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Extinction in multiple contexts does not necessarily make extinction less vulnerable to relapse
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Behaviour Research and Therapy 44 (2006) 983–994 www.elsevier.com/locate/brat
Extinction in multiple contexts does not necessarily make extinction less vulnerable to relapse Mark E. Bouton, Ana Garcı´ a-Gutie´rrez, Jessica Zilski, Erik W. Moody Department of Psychology, University of Vermont, Burlington, VT 05405, USA Received 12 November 2004; received in revised form 28 July 2005; accepted 29 July 2005
Abstract Three fear-conditioning experiments with rat subjects examined the effects of extinction in multiple contexts on a final relapse (renewal) effect that occurred when the extinguished fear cue was tested in a new context (Experiments 1 and 3) or in the context in which fear conditioning had first occurred (Experiment 2). Rats that received extinction in three contexts demonstrated more fear during extinction than rats that received the same number and temporal distribution of extinction trials in one context; extinction was partially lost with each context switch. Although extinction in multiple contexts thus had an impact on extinction behavior, it did not reduce the size of the final renewal effect. Fear during extinction was occasionally positively correlated with fear during final testing, but the two were never negatively correlated. The results suggest that extinction in multiple contexts does not necessarily weaken fear renewal, and that extinction procedures that generate high levels of responding in extinction do not necessarily make extinction learning less context-specific. r 2005 Elsevier Ltd. All rights reserved. Keywords: Fear extinction; Multiple contexts; Renewal effect
Introduction Fear conditioning is often thought to be involved in the etiology of anxiety disorders (e.g., Bouton, Mineka, & Barlow, 2001; Goldstein & Chambless, 1978; Mineka & Zinbarg, 1996; Wolpe, 1958; Wolpe & Rowan, 1988). The idea is that emotional trauma may play the role of an unconditional stimulus (US) that may enter into an association with cues (conditional stimuli, or CSs) that are also present at the same time. Cognitive behavior therapies designed to eliminate thoughts, emotions, or behavior that result from conditioning often involve repeated exposure to the feared cue, which theoretically causes extinction, a loss of responding to the CS that occurs as a consequence of exposure to the CS alone. However, it is now widely understood that extinction does not destroy the original fear learning, but rather depends in part on new learning that suppresses or inhibits it (e.g., Bouton, 2002, 2004; Rescorla, 2001). Various effects studied in the laboratory, such as spontaneous recovery (in which a response can return over time after extinction), reinstatement (in which an extinguished response recovers if the organism is exposed to the US after extinction), and renewal (in Corresponding author. Tel.: +1 802 646 4164; fax: +1 802 656 8783.
E-mail address: [email protected] (M.E. Bouton). 0005-7967/$ - see front matter r 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.brat.2005.07.007
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which extinguished responding can recover if the context is changed after extinction) all indicate that extinction is not the same as unlearning (e.g., see Bouton, 1991, 2002, 2004; Bouton & Swartzentruber, 1991, for reviews). All of these effects are consistent with the idea that extinction creates new learning that is highly context-specific. All of them can also be considered mechanisms of relapse after extinction. Given the vulnerability of extinguished behavior to relapse, it is of interest to know whether better extinction treatments can be designed to help prevent it. One possibility, originally suggested by Bouton (1991), is that extinction exposures to the cue in several contexts, rather than one context, might help reduce the context-specificity of extinction indicated by the renewal effect. The hypothesis was based on findings in the human memory literature which suggest that although memory for word lists may sometimes be forgotten if the context is changed between learning and testing (e.g., Smith, 1979), learning the list in multiple contexts instead of one context can create better recall in a new context (Smith, 1982). Perhaps learning extinction in multiple contexts might likewise encourage retrieval of extinction in new contexts. The hypothesis has been tested in rats by Gunther, Denniston, and Miller (1998) and by Chelonis, Calton, Hart, and Schachtman (1999). Gunther et al. studied fear conditioning, in which a noise was paired with shock and then fear of it was assessed by testing its ability to suppress licking at a tube filled with water. Fear of the noise was first conditioned via noise-shock pairings in Context A. Then the rats were given extinction trials in a second context (Context B) or in several contexts (Contexts B, C, and D) over a series of sessions. The number of extinction trials, and their distribution in time, was the same in the two groups. Two days after the last extinction session, the noise was then tested in yet another context (Context E). Renewed fear was observed in rats that had received extinction in only one context, but the effect was attenuated (though not abolished) in the group that received extinction in multiple contexts. Chelonis et al. (1999) reported consistent results in a flavor-aversion experiment. Rats received a pairing of a sucrose solution with illness in Context A, and then extinction (sucrose presentations without illness) in either Context B or in Contexts B, C, and D. The strength of the aversion to sucrose was finally tested in the original conditioning context (Context A) 24 h after the end of extinction. The results again suggested that extinction in multiple contexts caused less renewal than extinction in a single context. Extinction in multiple contexts thus appears to reduce renewal when testing is conducted in the original conditioning context (Chelonis et al., 1999) or in a new context (Gunther et al., 1998). Although these two reports suggest that renewal can be reduced by extinction in multiple contexts, the experiments did not investigate the mechanism or mechanisms that might cause the effect. One possibility is that extinction in multiple contexts might simply encourage generalization of extinction to other contexts. For example, if a single context is made up of many features, then extinction in several contexts will increase the overall number of features that are connected with extinction, and thus the likelihood that a new context will contain a common feature that has already been associated with extinction. A second possibility is that extinction might cause inhibitory conditioning of the context (e.g., Rescorla & Wagner, 1972); once inhibition is present in a context during extinction, it might ‘‘protect’’ the CS from total associative loss (e.g., Lovibond, Davis, & O’Flaherty, 2000; Rescorla, 2003; Rescorla & Wagner, 1972; Thomas & Ayres, 2004). When extinction occurs in multiple contexts, each switch to a new context would remove the background inhibition, and thus remove any resulting protection from extinction. A third possibility is that each context switch in extinction might cause a renewal effect, and thus a higher level of conditioned responding in extinction. Cognitive behavior therapists have often wondered whether the success of therapy depends on the amount of responding evoked in the therapy session (e.g., Foa & Kozak, 1986; see also Marks, 1978, for a review). Recent research suggests that the presence of safety behaviors (e.g., Salkovskis, Clark, Hackmann, Wells, & Gelder, 1999) during therapy may reduce fear during therapy but have a negative effect on therapeutic success (Rentz, Powers, Smits, Cougle, & Telch, 2003; Sloan & Telch, 2002). From a learning-theoretical perspective, high responding in extinction might allow more learning of direct inhibition of the response, which Rescorla (2001) has recently emphasized as a cause of extinction (see also Solomon & Wynne, 1954). Rescorla inferred the role of response inhibition in Pavlovian extinction from studies that manipulated response level in extinction with stimulus compounding techniques or variations in motivation level (e.g., hunger level during extinction of a CS associated with food). None of the possible explanations of the effect of extinction in multiple contexts were evaluated in the earlier experiments, which merely demonstrated the effect. For example, Gunther et al. (1998) did not collect
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data in extinction, so it is not possible to evaluate how the level of responding in extinction related to the level of responding in the final renewal test. And although Chelonis et al. (1999) did collect data in extinction, they observed no difference in extinction between the single- and multiple-context extinction groups. The initial purpose of the present experiments was therefore to analyze the effects of extinction in multiple contexts in more detail. We used the ‘‘conditioned suppression’’ method that we have used in a large number of experiments on fear extinction and the renewal effect in this laboratory (e.g., Bouton & Brooks, 1993; Bouton & King, 1983; Bouton & Ricker, 1994; Bouton & Swartzentruber, 1989). In that method, fear is assessed by the ability of a CS associated with shock to suppress an ongoing operant lever-pressing baseline that is reinforced by food (e.g., Estes & Skinner, 1941). Suppression to auditory CSs is correlated with freezing, a well-known defensive behavior in the rat (e.g., Bouton & Bolles, 1980), although the relationship between suppression and freezing is not as clear with visual CSs (e.g., Kim, Rivers, Bevins, & Ayres, 1996). In the present experiments, rats received fear conditioning with a tone in Context A, extinction in three sessions in Context B or in Contexts BCD, and then tests of the tone in Context E (a neutral context) or in Context A. Because extinction was conducted while the animals lever-pressed, we were able to measure the level of fear of the tone in extinction and thus test the extent to which it was correlated with the level of fear that was present during the final renewal test. If