least when such reduction cannot be accounted for by simple fatigue or sensory adaptation (Thompson and Spencer, 1966). Importantly, there is a distinction between short- and long-term habituation (e.g. Sharpless and Jasper, 1956). The latter has been frequently treated as an example of learning. Of particular interest has been the claim that long-term habituation is based on the acquisition of stimulus–context associations (Wagner, 1979; but see Marlin and Miller, 1981). Irrespective of any specific theory of habituation, the fact that it may survive retention intervals in the order of weeks (e.g. Harding and Rundle, 1969; Leaton, 1974) would, indeed, support a learning interpretation. The relationship between retention intervals and the context in which they occur has played an important role in testing Wagner’s model of associative learning as applied to long-term habituation. If such habituation depends on the formation of stimulus–context associations, then exposing the animal to the context after the repeated stimulus presentations in that same context should result in extinction of the stimulus–context association, and therefore it should interfere with the expression of the habituated response. On the other hand, if the intervals are spent in a different context from that in which the repeated stimulus presentations occurred, then habituation should be intact, or at least not as attenuated as in the same context condition. The delayed-testing procedure as applied to habituation of taste aversion usually focuses on neophobia. It is well documented that upon first presentation of a novel flavor, the rat, and other omnivores, will drink or eat considerably less than on subsequent presentations of the same flavor (e.g. Domjan, 1976; Siegel, 1974). The difference in the amount of the novel flavor consumed on the first trial and the amount consumed on the trial at which asymptotic consumption is reached defines the magnitude of the neophobic response. By interpolating a delay interval between the last trial of the exposure stage and a test trial, one can assess the effects of time on the habituated neophobic response. In general, an increase in the retention interval, at least up to 24 h, reduces neophobia (e.g. Bonardi et al., 1991; Bond and Westbrook, 1982; Green and Parker,
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1975; but see Kasprow and Schachtman, 1993). However, the present paper focuses on relatively long retention intervals, primarily because most studies of the effects of retention interval on LI, extinction, and recovery from extinction use long intervals, and our aim is to develop a common theoretical framework for these disparate experimental paradigms. A number of studies have indicated that the length of the delay period between exposure and test does not affect recovery of the habituated neophobic response. This appears to be true when the exposure, delay, and test phases are all conducted in the same context (Aguado et al., 1994, Experiment 2; Kaye et al., 1988, Experiments 1–3; Kraemer and Roberts, 1984, Experiments 3 and 4; Siegel, 1974), as well as when the delay context is different from that of the other stages (Best et al., 1978; Miller et al., 1990, Experiment 1; Steinert et al., 1980). We choose to continue this line of investigation with the same exact parameter values that we have used to modulate delay-induced LI, producing attenuated LI when the retention interval context was identical to the pre-exposure, acquisition, and testing contexts, and super-LI when the retention interval context was different from the other contexts. Thus, the main aim of Experiment 1 was to examine the effects of delayed testing (1 day versus 21 days) and place of experimental treatment (home cages versus experimental cages) on the habituation and recovery of neophobia. To this end, after four trials of mere exposure to a saccharin solution, intended to obtain habituation of neophobia, a test trial was conducted 1 or 21 days after exposure. For half of the animals, all experimental treatments were conducted in a familiar context (home cages). For the other half, all experimental treatments, except for the delay, were conducted in a different, non-familiar context (experimental cages).1 The experimental design is summarized in Table 1. We predicted an Exposure × Delay × Context interaction. The stimulus exposed group that 1 The context manipulation confounds familiar/non-familiar with home/experimental cages. Elsewhere, we have presented the rationale for the contention that the critical element for producing super-LI is the uniqueness of the delay context relative to the training contexts, and not its familiarity (Lubow and De la Casa, 2002). We chose the same procedure here in order to reproduce the conditions that produced the super-LI effect in previous experiments (De la Casa and Lubow, 2000, 2002; Lubow and De la Casa, 2002).
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Table 1 Designs for Experiment 1 (upper section) and Experiment 2 (lower section) Group
Place
Exposure
Conditioning
Delay (days)
Test
Experiment 1 EX/HOME/1 EX/EXP/1 EX/HOME/21 EX/EXP/21 NEX/HOME/1 NEX/EXP/1 NEX/HOME/21 NEX/EXP/21
Home Exp. Home Exp. Home Exp. Home Exp.