treatments that cause more responding during extinction cause better extinction learning (e.g., Rescorla, 2001), then one might expect to find a negative correlation between fear expressed during extinction and fear expressed during the final renewal test. Experiment 1 The first experiment employed a design analogous to that employed by Gunther et al. (1998). The rats were first trained to lever press on a variable-interval schedule of food reinforcement in several contexts. Then they received tone-shock pairings in Context A. After the end of conditioning, the two groups then received presentations of the tone alone (extinction trials) in three daily sessions. One group (Group ABBBE) received all extinction sessions in Context B. The other group (Group ABCDE) received the same number of trials (and distribution of trials) in Contexts B, C, and D. In a final session, fear of the tone was tested in Context E, a context that had not been associated with conditioning or extinction. We expected renewed fear of the tone in Group ABBBE, a standard renewal group. The question was whether extinction in multiple contexts would reduce the renewal effect in Group ABCDE, and whether fear in extinction would be correlated with fear during final renewal testing. The experiment started with 16 rats in each group, which was designed to provide higher than our usual statistical power (almost all of the context, conditioning, and extinction effects we have reported in the conditioned suppression method have been detected with n ¼ 8). Method Subjects The subjects were 32 female Wistar rats purchased from Charles River Laboratories (St. Constant, Quebec). They were between 75 and 90 days old at the start of the experiment and were individually housed in suspended wire mesh cages in a colony room with a 12:12 light:dark cycle. The rats were food-deprived to 80% of their initial body weights throughout the experiment. Apparatus The experiment used six sets of four conditioning chambers housed in sound attenuation cubicles. Each set was in a separate room of the laboratory. The first four sets provided Contexts B, C, D, and E (balanced by means of a Latin Square arrangement). The last two sets each provided Context A for half the rats. The boxes in Set 1 measured 26 25 19 cm. Three of the walls were made of aluminum, while the remaining wall was clear acrylic. The floor was made of tubular steel bars (16 mm diameter) spaced 3.2 cm apart (center to center) and mounted perpendicular to the front wall. A lever was positioned to the right of a food cup on the front wall. A distinctive odor was created by white vinegar in a dish outside the chamber. The boxes in Set 2 measured 32 25 21 cm; two walls and the ceiling were made of clear acrylic, whereas the side walls were aluminum. The floor was made of 0.5-cm (diameter) stainless-steel grids parallel to the
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front wall. The lever was positioned to the left of the food cup, and a dish containing Vicks Vaporub was outside the chamber. The boxes in Sets 3 and 4 measured 31.75 24.13 29.21 cm. Two walls and ceiling were made of clear acrylic, while the remaining walls were aluminum. In Set 3, the floor was stainless-steel grids (0.48 cm in diameter) spaced 3.18 cm center-to-center. A side wall and ceiling were striped. The lever was positioned to the right of the food cup, and a 4% McCormick anise extract solution was in a dish outside the chamber. In Set 4, the floor was made of alternating grids of different diameters (0.48 and 1.27 cm) separated by 1.59 cm (centerto-center). One wall and ceiling were covered with rows of large dark dots. The lever was positioned to the left of the food cup, and an 8% McCormick coconut extract solution was in a dish outside the chamber. The fifth and sixth sets of boxes each measured 30.5 24.1 21 cm. Two walls were aluminum, while two walls and the ceiling were clear acrylic. In Set 5, the floor consisted of 0.48-cm (diameter) bars that were spaced 1.6 cm center to center and mounted parallel to the front wall. The lever was to the left of the food cup, and odor was provided by a Citrus oil room freshener outside the chamber. In Set 6, the floor consisted of similar bars that they were ‘‘staggered’’ such that the height of adjacent bars differed by 1.6 cm. The lever was to the right of the food cup, and odor was provided by Pine-Sol. In all boxes, illumination was provided by two 7.5-w incandescent bulbs mounted to the ceiling of the sound attenuation cubicle. The CS was a 60-s presentation of a 3000-Hz tone (80 dBA) delivered through a 7.6 cm speaker mounted to the ceiling of the sound attenuation chamber, approximately 27 cm above each grid floor. Background noise level was 60 dBA in all boxes. The footshock US was a 0.5-s 1.0-mA footshock provided by Med Associates ENV-414 shock sources. Lever pressing was reinforced with 45-mg Noyes precision food pellets (Research Diets, Inc., New Brunswick, NJ). The apparatus was controlled by computer equipment located in an adjacent room. Procedure Baseline training. The rats were first trained to lever press in four contexts over eight 50-min daily sessions. In the first two sessions, all rats received shaping in the box that would become Context B. In the first session, the first 30 lever presses were reinforced; an FR-7 schedule was then in place for the next 5 reinforcers, after which a VI-90 schedule that was used for the rest of the experiment went into effect. In the second session, the first 5 responses were reinforced before the VI-90 schedule took effect. (This was the procedure for every session in the remainder of the experiment.) After these two sessions in Context B, the rats then received daily sessions in Context C, C, D, D, E, and E. As mentioned above, box Sets 1, 2, 3, and 4 were assigned as Contexts B, C, D, and E for individual rats by means of a Latin Square. Conditioning. Fear conditioning then began in Context A on the next day. In each of four daily sessions, there were three presentations of the tone CS, each terminating in the onset of the footshock. The intertrial interval was variable with a mean of 20 min. The first conditioning session involved an extra 15 min of responding on the VI baseline at the start (before the Pavlovian schedule was initiated) to give the animals practice lever pressing in these new contexts. By the end of the phase, all rats had received a total of 12 pairings of the tone and the 0.5-s, 1-mA shock. On the day following the conclusion of fear conditioning, the animals had a baseline recovery session (following the usual baseline training procedure) in Context E. Extinction. There were then three daily sessions of extinction, each containing four presentations of the tone alone (mean ITI ¼ 10 min) while the rats were lever pressing. The first session was conducted in Context B for all animals. After that session, the rats were randomly assigned to two groups (n ¼ 16) in a manner that maintained the box balancing. On the two days that followed, Group ABBBE received two further extinction sessions in Context B. Group ABCDE, in contrast, received an identical treatment in Contexts C and then D. Renewal test. On the day following the last extinction session, all rats were given four tone-alone trials while lever pressing in Context E. The first test trial occurred 15 min after the start of this 50-min session.
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Data analyses. Suppression to the tone was indexed in terms of suppression ratios, x=ðx þ yÞ, where x represents the number of lever presses made during the CS and y represents the number of lever-presses made in the equivalent period prior to the onset of the CS (pre-CS period). A ratio of 0 indicates complete suppression of responding during the CS, while a ratio of 0.5 indicates no response suppression during the CS. Suppression ratios were analyzed using analyses of variance (ANOVA). Parallel analyses were also conducted on responding during the pre-CS period. The rejection criterion was always po:05. Two rats in Group ABCDE were removed from the experiment because they showed no evidence of successful fear conditioning (e.g., suppression ratios4.43 on each trial of the first extinction session). Results Fig. 1 shows the suppression of the two groups on each trial of extinction and final renewal testing (far right). As the figure suggests, Group ABCDE was more afraid of the CS during extinction, because the context changes between the extinction sessions caused modest renewal effects. However, despite this difference between groups during extinction, they showed a comparable renewal of suppression when the tone was tested in Context E. These impressions were confirmed by statistical analyses, which focused on the transitions between sessions. A Group Trial ANOVA on the last trial of the first extinction session and the first trial of the second session revealed a significant Group Trial interaction, F ð1; 28Þ ¼ 4:30, as well as a Trial effect, F ð1; 28Þ ¼ 12:61. The Group effect was not significant, F ð1; 28Þ ¼ 1:78. Pairwise comparisons exploring the interaction indicated that Group ABCDE’s suppression increased between the sessions, F ð1; 28Þ ¼ 14:71, whereas Group ABBBE’s did not, F ð1; 28Þ ¼ 1:22. A compatible pattern was evident in a similar ANOVA on the last trial of the second session and the first of the third. Here there was a Group effect, F ð1; 28Þ ¼ 5:37, as well as a Trial effect, F ð1; 28Þ ¼ 7:82, although the interaction was not significant, F ð1; 28Þo1. Although the figure suggests that both groups increased suppression across these trials, pairwise comparisons indicated that the increase was significant again in Group ABCDE, F ð1; 28Þ ¼ 6:35, but not in Group ABBBE, F ð1; 28Þ ¼ 2:17. The results
0.6 ABCDE
Suppression Ratio
0.5
ABBBE
0.4
0.3
E
0.2 D 0.1 C 0.0
B Trials Extinction
Test
Fig. 1. Mean suppression to the tone for Groups ABCDE and ABBBE during each trial of extinction (left) and the final renewal test (right) in Experiment 1.
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Table 1 Correlations between extinction performance and renewal test performance in Experiment 1 Extinction and test trials correlated
1 1–2 1–4
Correlations, r Extinction session
Partial correlations, r Extinction session
1
2
3
df
2
3
df
.18 .50* .48*
.31 .41* .40*
.05 .32 .42*
28 28 28
.08 .06 .11
.10 .16 .32
27 27 27
*po:05.
thus suggest that there were renewal effects in Group ABCDE at the start of Sessions 2 and 3, coincident with each context switch. Despite these effects of the context manipulation, the groups showed comparable renewal during the final test session in Context E. Here the Group Trial ANOVA on the last extinction trial and the first test trial indicated only a significant Trial effect, F ð1; 28Þ ¼ 9:87. Neither the Group effect, nor the Group Trial interaction, approached significance, F’s(1,28)o1. Another Group Trial ANOVA on the four trials of the final renewal test similarly revealed a significant Trial effect, F ð1; 28Þ ¼ 10:86, indicating a decrease in suppression (further extinction) over testing, but the Group main effect and the Group Trial interaction did not approach significance, F ’sð1; 28Þo1. There was no evidence in this experiment that extinction in multiple contexts affected the size of the final renewal effect. We performed identical ANOVAs on the pre-CS scores. No effects or interactions were significant; all F’s were less than 1 except for the Trial effect on the Session 2–3 transition, F ð1; 28Þ ¼ 3:36, and the Group effect on Session 3-Renewal test transition, F ð1; 28Þ ¼ 1:7. Groups ABBBE and ABCDE had mean pre-CS scores of 24.4 and 24.2 during extinction and 20.7 and 25.8 during the final renewal test, respectively. To further examine the relationship between the level of suppression in extinction and the final renewal effect, we calculated correlations between the rats’ suppression during different extinction sessions and during the final renewal test. The correlations are summarized in Table 1. The data were aggregated in several ways. The first row summarizes the correlations between the first trial of the corresponding extinction session and the first trial of the final renewal test; the second row summarizes the correlations between the average of the first two trials of the corresponding extinction session and the average of the first two trials of the final renewal test; and the third row summarizes the correlations between the average of the four trials of the corresponding extinction session and the four trials of the final renewal test. If anything, the correlations were positive, and significantly so when the data were aggregated in two- and four-trial blocks. In other words, rats that showed the most fear during extinction also tended to show the most fear during renewal testing. This result appears to reflect individual differences in the extent of original fear conditioning. The right columns summarize the partial correlation coefficients that partialled out suppression on the first two-trial block of Extinction Session 1, which was mainly affected by conditioning rather than extinction. (We were unable to use data from actual conditioning sessions because the pre-CS scores there were too suppressed.) None of the partial correlation coefficients approached significance. Thus, although the correlation between fear during extinction and renewal testing Context E was positive, this was due to the fact that rats that emerged from conditioning with strong fear of the tone also showed the strongest renewal in the end. Discussion The final tests in Context E revealed an increase in suppression that may be attributed to a renewal effect. Similar renewals were also observed during the extinction phase. That is, the context switches in extinction that Group ABCDE received caused increases in suppression that were not observed in the control group (Group ABBBE). Although the suppression of Group ABCDE during the extinction sessions confirm that the multiple-context treatment had an effect on behavior, and that the animals thus perceived the contexts as different, extinction in multiple contexts did not demonstrably reduce the size of the final renewal effect in
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Context E. Extinction was no less vulnerable to renewal after the multiple-context extinction procedure than after a standard single-context procedure. This result is compatible with the finding that fear of the CS during the final renewal test was positively related to fear during extinction. This pattern may be inconsistent with the view that high responding in extinction ensures better, or more permanent, extinction learning (cf. Rescorla, 2001; Solomon & Wynne, 1954). Instead, the correlational analyses suggest that individuals that acquired strong fear during conditioning also showed strong fear during extinction and during the final renewal test. Higher levels of suppression in extinction did not make extinction less context-specific; renewal of fear was still observed. Experiment 2 Experiment 1 studied the so-called ‘‘ABC’’ renewal effect in which fear is renewed when the CS is tested in a neutral context that has not been previously associated with either extinction or conditioning. It seemed possible that the lack of attenuation of renewal by extinction in multiple contexts was peculiar to that renewal design. Another commonly studied design is ‘‘ABA’’ renewal, in which final renewal is caused by return to the original conditioning context (Context A). Unlike renewal in the ABC design, which depends exclusively on release from some inhibitory process controlled by the extinction context, renewal in the ABA design can reflect both release from inhibition and a positive modulation of responding by the original conditioning context. Chelonis et al. (1999) used an ABA design. It was conceivable that extinction in multiple contexts might provide a better hedge against this type of renewal effect. Experiment 2 was therefore designed to extend the generality of Experiment 1 by comparing groups that received extinction in single or multiple contexts on the strength of their renewal when tested in the original fear-conditioning context, Context A. Method Subjects and apparatus The subjects were 32 female Wistar rats of the same age and from the same supplier as those in Experiment 1. The apparatus was four sets of four boxes (Sets 1, 2, 3, and 4) described in the previous experiment. Procedure Baseline training, conditioning, and extinction were the same as in Experiment 1 except as noted. During baseline training, the rats received shaping and practice lever pressing in the order Contexts BBCCDDAA. Four conditioning sessions then followed, each 50 min in duration, and each containing three tone-shock pairings. There was then a baseline recovery session in Context A, and then extinction in three sessions conducted in Context B (Group ABBBA) or in B, C, and D (Group ABCDA). (As before, the groups were matched on their suppression in Context B during the first extinction session.) In the final renewal test (conducted the day after the last extinction session), all rats received four tone presentations in Context A—the original fear conditioning context. As before, the first tone was presented 15 min after the start of the session. Results Fig. 2 summarizes the suppression of the two groups on each trial of extinction and renewal testing. The results were consistent with those of Experiment 1. The multiple-context group, Group ABCDA, was again more afraid of the CS during extinction, because each context change caused a renewal effect. However, despite this effect, the two groups showed comparable renewal when they were returned to the original conditioning context (Context A). Statistical analysis followed the strategy used in Experiment 1. A Group Trial ANOVA on the last trial of the first extinction session and the first trial of the second revealed nonreliable Group and Group Trial effects F’s(1,30)o1. The trial effect was highly significant, F(1,30) ¼ 6.24. Pairwise comparisons indicated that Group ABCDA increased suppression between trials, F(1,30) ¼ 6.03, whereas Group ABBBA did not, F(1,30) ¼ 1.50. The ANOVA on the Session 2–3 transition revealed a Trial effect, F(1,30) ¼ 22.32, and a Group Trial interaction, F(1,30) ¼ 5.35, although the group effect was not reliable, F(1,30) ¼ 2.31. Pairwise
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0.6
ABCDA ABBBA
Suppression Ratio
0.5
0.4
0.3
0.2 A C
0.1
D
B
0 Trials Extinction
Test
Fig. 2. Mean suppression to the tone for Groups ABCDA and ABBBA during each trial of extinction (left) and the final renewal test (right) in Experiment 2.
comparisons again indicated that Group ABCDA’s increase in suppression was significant, F(1,30) ¼ 25.00, whereas Group ABBBA’s was not, F(1,30) ¼ 2.56. Like the results of Experiment 1, the results of this experiment suggest that extinction in multiple contexts causes more suppression—through successive renewal effects—in extinction. The groups did not differ, however, on the last extinction trial, F(1,30) ¼ 2.65. Despite the effectiveness of the independent variable in extinction, there was no demonstrable difference between the groups in the final renewal effect. Here the Group Trial ANOVA on the last extinction trial and the first test trial once again indicated only a significant Trial effect, F(1,30) ¼ 8.39. Neither the Group effect, F(1,30) ¼ 1.48, nor the Group Trial interaction, F(1,30)o1, approached statistical significance. An ANOVA comparing the groups’ suppression on all four trials of the final renewal test revealed a significant Trial effect, F(3,90) ¼ 14.65. But there was no Group effect, F(1,30) ¼ 1.01, or Group Trial interaction, F(3,90) o1. The results failed to confirm that extinction in multiple contexts reduces the size of the ABA renewal effect. Identical analyses were conducted on the pre-CS scores. These indicated no Group, Trial, or Group Trial interactions, largest F(1,30) ¼ 2.80. Groups ABBBA and ABCDA had (respective) mean pre-CS scores of 20.4 and 20.0 during extinction and 23.5 and 28.6 during the final renewal test. Table 2 summarizes the correlations between tone fear during the extinction sessions and during final renewal testing. In this experiment, the correlations were mostly nonsignificant, although at the highest level of aggregation (four-trial blocks), there was once again a significant positive correlation between fear during the first extinction session and fear during the final renewal test. It is interesting that the correlations were lower here than in Experiment 1. The difference may reflect random variation between experiments, or the fact that fear during extinction in neutral contexts (Contexts B, C, D) is a better predictor of fear in another neutral context (Context E; Experiment 1) than in the original conditioning context (Context A; current experiment). Discussion The results of Experiment 2 were consistent with those of Experiment 1: despite the fact that testing was now conducted in the original fear-conditioning context, extinction in multiple contexts had no detectable
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Table 2 Correlations between extinction performance and renewal test performance in Experiment 2 Extinction and test trials correlated
1 1–2 1–4
Correlations, r Extinction session
Partial correlations, r Extinction session
1
2
3
df
2
3
df
.12 .06 .36*
.16 .13 .10
.19 .17 .08
30 30 30
.26 .18 .02
.23 .20 .03
29 29 29
*po:05.
effect on the strength of the final renewal effect. This, along with the results of the correlational analyses, once again suggest that higher responding in extinction does not produce a more permanent (or less contextspecific) extinction effect. Experiment 3 The findings of Experiments 1 and 2 failed to replicate results previously reported by Gunther et al. (1998) and Chelonis et al. (1999). There were, of course, many differences between the present experiments and the previous ones. However, one difference that might be especially important is that our conditioned suppression method required that the rats be trained to lever press in each of the contexts before conditioning, extinction, and renewal testing. One consequence was that each of the contexts had been associated with the same foodpellet reinforcer. This common association could have encouraged generalization between the contexts through the process of mediated generalization (e.g., Honey & Hall, 1989), and thus reduced the effect of extinction in multiple contexts. Of course, the fact that the context switches in extinction caused demonstrable renewal effects indicates that the rats did not generalize completely between them. Nonetheless, the experiments by Gunther et al. and by Chelonis et al. did not involve presenting a common reinforcer in each context. Experiment 3 therefore compared ABBBE groups and ABCDE groups as in Experiment 1 in a method in which Context E was the only context in which the rats received reinforcers and lever-press training. This method was more directly analogous to that of Gunther et al. (1998), and might theoretically reduce generalization between the various contexts in Group ABCDE. Method Subjects and apparatus The subjects were 32 female Wistar rats of the same age and from the same supplier as those in Experiments 1 and 2. The apparatus was the same sets of boxes used in Experiment 1. During conditioning and extinction, however, the levers were removed. Procedure The procedure was identical to that described in Experiment 1 with the following exceptions. During baseline training, the rats received shaping and VI practice in eight sessions in Context E only. Conditioning and extinction were then conducted in the various contexts with the levers removed. There were four sessions of conditioning in Context A (three tone-shock pairings in each), followed by three sessions of extinction (four tone alone trials) in Context B (Group ABBBE) or B, C, and D (ABCDE). After the final extinction session, the rats received a baseline recovery session in Context E, and on the following day four final tests of the CS while lever pressing in Context E.