Sacch Sacch Sacch Sacch Water Water Water Water
– – – – – – – –
1 1 21 21 1 1 21 21
Sacch Sacch Sacch Sacch Sacch Sacch Sacch Sacch
Experiment 2 HOME/1 EXP/1 HOME/21 EXP/21
Home Exp. Home Exp.
– – – –
Sacch–US Sacch–US Sacch–US Sacch–US
1 1 21 21
Sacch Sacch Sacch Sacch
Abbreviations: home, home cages; exp., experimental cages; and sacch, saccharine
spent the delay in the same context where the experimental treatment was conducted should show recovery of neophobia, thus drinking less of the flavored solution, due to extinction of the context–flavor association (Wagner, 1981), as compared to the group in which the delay context was different from the treatment context, which should show a decrease of the neophobic response after the delay (e.g. Bonardi et al., 1991). This prediction relates to the super-LI effect (e.g. De la Casa and Lubow, 2000), because the enhancement of LI that is observed after a delay that is spent in a context different than the context of the experimental treatment could be mediated, at least in part, by the expected decrease in the neophobic response. 1.1. Method 1.1.1. Subjects Fifty-six male adult Wistar rats (n = 7 per group) participated in the experiment (mean weight 329 g, range 302–383 g). The animals were individually housed in 40 cm×20 cm×24 cm Plexiglas cages, with wood shavings as bedding, on a 12:12 h light:dark cycle. Standard rat food was continuously available. Tap water was supplied from bottles with stainless steel spouts. 1.1.2. Apparatus For animals in the experimental cage condition, exposure and test were conducted in an isolated room,
different from the colony room. For all sessions in this condition, animals were transported to the experimental room and placed in individual 30 cm × 18 cm × 18 cm Plexiglas cages, with wood shavings as bedding, where exposure and test trials took place. For those animals in the home cage condition, all experimental manipulations were conducted in the home cages. All liquid rations were provided at room temperature in 150-ml graduated plastic bottles, fitted with stainless steel spouts, similar to those used for normal rations. The bottles were attached to the fronts of the cages during liquid presentations. The amount of fluid consumed was calculated as the difference between bottle weight before and after each liquid presentation. The fluids during the pre-exposure session were a 0.04% sodium saccharin solution for the Exposed subjects, and tap water for the Non-exposed subjects. 1.1.3. Procedure After 7 days on a 23.5 h water-deprivation schedule, the exposure phase was initiated. For half of the animals, all experimental manipulations were conducted in the home cages (HOM condition); for the other half, exposure and test were conducted in the experimental cages, but the delay was spent in the home cage (EXP condition). During this phase, half of the animals had access to the saccharin solution for 4 days, 5 min per day (EX condition). The remaining animals consumed water for the same period (NEX condition). On each of the exposure days, the 5 min availability of liquid was
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followed immediately by 25 min of water to complete the daily 30 min ration. The test phase, similar for all animals, consisted of a single 5 min exposure of saccharin. This phase was initiated 1 day after exposure for half of the animals (1-day condition) and 21 days after exposure for the other half (21-day condition). To equate deprivation levels at the time of testing for both delay conditions, animals in the 21-day condition received ad libitum water from days 13 to 20. On day 21, the water-deprivation schedule was reinstated. Test trials for animals in the 21 day of delay condition were conducted on day 32. Fluid consumption during all experimental sessions was computed. 1.2. Results and discussion 1.2.1. Pre-exposure phase A 2 × 2 × 4 mixed ANOVA (Exposure, Context, and Trials) was conducted on mean amount of fluid consumed by the four groups. There was a significant main effect of Context [F(1, 52) = 15.93, P < 0.001], with subjects exposed in the home cages drinking more than those exposed in the experimental cages (9.84 ml, S.D. = 1.42 and 8.37 ml, S.D. = 1.32, respectively). The main effect of Exposure (saccharin versus water) and the Context × Exposure interaction were not significant (Ps > 0.75). For the within-subject analyses, there was a significant effect of Trials [F(3, 156) =
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9.38, P < 0.001], with fluid consumption increasing across trials. The Trials × Context and Trials × Exposure interactions were significant [F(3, 156) = 2.94, P < 0.05, and F(3, 156) = 2.73, P < 0.05]. The Trials×Context interaction reflects an increase of fluid consumption across trials for subjects in the home cages, but not for those in the experimental cages. The Trials × Exposure interaction reflects the expected increase in saccharin consumption across trials (habituation of neophobia). The remaining interactions with Trials were not significant (Ps > 0.15). 1.2.2. Test phase Fig. 1 shows mean amount of saccharin consumed on the test day as a function of Exposure and Delay for those subjects in the home cage condition (Panel A) and the experimental cage condition (Panel B). As can be seen, EX groups consumed more saccharin solution than NEX groups; 21-day delay groups drank more than 1-day delay groups; and home cage groups drank more than experimental cage groups. These observations were confirmed by a 2 × 2 × 2 ANOVA (EX-NEX, Delay, and Context). The three between-group effects were significant [F(1, 48) = 8.76, P < 0.01; F(1, 48) = 4.38, P < 0.05; F(1, 48) = 14.05, P < 0.001, for Exposure, Delay and Context factors, respectively]. None of the interactions was significant (F s < 1).