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0.6
Suppression Ratio
0.5
0.4
0.3 ABCDE ABBBE 0.2
0.1
0 Trials Renewal Test Fig. 3. Mean suppression ratio to the tone for Groups ABCDE and ABBBE during the renewal test of Experiment 3.
Results and discussion The results of the test session are summarized in Fig. 3. As the figure suggests, there was once again a modest renewal effect in both groups, and no hint of a difference in its size. A Group Trial ANOVA on the test data revealed a significant Trial effect, F ð3; 90Þ ¼ 10:59, that indicated extinction of suppression (as usual) over the four test trials. But the Group effect, F ð1; 30Þo1, and the Group Trial interaction, F ð3; 90Þ ¼ 1:12, failed to approach reliability. An identical analysis on the pre-CS scores revealed nonsignificant effects of Trial, F ð3; 90Þ ¼ 2:34, p ¼ :078, Group, F(1,30) o1, or Group Trial, F ð3; 90Þ ¼ 1:71. The mean response rates during the pre-CS periods were 24.87 and 26.89 for Groups ABBBE and ABCDE, respectively. Despite the absence of a common reinforcer in the various contexts, Experiment 3 produced results that paralleled those of the previous experiments perfectly. Under a range of conditions, we have produced no evidence that extinction in multiple contexts reduces the strength of renewal compared to that observed in a group that receives extinction in only one context.
General discussion The results of these experiments suggest that extinction in three different contexts does not necessarily reduce the renewal of fear that occurs when animals are tested in either a fourth neutral context (Experiments 1 and 3) or in the original fear conditioning context (Experiment 2). The results suggest that neither the ABC nor the ABA renewal effect is reduced by extinction in multiple contexts in the fear-conditioning method that has been used extensively in this laboratory (e.g., Bouton & Brooks, 1993; Bouton & King, 1983; Bouton & Ricker, 1994; Bouton & Swartzentruber, 1989). The results thus imply that there are important variables that modulate the impact that extinction in multiple contexts had on the renewal effect in earlier experiments (Chelonis et al., 1999; Gunther et al., 1998). In fact, the earlier reports had already suggested the operation of modulating variables. For example, Chelonis
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et al. (1999, Experiment 2) failed to replicate the attenuation of renewal by extinction in multiple contexts when the rats were given equivalent exposure to all the contexts during extinction. (This is in fact why we did not include such control exposures in the present experiments.) In addition, Gunther et al. (1998) found that the advantage of extinction in multiple contexts was reduced if fear conditioning was also first conducted in multiple contexts. That is, although extinction in B, C, and D reduced the renewal effect when conditioning had only been conducted in Context A, it had substantially less effect if conditioning had first been conducted in Contexts A, A0 , and A00 . It is possible that conditioning in multiple contexts in this manner is closer to what occurs in everyday life. All told, the results of the present and earlier experiments clearly indicate that extinction in multiple contexts does not guarantee the prevention of renewal. Bouton, Woods, Moody, Sunsay, and Garcı´ a-Gutie´rrez (in press) recently reviewed animal laboratory research that has investigated ways in which extinction procedures can be modified to help reduce relapse effects like renewal. Although the literature suggests that treatments designed to enhance extinction learning (including extinction in multiple contexts) are occasionally helpful, one approach that seems to have consistent promise is to provide explicit ‘‘bridges’’ between the therapy (extinction) context and contexts where relapse is likely to be a problem. For example, a therapist might accept the possible context-specificity of extinction and conduct extinction directly in the contexts where lapses might occur. Alternatively, the therapist might provide retrieval cues that can be presented or used in a potential relapse context to help retrieve the extinction experience (e.g., Brooks & Bouton, 1993, 1994; Collins & Brandon, 2002). The results of the present experiments are interesting from a theoretical standpoint. Perhaps most clearly, they suggest that higher levels of responding in extinction (as shown in the multiple-context groups) did not produce a more thorough extinction effect that was less vulnerable to relapse. This finding, along with correlational analyses that never revealed a significant negative relationship between the level of fear in extinction and the level of fear observed during the final renewal test, suggest that evoking high levels of fear during extinction or exposure therapy may not yield a more durable therapeutic effect (e.g., Marks, 1978). From a learning-theoretical perspective, if higher levels of fear in extinction do allow stronger response inhibition to develop (Rescorla, 2001), that response inhibition must still be at least partly specific to the context(s) in which it is learned. The current results suggest that neither extinction in multiple contexts nor high levels of responding in extinction necessarily prevents the renewal effect, one of several possible mechanisms of clinical relapse that have been investigated in the animal laboratory. Acknowledgments This research was supported by Grant RO1 MH64847 from the National Institute of Mental Health. References Bouton, M. E. (1991). A contextual analysis of fear extinction. In P. R. Martin (Ed.), Handbook of behavior therapy and psychological science: An integrative approach (pp. 435–453). Elmsford, NY: Pergamon Press, Inc. Bouton, M. E. (2002). Context, ambiguity, and unlearning: Sources of relapse after behavioral extinction. Biological Psychology, 52, 976–986. Bouton, M. E. (2004). Context and behavioral process in extinction. Learning & Memory, 11, 485–494. Bouton, M. E., & Bolles, R. C. (1980). Conditioned fear assessed by freezing and by the suppression of three different baselines. Animal Learning & Behavior, 8, 429–434. Bouton, M. E., & Brooks, D. C. (1993). Time and context effects on performance in a Pavlovian discrimination reversal. Journal of Experimental Psychology: Animal Behavior Processes, 19, 165–179. Bouton, M. E., & King, D. A. (1983). Contextual control of the extinction of conditioned fear: Tests for the associative value of the context. Journal of Experimental Psychology: Animal Behavior Processes, 9, 248–265. Bouton, M. E., Mineka, S., & Barlow, D. H. (2001). A modern learning-theory perspective on the etiology of panic disorder. Psychological Review, 108, 4–32. Bouton, M. E., & Ricker, S. T. (1994). Renewal of extinguished responding in a second context. Animal Learning & Behavior, 22, 317–324. Bouton, M. E., & Swartzentruber, D. (1989). Slow reacquisition following extinction: Context, encoding, and retrieval mechanisms. Journal of Experimental Psychology: Animal Behavior Processes, 15, 43–53. Bouton, M. E., & Swartzentruber, D. (1991). Sources of relapse after extinction in Pavlovian and instrumental learning. Clinical Psychology Review, 11, 123–140.
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Bouton, M. E., Woods, A. M., Moody, E. W., Sunsay, C., & Garcı´ a-Gutie´rrez, A. (in press). Counteracting the context-dependence of extinction: Relapse and some tests of possible methods of relapse prevention. In: M.G. Craske, D. Hermans, D. Vansteenwegen (Eds.), Fear and learning: Basic science to clinical application. Washington, DC: American Psychological Association. Brooks, D. C., & Bouton, M. E. (1993). A retrieval cue for extinction attenuates spontaneous recovery. Journal of Experimental Psychology: Animal Behavior Processes, 19, 77–89. Brooks, D. C., & Bouton, M. E. (1994). A retrieval cue for extinction attenuates response recovery (renewal) caused by a return to the conditioning context. Journal of Experimental Psychology: Animal Behavior Processes, 20, 366–379. Chelonis, J. J., Calton, J. L., Hart, J. A., & Shachtman, T. R. (1999). Attenuation of the renewal effect by extinction in multiple contexts. Learning and Motivation, 30, 1–14. Collins, B. N., & Brandon, T. H. (2002). Effects of extinction context and retrieval cues on alcohol cue reactivity among nonalcoholic drinkers. Journal of Consulting and Clinical Psychology, 70, 390–397. Estes, W. K., & Skinner, B. F. (1941). Some quantitative properties of anxiety. Journal of Experimental Psychology, 29, 390–400. Foa, E. B., & Kozak, M. J. (1986). Emotional processing of fear: Exposure to corrective information. Psychological Bulletin, 99, 20–35. Goldstein, A. J., & Chambless, D. L. (1978). A reanalysis of agoraphobia. Behavior Therapy, 9, 47–59. Gunther, L. M., Denniston, J. C., & Miller, R. R. (1998). Conducting exposure treatment in multiple contexts can prevent relapse. Behavior Research and Therapy, 36, 75–91. Honey, R.C., & Hall, G. (1989). Acquired equivalence and distinctiveness of cues. Journal of Experimental Psychology: Animal Behavior Processes, 15, 338–346. Kim, S. D., Rivers, S., Bevins, R. A., & Ayres, J. J. B. (1996). Conditioned stimulus determinants of conditioned response form in Pavlovian fear conditioning. Journal of Experimental Psychology: Animal Behavior Processes, 22, 87–104. Lovibond, P. F., Davis, N. R., & O’Flaherty, A. S. (2000). Protection from extinction in human fear conditioning. Behaviour Research and Therapy, 38, 967–983. Marks, I. (1978). Behavioral psychotherapy of adult neurosis. In S. Garfield, & A. E. Bergin (Eds.), Handbook of psychotherapy and behaviour modification. Chichester, UK: Wiley. Mineka, S., & Zinbarg, R. (1996). Conditioning and ethological models of anxiety disorders: Stress in dynamic contexts anxiety models. In D. A. Hope (Ed.), Perspectives on anxiety, panic, and fear. Nebraska Symposium on Motivation, Vol. 43 (pp. 135–210). Lincoln: Nebraska University Press. Rentz, T. O., Powers, M. B., Smits, J. A. J., Cougle, J. R., & Telch, M. J. (2003). Active-imaginal exposure: Examination of a new behavioral treatment for cynophobia (dog phobia). Behaviour Research and Therapy, 41, 1337–1353. Rescorla, R. (2001). Experimental extinction. In R. R. Mowrer, & S. B. Klein (Eds.), Handbook of contemporary learning theories (pp. 119–154). Mahwah, NJ: Erlbaum. Rescorla, R. A. (2003). Protection from extinction. Learning & Behavior, 31, 124–132. Rescorla, R. A., & Wagner, A. R. (1972). A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. In A. H. Black, & W. F. Prokasy (Eds.), Classical conditioning II: Current research and theory (pp. 64–99). New York: Appleton-Century-Crofts. Salkovskis, P. M., Clark, D. M., Hackmann, A., Wells, A., & Gelder, M. G. (1999). An experimental investigation of the role of safetyseeking behaviours in the maintenance of panic disorder with agoraphobia. Behaviour Research and Therapy, 37, 559–574. Sloan, T. B., & Telch, M. J. (2002). The effects of safety-seeking behavior and guided threat appraisal on fear reduction during exposure: An experimental investigation. Behaviour Research and Therapy, 40, 235–251. Smith, S. M. (1979). Remembering in and out of context. Journal of Experimental Psychology: Human Learning and Memory, 5, 460–471. Smith, S. M. (1982). Enhancement of recall using multiple environmental contexts during learning. Memory & Cognition, 10, 405–412. Solomon, R. L., & Wynne, L. C. (1954). Traumatic avoidance learning: The principles of anxiety conservation and partial irreversibility. Psychological Review, 61, 353–385. Thomas, B. L., & Ayres, J. J. B. (2004). Use of the ABA fear renewal paradigm to assess the effects of extinction with co-present fear inhibitors or excitors: Implications for theories of extinction and for treating human fears and phobias. Learning and Motivation, 31, 22–52. Wolpe, J. (1958). Psychotherapy by reciprocal inhibition. Stanford, CA: Stanford University Press. Wolpe, J., & Rowan, V. C. (1988). Panic disorder: A product of classical conditioning. Behaviour Research and Therapy, 26, 441–450.
Behaviour Research and Therapy 44 (2006) 983–994 www.elsevier.com/locate/brat
Extinction in multiple contexts does not necessarily make extinction less vulnerable to relapse Mark E. Bouton, Ana Garcı´ a-Gutie´rrez, Jessica Zilski, Erik W. Moody Department of Psychology, University of Vermont, Burlington, VT 05405, USA Received 12 November 2004; received in revised form 28 July 2005; accepted 29 July 2005
Abstract Three fear-conditioning experiments with rat subjects examined the effects of extinction in multiple contexts on a final relapse (renewal) effect that occurred when the extinguished fear cue was tested in a new context (Experiments 1 and 3) or in the context in which fear conditioning had first occurred (Experiment 2). Rats that received extinction in three contexts demonstrated more fear during extinction than rats that received the same number and temporal distribution of extinction trials in one context; extinction was partially lost with each context switch. Although extinction in multiple contexts thus had an impact on extinction behavior, it did not reduce the size of the final renewal effect. Fear during extinction was occasionally positively correlated with fear during final testing, but the two were never negatively correlated. The results suggest that extinction in multiple contexts does not necessarily weaken fear renewal, and that extinction procedures that generate high levels of responding in extinction do not necessarily make extinction learning less context-specific. r 2005 Elsevier Ltd. All rights reserved. Keywords: Fear extinction; Multiple contexts; Renewal effect
Introduction Fear conditioning is often thought to be involved in the etiology of anxiety disorders (e.g., Bouton, Mineka, & Barlow, 2001; Goldstein & Chambless, 1978; Mineka & Zinbarg, 1996; Wolpe, 1958; Wolpe & Rowan, 1988). The idea is that emotional trauma may play the role of an unconditional stimulus (US) that may enter into an association with cues (conditional stimuli, or CSs) that are also present at the same time. Cognitive behavior therapies designed to eliminate thoughts, emotions, or behavior that result from conditioning often involve repeated exposure to the feared cue, which theoretically causes extinction, a loss of responding to the CS that occurs as a consequence of exposure to the CS alone. However, it is now widely understood that extinction does not destroy the original fear learning, but rather depends in part on new learning that suppresses or inhibits it (e.g., Bouton, 2002, 2004; Rescorla, 2001). Various effects studied in the laboratory, such as spontaneous recovery (in which a response can return over time after extinction), reinstatement (in which an extinguished response recovers if the organism is exposed to the US after extinction), and renewal (in Corresponding author. Tel.: +1 802 646 4164; fax: +1 802 656 8783.
E-mail address: [email protected] (M.E. Bouton). 0005-7967/$ - see front matter r 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.brat.2005.07.007
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which extinguished responding can recover if the context is changed after extinction) all indicate that extinction is not the same as unlearning (e.g., see Bouton, 1991, 2002, 2004; Bouton & Swartzentruber, 1991, for reviews). All of these effects are consistent with the idea that extinction creates new learning that is highly context-specific. All of them can also be considered mechanisms of relapse after extinction. Given the vulnerability of extinguished behavior to relapse, it is of interest to know whether better extinction treatments can be designed to help prevent it. One possibility, originally suggested by Bouton (1991), is that extinction exposures to the cue in several contexts, rather than one context, might help reduce the context-specificity of extinction indicated by the renewal effect. The hypothesis was based on findings in the human memory literature which suggest that although memory for word lists may sometimes be forgotten if the context is changed between learning and testing (e.g., Smith, 1979), learning the list in multiple contexts instead of one context can create better recall in a new context (Smith, 1982). Perhaps learning extinction in multiple contexts might likewise encourage retrieval of extinction in new contexts. The hypothesis has been tested in rats by Gunther, Denniston, and Miller (1998) and by Chelonis, Calton, Hart, and Schachtman (1999). Gunther et al. studied fear conditioning, in which a noise was paired with shock and then fear of it was assessed by testing its ability to suppress licking at a tube filled with water. Fear of the noise was first conditioned via noise-shock pairings in Context A. Then the rats were given extinction trials in a second context (Context B) or in several contexts (Contexts B, C, and D) over a series of sessions. The number of extinction trials, and their distribution in time, was the same in the two groups. Two days after the last extinction session, the noise was then tested in yet another context (Context E). Renewed fear was observed in rats that had received extinction in only one context, but the effect was attenuated (though not abolished) in the group that received extinction in multiple contexts. Chelonis et al. (1999) reported consistent results in a flavor-aversion experiment. Rats received a pairing of a sucrose solution with illness in Context A, and then extinction (sucrose presentations without illness) in either Context B or in Contexts B, C, and D. The strength of the aversion to sucrose was finally tested in the original conditioning context (Context A) 24 h after the end of extinction. The results again suggested that extinction in multiple contexts caused less renewal than extinction in a single context. Extinction in multiple contexts thus appears to reduce renewal when testing is conducted in the original conditioning context (Chelonis et al., 1999) or in a new context (Gunther et al., 1998). Although these two reports suggest that renewal can be reduced by extinction in multiple contexts, the experiments did not investigate the mechanism or mechanisms that might cause the effect. One possibility is that extinction in multiple contexts might simply encourage generalization of extinction to other contexts. For example, if a single context is made up of many features, then extinction in several contexts will increase the overall number of features that are connected with extinction, and thus the likelihood that a new context will contain a common feature that has already been associated with extinction. A second possibility is that extinction might cause inhibitory conditioning of the context (e.g., Rescorla & Wagner, 1972); once inhibition is present in a context during extinction, it might ‘‘protect’’ the CS from total associative loss (e.g., Lovibond, Davis, & O’Flaherty, 2000; Rescorla, 2003; Rescorla & Wagner, 1972; Thomas & Ayres, 2004). When extinction occurs in multiple contexts, each switch to a new context would remove the background inhibition, and thus remove any resulting protection from extinction. A third possibility is that each context switch in extinction might cause a renewal effect, and thus a higher level of conditioned responding in extinction. Cognitive behavior therapists have often wondered whether the success of therapy depends on the amount of responding evoked in the therapy session (e.g., Foa & Kozak, 1986; see also Marks, 1978, for a review). Recent research suggests that the presence of safety behaviors (e.g., Salkovskis, Clark, Hackmann, Wells, & Gelder, 1999) during therapy may reduce fear during therapy but have a negative effect on therapeutic success (Rentz, Powers, Smits, Cougle, & Telch, 2003; Sloan & Telch, 2002). From a learning-theoretical perspective, high responding in extinction might allow more learning of direct inhibition of the response, which Rescorla (2001) has recently emphasized as a cause of extinction (see also Solomon & Wynne, 1954). Rescorla inferred the role of response inhibition in Pavlovian extinction from studies that manipulated response level in extinction with stimulus compounding techniques or variations in motivation level (e.g., hunger level during extinction of a CS associated with food). None of the possible explanations of the effect of extinction in multiple contexts were evaluated in the earlier experiments, which merely demonstrated the effect. For example, Gunther et al. (1998) did not collect