Fig. 1. Mean amount of saccharin consumption as a function of delay between pre-exposure and test stages (1 and 21 days) on test trial for home cage condition and experimental cage condition. Error bars represent S.E.M.s.
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The fact that the NEX groups, which received saccharin for the first time in test, consumed less saccharin than the EX groups, which received saccharin for the fifth time, clearly revealed the neophobia effect. Importantly, although animals drank more saccharin in the home cage than in the experimental cage, and more after a 21-day delay than a 1-day delay, there was no significant interaction with the Exposure variable. These results indicate the expected habituation of neophobia. As shown by the significant main effect of exposure in the test stage, a neophobic response was present on the first exposure trial. However, the results are different from those predicted from associative learning models of habituation (e.g. Wagner, 1981). Thus, group EX/HOM/21, which spent the delay in the same context where pre-exposure took place, consumed a similar amount of saccharin on the test trial as group EX/EXP/21, which spent the delay in a context different from exposure [F(1, 13) < 1]. From an associative view, post-habituation exposure to the context in the absence of saccharin should have resulted in extinction of the context–flavor association acquired in the exposure stage. As a result, a recovery of the habituated neophobia would be expected for the EX/HOM/21 group but not for the EX/EXP/21 group, a difference that was not obtained (also see Fig. 1), thereby suggesting that super-LI is not affected by factors related to the modulation of neophobia.
2. Experiment 2 The same design used to assess the effects of retention intervals and delay context on the recovery of habituated neophobia was used to evaluate the modulation of conditioning strength. In the present experiment, stage 1 consisted of a single CS–US pairing (saccharin–LiCl) instead of the CS-nothing presentations. A number of studies have reported that CTA is stronger after long than short post-conditioning delays, a phenomenon that has been labeled the RIE (e.g. Batsell and Best, 1992a,b, 1993, 1994; Batsell and Pritchett, 1995), and which is independent of a reinstatement of neophobia (e.g. Batsell and Best, 1992a,b). Although the size of the effect does not increase beyond the first few days of delay (Batsell and Best, 1992b), RIE has been demonstrated with
intervals ranging from 3 to 21 days (Batsell and Best, 1993, 1994; Biederman et al., 1974). However, a number of studies have not found potentiation of conditioned aversion with long delays (Dragoin et al., 1973; Klein et al., 1977; Steinert et al., 1980). This also is the case in many studies that have RIE-relevant groups that serve as controls in LI experiments (e.g. Aguado et al., 1994; Bakner et al., 1991; Rosas and Bouton, 1996, Experiment 3). In our own studies (De la Casa and Lubow, 2000, 2002; Lubow and De la Casa, 2002), with delays of 1 and 21 days, we typically find that the long delay control (NPE) group exhibits greater CTA than the short-delay control group, but not significantly. The only obvious difference between groups in the Batsell and Best RIE experiments and the NPE groups in the LI experiments is that the NPE groups, unlike the RIE groups, are pre-exposed to the conditioning context. However, for CTA, the distinction between apparatus pre-exposure and non-pre-exposure would appear to be nominal since all procedures usually are carried out in the home cage. In short, we are unable to account for the absence of RIE in the NPE groups in LI studies with long delays. Nevertheless, if we accept that RIE is a valid reflection of an increase in conditioning performance after a long compared to a short post-conditioning delay, then we must also note that, with one exception, the experiments that reported RIE were conducted such that all stages, conditioning, interval, and test, were in the home cages. Batsell and Best (1992a, Experiment 6) specifically compared the effects of retention interval (1 and 6 days) when the intervals were spent in contexts different than or the same as the other experimental stages. RIE was present in the latter, but not in the former, condition. To confirm this latter finding, but using the parameter values with which we have produced super-LI and failed to produce significant RIE, we conducted an experiment that examined the effects of retention interval and retention interval context on the modulation of CTA. A summary of the procedure and 2 × 2 design is provided in Table 1. Consumption of saccharin solution was paired with the US (LiCl), following which animals were tested after either a 1- or 21-day delay. For half of the animals all of the treatments (conditioning, delay, and test) were conducted in the home cage (HOM). For the other half,
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conditioning and test were conducted in a chamber that was different from the home cage (EXP), and the delay was spent in the home cage.
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experimental session, animals had access to water in the home cage for 25 min. 2.2. Results and discussion
2.1. Method 2.1.1. Subjects Forty-eight male adult Wistar rats (n = 12 per group) participated in this experiment (mean weight 392 g, range 332–448 g). The animals were fed and housed as described in Experiment 1. 2.1.2. Apparatus As described in Experiment 1, for those animals in the home cage condition all experimental manipulations were conducted in the home cages. For those animals in the experimental cage condition, conditioning and testing were conducted in experimental chambers located in an isolated room, but the delay was spent in the home cages. Apparatus and fluids were the same as those described in Experiment 1. For the conditioning trial, each animal was injected (i.p.) with a 0.4 M LiCl solution (0.5% body weight). 2.1.3. Procedure After 7 days on a 23.5 h water-deprivation schedule, the conditioning trial was presented. For half of the animals, all experimental manipulations took place in the home cages (HOM condition); for the other half, conditioning and testing were conducted in experimental chambers located in an isolated room, but the delay was spent in the home cage (EXP condition). During this phase, all animals had access to the saccharin solution for a single trial (5 min). Immediately after saccharin consumption, LiCl was injected. The test phase was similar for all animals. Each subject was given access to the saccharin solution for 5 min on each of six successive days. This phase was initiated one day after conditioning for half of the animals (1-day condition) and 21 days after conditioning for the other half (21-day condition). To equate deprivation level at the time of testing for both delay conditions, animals in the 21-day condition received ad libitum water from days 9 to 20. The first test trial for those animals in the 21-day delay condition was conducted on day 29. All fluid consumptions during experimental sessions were recorded. As in Experiment 1, after completing each
2.2.1. Conditioning trial The mean amount of saccharin solution consumed by the animals in the HOM and EXP conditions was 9.10 (S.D. = 2.73) and 7.98 (S.D. = 1.51), respectively, a difference that was very similar to that obtained on the first pre-exposure trial of Experiment 1. However, the difference was not significant [F(1, 46) = 3.03, P > 0.08]. 2.2.2. Test phase Fig. 2 shows mean saccharin consumption across the six extinction trials for the four groups. As can be seen, there were main effects of Delay and Context, and interactions of both variables with trials. The mean amount of saccharin solution consumed on test days was subjected to a 2 × 2 × 6 mixed ANCOVA (Delay, Context of treatment, and Trials), with amount of saccharin consumed on the conditioning trial as a covariate. There was a significant main effect of Context of delay [F(1, 43) = 17.42, P < 0.001], with the HOM cage groups drinking more saccharin than the EXP cage groups (5.40 ml, S.D. = 2.47 and 3.06 ml, S.D. = 1.51, respectively). The main effect of Delay also was significant [F(1, 43) = 8.61, P < 0.01], with the 1-day groups drinking more than the 21-day groups (5.02 ml, S.D. = 2.38 and 3.36 ml, S.D. = 2.00, respectively). The Context × Delay interaction was not significant [F(1, 43) < 1]. The main effect of Trials was significant [F(5, 215) = 140.9, P < 0.001]. Extinction was faster for the 1-day delay groups than for the 21-day delay groups. In addition, irrespective of Delay, extinction was faster for the HOM groups than for the EXP groups. These observations were supported by significant Trials × Delay and Trials × Context interactions [F(5, 215) = 4.14, P < 0.001 and F(5, 215) = 7.67, P < 0.001, respectively]. The three-way interaction was not significant [F(5, 215) < 1]. In summary, Experiment 2 produced a strong RIE, with CTA being stronger after a 21-day delay than a 1-day delay. Furthermore, CTA was stronger when the conditioning and test stages were conducted in a context other than the delay context (home cage) as
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Fig. 2. Mean amount of saccharin solution consumed in the test stage as a function of delay between conditioning and test stages (1 and 21 days) and context of treatment (HOMe cages and EXPerimental cages). Error bars represent S.E.M.s.