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data in extinction, so it is not possible to evaluate how the level of responding in extinction related to the level of responding in the final renewal test. And although Chelonis et al. (1999) did collect data in extinction, they observed no difference in extinction between the single- and multiple-context extinction groups. The initial purpose of the present experiments was therefore to analyze the effects of extinction in multiple contexts in more detail. We used the ‘‘conditioned suppression’’ method that we have used in a large number of experiments on fear extinction and the renewal effect in this laboratory (e.g., Bouton & Brooks, 1993; Bouton & King, 1983; Bouton & Ricker, 1994; Bouton & Swartzentruber, 1989). In that method, fear is assessed by the ability of a CS associated with shock to suppress an ongoing operant lever-pressing baseline that is reinforced by food (e.g., Estes & Skinner, 1941). Suppression to auditory CSs is correlated with freezing, a well-known defensive behavior in the rat (e.g., Bouton & Bolles, 1980), although the relationship between suppression and freezing is not as clear with visual CSs (e.g., Kim, Rivers, Bevins, & Ayres, 1996). In the present experiments, rats received fear conditioning with a tone in Context A, extinction in three sessions in Context B or in Contexts BCD, and then tests of the tone in Context E (a neutral context) or in Context A. Because extinction was conducted while the animals lever-pressed, we were able to measure the level of fear of the tone in extinction and thus test the extent to which it was correlated with the level of fear that was present during the final renewal test. If treatments that cause more responding during extinction cause better extinction learning (e.g., Rescorla, 2001), then one might expect to find a negative correlation between fear expressed during extinction and fear expressed during the final renewal test. Experiment 1 The first experiment employed a design analogous to that employed by Gunther et al. (1998). The rats were first trained to lever press on a variable-interval schedule of food reinforcement in several contexts. Then they received tone-shock pairings in Context A. After the end of conditioning, the two groups then received presentations of the tone alone (extinction trials) in three daily sessions. One group (Group ABBBE) received all extinction sessions in Context B. The other group (Group ABCDE) received the same number of trials (and distribution of trials) in Contexts B, C, and D. In a final session, fear of the tone was tested in Context E, a context that had not been associated with conditioning or extinction. We expected renewed fear of the tone in Group ABBBE, a standard renewal group. The question was whether extinction in multiple contexts would reduce the renewal effect in Group ABCDE, and whether fear in extinction would be correlated with fear during final renewal testing. The experiment started with 16 rats in each group, which was designed to provide higher than our usual statistical power (almost all of the context, conditioning, and extinction effects we have reported in the conditioned suppression method have been detected with n ¼ 8). Method Subjects The subjects were 32 female Wistar rats purchased from Charles River Laboratories (St. Constant, Quebec). They were between 75 and 90 days old at the start of the experiment and were individually housed in suspended wire mesh cages in a colony room with a 12:12 light:dark cycle. The rats were food-deprived to 80% of their initial body weights throughout the experiment. Apparatus The experiment used six sets of four conditioning chambers housed in sound attenuation cubicles. Each set was in a separate room of the laboratory. The first four sets provided Contexts B, C, D, and E (balanced by means of a Latin Square arrangement). The last two sets each provided Context A for half the rats. The boxes in Set 1 measured 26 25 19 cm. Three of the walls were made of aluminum, while the remaining wall was clear acrylic. The floor was made of tubular steel bars (16 mm diameter) spaced 3.2 cm apart (center to center) and mounted perpendicular to the front wall. A lever was positioned to the right of a food cup on the front wall. A distinctive odor was created by white vinegar in a dish outside the chamber. The boxes in Set 2 measured 32 25 21 cm; two walls and the ceiling were made of clear acrylic, whereas the side walls were aluminum. The floor was made of 0.5-cm (diameter) stainless-steel grids parallel to the
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front wall. The lever was positioned to the left of the food cup, and a dish containing Vicks Vaporub was outside the chamber. The boxes in Sets 3 and 4 measured 31.75 24.13 29.21 cm. Two walls and ceiling were made of clear acrylic, while the remaining walls were aluminum. In Set 3, the floor was stainless-steel grids (0.48 cm in diameter) spaced 3.18 cm center-to-center. A side wall and ceiling were striped. The lever was positioned to the right of the food cup, and a 4% McCormick anise extract solution was in a dish outside the chamber. In Set 4, the floor was made of alternating grids of different diameters (0.48 and 1.27 cm) separated by 1.59 cm (centerto-center). One wall and ceiling were covered with rows of large dark dots. The lever was positioned to the left of the food cup, and an 8% McCormick coconut extract solution was in a dish outside the chamber. The fifth and sixth sets of boxes each measured 30.5 24.1 21 cm. Two walls were aluminum, while two walls and the ceiling were clear acrylic. In Set 5, the floor consisted of 0.48-cm (diameter) bars that were spaced 1.6 cm center to center and mounted parallel to the front wall. The lever was to the left of the food cup, and odor was provided by a Citrus oil room freshener outside the chamber. In Set 6, the floor consisted of similar bars that they were ‘‘staggered’’ such that the height of adjacent bars differed by 1.6 cm. The lever was to the right of the food cup, and odor was provided by Pine-Sol. In all boxes, illumination was provided by two 7.5-w incandescent bulbs mounted to the ceiling of the sound attenuation cubicle. The CS was a 60-s presentation of a 3000-Hz tone (80 dBA) delivered through a 7.6 cm speaker mounted to the ceiling of the sound attenuation chamber, approximately 27 cm above each grid floor. Background noise level was 60 dBA in all boxes. The footshock US was a 0.5-s 1.0-mA footshock provided by Med Associates ENV-414 shock sources. Lever pressing was reinforced with 45-mg Noyes precision food pellets (Research Diets, Inc., New Brunswick, NJ). The apparatus was controlled by computer equipment located in an adjacent room. Procedure Baseline training. The rats were first trained to lever press in four contexts over eight 50-min daily sessions. In the first two sessions, all rats received shaping in the box that would become Context B. In the first session, the first 30 lever presses were reinforced; an FR-7 schedule was then in place for the next 5 reinforcers, after which a VI-90 schedule that was used for the rest of the experiment went into effect. In the second session, the first 5 responses were reinforced before the VI-90 schedule took effect. (This was the procedure for every session in the remainder of the experiment.) After these two sessions in Context B, the rats then received daily sessions in Context C, C, D, D, E, and E. As mentioned above, box Sets 1, 2, 3, and 4 were assigned as Contexts B, C, D, and E for individual rats by means of a Latin Square. Conditioning. Fear conditioning then began in Context A on the next day. In each of four daily sessions, there were three presentations of the tone CS, each terminating in the onset of the footshock. The intertrial interval was variable with a mean of 20 min. The first conditioning session involved an extra 15 min of responding on the VI baseline at the start (before the Pavlovian schedule was initiated) to give the animals practice lever pressing in these new contexts. By the end of the phase, all rats had received a total of 12 pairings of the tone and the 0.5-s, 1-mA shock. On the day following the conclusion of fear conditioning, the animals had a baseline recovery session (following the usual baseline training procedure) in Context E. Extinction. There were then three daily sessions of extinction, each containing four presentations of the tone alone (mean ITI ¼ 10 min) while the rats were lever pressing. The first session was conducted in Context B for all animals. After that session, the rats were randomly assigned to two groups (n ¼ 16) in a manner that maintained the box balancing. On the two days that followed, Group ABBBE received two further extinction sessions in Context B. Group ABCDE, in contrast, received an identical treatment in Contexts C and then D. Renewal test. On the day following the last extinction session, all rats were given four tone-alone trials while lever pressing in Context E. The first test trial occurred 15 min after the start of this 50-min session.
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Data analyses. Suppression to the tone was indexed in terms of suppression ratios, x=ðx þ yÞ, where x represents the number of lever presses made during the CS and y represents the number of lever-presses made in the equivalent period prior to the onset of the CS (pre-CS period). A ratio of 0 indicates complete suppression of responding during the CS, while a ratio of 0.5 indicates no response suppression during the CS. Suppression ratios were analyzed using analyses of variance (ANOVA). Parallel analyses were also conducted on responding during the pre-CS period. The rejection criterion was always po:05. Two rats in Group ABCDE were removed from the experiment because they showed no evidence of successful fear conditioning (e.g., suppression ratios4.43 on each trial of the first extinction session). Results Fig. 1 shows the suppression of the two groups on each trial of extinction and final renewal testing (far right). As the figure suggests, Group ABCDE was more afraid of the CS during extinction, because the context changes between the extinction sessions caused modest renewal effects. However, despite this difference between groups during extinction, they showed a comparable renewal of suppression when the tone was tested in Context E. These impressions were confirmed by statistical analyses, which focused on the transitions between sessions. A Group Trial ANOVA on the last trial of the first extinction session and the first trial of the second session revealed a significant Group Trial interaction, F ð1; 28Þ ¼ 4:30, as well as a Trial effect, F ð1; 28Þ ¼ 12:61. The Group effect was not significant, F ð1; 28Þ ¼ 1:78. Pairwise comparisons exploring the interaction indicated that Group ABCDE’s suppression increased between the sessions, F ð1; 28Þ ¼ 14:71, whereas Group ABBBE’s did not, F ð1; 28Þ ¼ 1:22. A compatible pattern was evident in a similar ANOVA on the last trial of the second session and the first of the third. Here there was a Group effect, F ð1; 28Þ ¼ 5:37, as well as a Trial effect, F ð1; 28Þ ¼ 7:82, although the interaction was not significant, F ð1; 28Þo1. Although the figure suggests that both groups increased suppression across these trials, pairwise comparisons indicated that the increase was significant again in Group ABCDE, F ð1; 28Þ ¼ 6:35, but not in Group ABBBE, F ð1; 28Þ ¼ 2:17. The results
0.6 ABCDE
Suppression Ratio
0.5
ABBBE
0.4
0.3
E
0.2 D 0.1 C 0.0
B Trials Extinction
Test
Fig. 1. Mean suppression to the tone for Groups ABCDE and ABBBE during each trial of extinction (left) and the final renewal test (right) in Experiment 1.
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Table 1 Correlations between extinction performance and renewal test performance in Experiment 1 Extinction and test trials correlated
1 1–2 1–4
Correlations, r Extinction session
Partial correlations, r Extinction session
1
2
3
df
2
3
df
.18 .50* .48*
.31 .41* .40*
.05 .32 .42*
28 28 28
.08 .06 .11
.10 .16 .32
27 27 27
*po:05.
thus suggest that there were renewal effects in Group ABCDE at the start of Sessions 2 and 3, coincident with each context switch. Despite these effects of the context manipulation, the groups showed comparable renewal during the final test session in Context E. Here the Group Trial ANOVA on the last extinction trial and the first test trial indicated only a significant Trial effect, F ð1; 28Þ ¼ 9:87. Neither the Group effect, nor the Group Trial interaction, approached significance, F’s(1,28)o1. Another Group Trial ANOVA on the four trials of the final renewal test similarly revealed a significant Trial effect, F ð1; 28Þ ¼ 10:86, indicating a decrease in suppression (further extinction) over testing, but the Group main effect and the Group Trial interaction did not approach significance, F ’sð1; 28Þo1. There was no evidence in this experiment that extinction in multiple contexts affected the size of the final renewal effect. We performed identical ANOVAs on the pre-CS scores. No effects or interactions were significant; all F’s were less than 1 except for the Trial effect on the Session 2–3 transition, F ð1; 28Þ ¼ 3:36, and the Group effect on Session 3-Renewal test transition, F ð1; 28Þ ¼ 1:7. Groups ABBBE and ABCDE had mean pre-CS scores of 24.4 and 24.2 during extinction and 20.7 and 25.8 during the final renewal test, respectively. To further examine the relationship between the level of suppression in extinction and the final renewal effect, we calculated correlations between the rats’ suppression during different extinction sessions and during the final renewal test. The correlations are summarized in Table 1. The data were aggregated in several ways. The first row summarizes the correlations between the first trial of the corresponding extinction session and the first trial of the final renewal test; the second row summarizes the correlations between the average of the first two trials of the corresponding extinction session and the average of the first two trials of the final renewal test; and the third row summarizes the correlations between the average of the four trials of the corresponding extinction session and the four trials of the final renewal test. If anything, the correlations were positive, and significantly so when the data were aggregated in two- and four-trial blocks. In other words, rats that showed the most fear during extinction also tended to show the most fear during renewal testing. This result appears to reflect individual differences in the extent of original fear conditioning. The right columns summarize the partial correlation coefficients that partialled out suppression on the first two-trial block of Extinction Session 1, which was mainly affected by conditioning rather than extinction. (We were unable to use data from actual conditioning sessions because the pre-CS scores there were too suppressed.) None of the partial correlation coefficients approached significance. Thus, although the correlation between fear during extinction and renewal testing Context E was positive, this was due to the fact that rats that emerged from conditioning with strong fear of the tone also showed the strongest renewal in the end. Discussion The final tests in Context E revealed an increase in suppression that may be attributed to a renewal effect. Similar renewals were also observed during the extinction phase. That is, the context switches in extinction that Group ABCDE received caused increases in suppression that were not observed in the control group (Group ABBBE). Although the suppression of Group ABCDE during the extinction sessions confirm that the multiple-context treatment had an effect on behavior, and that the animals thus perceived the contexts as different, extinction in multiple contexts did not demonstrably reduce the size of the final renewal effect in
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Context E. Extinction was no less vulnerable to renewal after the multiple-context extinction procedure than after a standard single-context procedure. This result is compatible with the finding that fear of the CS during the final renewal test was positively related to fear during extinction. This pattern may be inconsistent with the view that high responding in extinction ensures better, or more permanent, extinction learning (cf. Rescorla, 2001; Solomon & Wynne, 1954). Instead, the correlational analyses suggest that individuals that acquired strong fear during conditioning also showed strong fear during extinction and during the final renewal test. Higher levels of suppression in extinction did not make extinction less context-specific; renewal of fear was still observed. Experiment 2 Experiment 1 studied the so-called ‘‘ABC’’ renewal effect in which fear is renewed when the CS is tested in a neutral context that has not been previously associated with either extinction or conditioning. It seemed possible that the lack of attenuation of renewal by extinction in multiple contexts was peculiar to that renewal design. Another commonly studied design is ‘‘ABA’’ renewal, in which final renewal is caused by return to the original conditioning context (Context A). Unlike renewal in the ABC design, which depends exclusively on release from some inhibitory process controlled by the extinction context, renewal in the ABA design can reflect both release from inhibition and a positive modulation of responding by the original conditioning context. Chelonis et al. (1999) used an ABA design. It was conceivable that extinction in multiple contexts might provide a better hedge against this type of renewal effect. Experiment 2 was therefore designed to extend the generality of Experiment 1 by comparing groups that received extinction in single or multiple contexts on the strength of their renewal when tested in the original fear-conditioning context, Context A. Method Subjects and apparatus The subjects were 32 female Wistar rats of the same age and from the same supplier as those in Experiment 1. The apparatus was four sets of four boxes (Sets 1, 2, 3, and 4) described in the previous experiment. Procedure Baseline training, conditioning, and extinction were the same as in Experiment 1 except as noted. During baseline training, the rats received shaping and practice lever pressing in the order Contexts BBCCDDAA. Four conditioning sessions then followed, each 50 min in duration, and each containing three tone-shock pairings. There was then a baseline recovery session in Context A, and then extinction in three sessions conducted in Context B (Group ABBBA) or in B, C, and D (Group ABCDA). (As before, the groups were matched on their suppression in Context B during the first extinction session.) In the final renewal test (conducted the day after the last extinction session), all rats received four tone presentations in Context A—the original fear conditioning context. As before, the first tone was presented 15 min after the start of the session. Results Fig. 2 summarizes the suppression of the two groups on each trial of extinction and renewal testing. The results were consistent with those of Experiment 1. The multiple-context group, Group ABCDA, was again more afraid of the CS during extinction, because each context change caused a renewal effect. However, despite this effect, the two groups showed comparable renewal when they were returned to the original conditioning context (Context A). Statistical analysis followed the strategy used in Experiment 1. A Group Trial ANOVA on the last trial of the first extinction session and the first trial of the second revealed nonreliable Group and Group Trial effects F’s(1,30)o1. The trial effect was highly significant, F(1,30) ¼ 6.24. Pairwise comparisons indicated that Group ABCDA increased suppression between trials, F(1,30) ¼ 6.03, whereas Group ABBBA did not, F(1,30) ¼ 1.50. The ANOVA on the Session 2–3 transition revealed a Trial effect, F(1,30) ¼ 22.32, and a Group Trial interaction, F(1,30) ¼ 5.35, although the group effect was not reliable, F(1,30) ¼ 2.31. Pairwise
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0.6
ABCDA ABBBA
Suppression Ratio
0.5
0.4
0.3
0.2 A C
0.1
D
B
0 Trials Extinction
Test
Fig. 2. Mean suppression to the tone for Groups ABCDA and ABBBA during each trial of extinction (left) and the final renewal test (right) in Experiment 2.
comparisons again indicated that Group ABCDA’s increase in suppression was significant, F(1,30) ¼ 25.00, whereas Group ABBBA’s was not, F(1,30) ¼ 2.56. Like the results of Experiment 1, the results of this experiment suggest that extinction in multiple contexts causes more suppression—through successive renewal effects—in extinction. The groups did not differ, however, on the last extinction trial, F(1,30) ¼ 2.65. Despite the effectiveness of the independent variable in extinction, there was no demonstrable difference between the groups in the final renewal effect. Here the Group Trial ANOVA on the last extinction trial and the first test trial once again indicated only a significant Trial effect, F(1,30) ¼ 8.39. Neither the Group effect, F(1,30) ¼ 1.48, nor the Group Trial interaction, F(1,30)o1, approached statistical significance. An ANOVA comparing the groups’ suppression on all four trials of the final renewal test revealed a significant Trial effect, F(3,90) ¼ 14.65. But there was no Group effect, F(1,30) ¼ 1.01, or Group Trial interaction, F(3,90) o1. The results failed to confirm that extinction in multiple contexts reduces the size of the ABA renewal effect. Identical analyses were conducted on the pre-CS scores. These indicated no Group, Trial, or Group Trial interactions, largest F(1,30) ¼ 2.80. Groups ABBBA and ABCDA had (respective) mean pre-CS scores of 20.4 and 20.0 during extinction and 23.5 and 28.6 during the final renewal test. Table 2 summarizes the correlations between tone fear during the extinction sessions and during final renewal testing. In this experiment, the correlations were mostly nonsignificant, although at the highest level of aggregation (four-trial blocks), there was once again a significant positive correlation between fear during the first extinction session and fear during the final renewal test. It is interesting that the correlations were lower here than in Experiment 1. The difference may reflect random variation between experiments, or the fact that fear during extinction in neutral contexts (Contexts B, C, D) is a better predictor of fear in another neutral context (Context E; Experiment 1) than in the original conditioning context (Context A; current experiment). Discussion The results of Experiment 2 were consistent with those of Experiment 1: despite the fact that testing was now conducted in the original fear-conditioning context, extinction in multiple contexts had no detectable
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Table 2 Correlations between extinction performance and renewal test performance in Experiment 2 Extinction and test trials correlated
1 1–2 1–4
Correlations, r Extinction session
Partial correlations, r Extinction session
1
2
3
df
2
3
df
.12 .06 .36*
.16 .13 .10
.19 .17 .08
30 30 30
.26 .18 .02
.23 .20 .03
29 29 29
*po:05.