compared to when all stages, including delay, were in the same context (home cage). Nevertheless, as indicated by the absence of a significant Delay × Context interaction, the RIE was not affected by the different context conditions. Although many studies have reported RIE when all the experimental stages, including the delay period, were conducted in the home cage (e.g. Batsell and Best, 1992a,b, 1994), there have been a number of failures to produce RIE when the delay context was different from that of conditioning/test (Batsell and Best, 1992a, Experiment 6; Kraemer et al., 1988; Miller et al., 1990, Experiment 1; Steinert et al., 1980). The present study is the first to demonstrate that RIE survives such a manipulation. Fig. 2 suggests that the discrepancy between the results of the present study and those that failed to produce RIE may be due to differences in the number of test trials. As can be seen, RIE develops more rapidly in the HOM group than the EXP group. Indeed, there does not appear to be any evidence for RIE in the HOM group until trial 3. It is therefore noteworthy that the two studies with the same delays as the present one, namely 1 and 21 days, that failed to obtain RIE, used only one 30-min test trial (Kraemer et al., 1988; Miller et al., 1990).
3. General discussion The reported experiments clearly demonstrate the relevance of retention interval and context in which the experimental treatment is conducted for neophobia and conditioning. Specifically, Experiment 1 revealed, not surprisingly, that when a flavored solution is presented in a familiar context (home cage) consumption is higher than when it is presented in a non-familiar context (experimental cages). Relatedly, Honey et al.8 1992) reported that intake of a novel liquid increased with number of presentations, but fell when afterwards it was presented in a different context. This decline in consumption did not occur when the test context was familiarized independently of the flavor presentations. In addition, in our Experiment 1, when a long delay was introduced between flavor exposure and test, there was an increase in saccharin consumption, reflecting attenuation of the neophobic response as opposed to its recovery (for similar results, see Bonardi et al., 1991; Green and Parker, 1975). Experiment 2 revealed a RIE for conditioning that was opposite to that found for neophobia: flavored fluid consumption decreased (i.e. an increase in conditioning) when the test was conducted 21 days after
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conditioning as compared to 1 day after conditioning. This RIE was evident in both home cage and experimental cage conditions. Furthermore, extinction proceeded faster for those groups conditioned and tested in a familiar home cage than for those conditioned and tested in the unfamiliar experimental cage. 3.1. Effects of retention interval The effects of retention intervals interpolated between various procedural stages of a variety of paradigms have become the subject of much theoretical interest, as seen in studies of extinction (e.g. Brooks and Bouton, 1993), counter-conditioning (e.g. Bouton and Peck, 1992), and LI (e.g. Aguado et al., 1994, 2001; De la Casa and Lubow, 2000, 2002). To explain these effects, Bouton (1993; Bouton et al., 1999) has proposed that extended passages of time result in, or are equivalent to, a context change. Lubow and De la Casa (2002) have suggested that such delay-induced changes specifically modulate the recovery of first associations (see below). If one accepts that elicitation of a habituated response in a particular context depends on the prior formation of a stimulus–context association in that same context (Wagner, 1979), then a time-induced context change between exposure and test also would result in the recovery of the neophobia that otherwise would have appeared as habituated. On the other hand, a context change should not affect CTA, since an excitatory conditioned response is relatively context-independent (e.g. Bouton, 1994). Clearly, our results do not support these hypotheses. Increases in retention interval reduced neophobic response and increased CTA. However, there is a potentially important difference between the procedures described in the present study and those usually employed to analyze Retention interval effects in extinction, counter-conditioning, and LI experiments. The latter typically require three stages, with the retention interval introduced between the second and test stages. The neophobia and conditioning experiments of the present study consisted of two phases, with the retention interval interpolated between the first and test stages. As a consequence, the two sets of procedures differ in terms of the number of hypothetical associations that are acquired before the test (one association for neophobia and simple
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conditioning, and two associations for extinction, counter-conditioning, and LI). Recently, we have proposed that long as compared to short retention intervals potentiate proactive interference, that is, the association that was acquired first gains in strength relative to the second association as the interval increases (Lubow and De la Casa, 2002). Specifically, the effects of a retention interval would critically depend on the acquisition of two or more sequentially learned associations in the same context. Under these circumstances, linking the same contextual cues to the memories of the two (or more) conditioning episodes (Bouton, 1993) provides the basis for interference effects, with an increase in retention interval potentiating the contribution of the first-learned association. In the present experiments, in spite of the absence of significant interactions with context of delay, the passage of time by itself potently affected behavior. The neophobic response was significantly less after the 21-day as compared to the 1-day retention interval. The decline in neophobia with time has an adaptive advantage. After flavor consumption, long intervals without an aversive consequence would signify increased certainty as to the safety of that flavor. This “learned safety” proposal (Kalat and Rozin, 1973) would be fully compatible with the habituation of neophobia observed in the 1-day group and the reduction in neophobia after 21 days in Experiment 1. Whether this effect is long-lasting, or restricted to relatively short intervals remains an open question. Although a decrease of the neophobic response has been obtained after a 24 h retention interval (Bonardi et al., 1991; Green and Parker, 1975) but not after 30 days (Domjan, 1977), the potentiating effect of a retention interval on the expression of CTA has not been consistently obtained (Batsell and Best, 1992a,b, 1993, 1994; Batsell and Pritchett, 1995; Dragoin et al., 1973; Klein et al., 1977; Steinert et al., 1980). On the basis of the Rescorla–Wagner model (1972), one might expect a Retention interval × Context interaction in Experiment 2, with RIE in the EXP condition but not in the HOM condition, due to extinction of the Context–US association during the long delay in the HOM condition (with animals spending the delay in the same context as conditioning) but not in the EXP condition (with animals spending the delay in a different context from conditioning). However, we
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obtained RIE in both HOM and EXP conditions, thereby not supporting the Rescorla–Wagner hypothesis. Our results are compatible with the retrieval disruption hypothesis of RIE. As proposed by Batsell and Best (1994), the reduced conditioning observed after a short delay is the result of a retrieval failure produced by the non-associative changes generated by a recent surprising US. If time-induced changes in conditioned response magnitude are produced by non-associative post-US effects (Batson and Best, 1982), then RIE should not be affected by the context of delay. 3.2. Effects of context of treatment The role of context in habituation has been amply recognized (e.g. Honey et al., 1992). From an associative point of view, habituation depends on the capacity of the context to elicit a representation of the stimulus in short-term memory (Wagner, 1979). Thus, the first time the stimulus is presented it is actively processed and it evokes the corresponding orienting/neophobic response. However, after repeated stimulus presentations in a particular context, that context acquires the capacity to retrieve the stimulus representation from long-term memory, thereby preventing active processing and reducing orienting/neophobic responses. However, the results of Experiment 1 are consistent with a non-associative model of habituation, one that proposes that the response decrement is generated to all elements of the the training situation. From this view, the greater the exposure to the complex stimulus (context plus stimulus), the greater the response decrement (Korn and Moyer, 1966; Marlin and Miller, 1981). In our design, the novelty of the experimental context would have contributed to the reduction in saccharin consumption observed in the EXP condition. Similarly, exposure to the saccharin flavor would result in increased consumption at testing as compared to NPE groups. Thus, neophobia would be the result of a summation of stimulus and context novelty, with novel/novel producing the highest levels of neophobia and familiar/familiar the lowest levels. The effects of place of conditioning and testing in CTA procedures has received little attention in previous research. To the best of our knowledge, only one study has examined the effects of Home versus Experimental contexts on simple CTA. Swank (2000) reported a trend towards greater aversion when the con-
ditioning episode was conducted in a novel context as compared with a familiar home context. Similarly, we found that conditioning was stronger when the CS–US pairing occurred in the experimental/unfamiliar context than in the home/familiar context. In summary, our results indicate that a set of conditions traditionally ignored in CTA and flavor neophobia procedures play an important role in determining consummatory behavior and learning. The place of the experimental treatment (home versus experimental cages) and the interval between the conditioning and testing episodes are variables that unmistakably modulate learning/expression of flavor–consequence and flavor–no consequence associations. The independent effects of place of exposure/conditioning and delay on neophobia and CTA, and the fact that they do not interact, have implications for the understanding of both phenomena, and for developing an explanation of the super-LI effect. It appears that one can reject explanations of the super-LI effect (De la Casa and Lubow, 2000, 2002; Lubow and De la Casa, 2002) based on either the interaction of passage of time and place of training on neophobia or on CTA. The absence of a Retention interval × Place interactions in Experiments 1 and 2 suggests that the direction of modulated LI with the passage of time, super- or attenuated LI, is the result of a triple interaction between two conflicting associations, training context and retention interval, the exact nature of which remains to be revealed.
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