effect on the strength of the final renewal effect. This, along with the results of the correlational analyses, once again suggest that higher responding in extinction does not produce a more permanent (or less contextspecific) extinction effect. Experiment 3 The findings of Experiments 1 and 2 failed to replicate results previously reported by Gunther et al. (1998) and Chelonis et al. (1999). There were, of course, many differences between the present experiments and the previous ones. However, one difference that might be especially important is that our conditioned suppression method required that the rats be trained to lever press in each of the contexts before conditioning, extinction, and renewal testing. One consequence was that each of the contexts had been associated with the same foodpellet reinforcer. This common association could have encouraged generalization between the contexts through the process of mediated generalization (e.g., Honey & Hall, 1989), and thus reduced the effect of extinction in multiple contexts. Of course, the fact that the context switches in extinction caused demonstrable renewal effects indicates that the rats did not generalize completely between them. Nonetheless, the experiments by Gunther et al. and by Chelonis et al. did not involve presenting a common reinforcer in each context. Experiment 3 therefore compared ABBBE groups and ABCDE groups as in Experiment 1 in a method in which Context E was the only context in which the rats received reinforcers and lever-press training. This method was more directly analogous to that of Gunther et al. (1998), and might theoretically reduce generalization between the various contexts in Group ABCDE. Method Subjects and apparatus The subjects were 32 female Wistar rats of the same age and from the same supplier as those in Experiments 1 and 2. The apparatus was the same sets of boxes used in Experiment 1. During conditioning and extinction, however, the levers were removed. Procedure The procedure was identical to that described in Experiment 1 with the following exceptions. During baseline training, the rats received shaping and VI practice in eight sessions in Context E only. Conditioning and extinction were then conducted in the various contexts with the levers removed. There were four sessions of conditioning in Context A (three tone-shock pairings in each), followed by three sessions of extinction (four tone alone trials) in Context B (Group ABBBE) or B, C, and D (ABCDE). After the final extinction session, the rats received a baseline recovery session in Context E, and on the following day four final tests of the CS while lever pressing in Context E.
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0.6
Suppression Ratio
0.5
0.4
0.3 ABCDE ABBBE 0.2
0.1
0 Trials Renewal Test Fig. 3. Mean suppression ratio to the tone for Groups ABCDE and ABBBE during the renewal test of Experiment 3.
Results and discussion The results of the test session are summarized in Fig. 3. As the figure suggests, there was once again a modest renewal effect in both groups, and no hint of a difference in its size. A Group Trial ANOVA on the test data revealed a significant Trial effect, F ð3; 90Þ ¼ 10:59, that indicated extinction of suppression (as usual) over the four test trials. But the Group effect, F ð1; 30Þo1, and the Group Trial interaction, F ð3; 90Þ ¼ 1:12, failed to approach reliability. An identical analysis on the pre-CS scores revealed nonsignificant effects of Trial, F ð3; 90Þ ¼ 2:34, p ¼ :078, Group, F(1,30) o1, or Group Trial, F ð3; 90Þ ¼ 1:71. The mean response rates during the pre-CS periods were 24.87 and 26.89 for Groups ABBBE and ABCDE, respectively. Despite the absence of a common reinforcer in the various contexts, Experiment 3 produced results that paralleled those of the previous experiments perfectly. Under a range of conditions, we have produced no evidence that extinction in multiple contexts reduces the strength of renewal compared to that observed in a group that receives extinction in only one context.
General discussion The results of these experiments suggest that extinction in three different contexts does not necessarily reduce the renewal of fear that occurs when animals are tested in either a fourth neutral context (Experiments 1 and 3) or in the original fear conditioning context (Experiment 2). The results suggest that neither the ABC nor the ABA renewal effect is reduced by extinction in multiple contexts in the fear-conditioning method that has been used extensively in this laboratory (e.g., Bouton & Brooks, 1993; Bouton & King, 1983; Bouton & Ricker, 1994; Bouton & Swartzentruber, 1989). The results thus imply that there are important variables that modulate the impact that extinction in multiple contexts had on the renewal effect in earlier experiments (Chelonis et al., 1999; Gunther et al., 1998). In fact, the earlier reports had already suggested the operation of modulating variables. For example, Chelonis
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et al. (1999, Experiment 2) failed to replicate the attenuation of renewal by extinction in multiple contexts when the rats were given equivalent exposure to all the contexts during extinction. (This is in fact why we did not include such control exposures in the present experiments.) In addition, Gunther et al. (1998) found that the advantage of extinction in multiple contexts was reduced if fear conditioning was also first conducted in multiple contexts. That is, although extinction in B, C, and D reduced the renewal effect when conditioning had only been conducted in Context A, it had substantially less effect if conditioning had first been conducted in Contexts A, A0 , and A00 . It is possible that conditioning in multiple contexts in this manner is closer to what occurs in everyday life. All told, the results of the present and earlier experiments clearly indicate that extinction in multiple contexts does not guarantee the prevention of renewal. Bouton, Woods, Moody, Sunsay, and Garcı´ a-Gutie´rrez (in press) recently reviewed animal laboratory research that has investigated ways in which extinction procedures can be modified to help reduce relapse effects like renewal. Although the literature suggests that treatments designed to enhance extinction learning (including extinction in multiple contexts) are occasionally helpful, one approach that seems to have consistent promise is to provide explicit ‘‘bridges’’ between the therapy (extinction) context and contexts where relapse is likely to be a problem. For example, a therapist might accept the possible context-specificity of extinction and conduct extinction directly in the contexts where lapses might occur. Alternatively, the therapist might provide retrieval cues that can be presented or used in a potential relapse context to help retrieve the extinction experience (e.g., Brooks & Bouton, 1993, 1994; Collins & Brandon, 2002). The results of the present experiments are interesting from a theoretical standpoint. Perhaps most clearly, they suggest that higher levels of responding in extinction (as shown in the multiple-context groups) did not produce a more thorough extinction effect that was less vulnerable to relapse. This finding, along with correlational analyses that never revealed a significant negative relationship between the level of fear in extinction and the level of fear observed during the final renewal test, suggest that evoking high levels of fear during extinction or exposure therapy may not yield a more durable therapeutic effect (e.g., Marks, 1978). From a learning-theoretical perspective, if higher levels of fear in extinction do allow stronger response inhibition to develop (Rescorla, 2001), that response inhibition must still be at least partly specific to the context(s) in which it is learned. The current results suggest that neither extinction in multiple contexts nor high levels of responding in extinction necessarily prevents the renewal effect, one of several possible mechanisms of clinical relapse that have been investigated in the animal laboratory. Acknowledgments This research was supported by Grant RO1 MH64847 from the National Institute of Mental Health. References Bouton, M. E. (1991). A contextual analysis of fear extinction. In P. R. Martin (Ed.), Handbook of behavior therapy and psychological science: An integrative approach (pp. 435–453). Elmsford, NY: Pergamon Press, Inc. Bouton, M. E. (2002). Context, ambiguity, and unlearning: Sources of relapse after behavioral extinction. Biological Psychology, 52, 976–986. Bouton, M. E. (2004). Context and behavioral process in extinction. Learning & Memory, 11, 485–494. Bouton, M. E., & Bolles, R. C. (1980). Conditioned fear assessed by freezing and by the suppression of three different baselines. Animal Learning & Behavior, 8, 429–434. Bouton, M. E., & Brooks, D. C. (1993). Time and context effects on performance in a Pavlovian discrimination reversal. Journal of Experimental Psychology: Animal Behavior Processes, 19, 165–179. Bouton, M. E., & King, D. A. (1983). Contextual control of the extinction of conditioned fear: Tests for the associative value of the context. Journal of Experimental Psychology: Animal Behavior Processes, 9, 248–265. Bouton, M. E., Mineka, S., & Barlow, D. H. (2001). A modern learning-theory perspective on the etiology of panic disorder. Psychological Review, 108, 4–32. Bouton, M. E., & Ricker, S. T. (1994). Renewal of extinguished responding in a second context. Animal Learning & Behavior, 22, 317–324. Bouton, M. E., & Swartzentruber, D. (1989). Slow reacquisition following extinction: Context, encoding, and retrieval mechanisms. Journal of Experimental Psychology: Animal Behavior Processes, 15, 43–53. Bouton, M. E., & Swartzentruber, D. (1991). Sources of relapse after extinction in Pavlovian and instrumental learning. Clinical Psychology Review, 11, 123–140.
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