Predictability and controllability: Differential effects upon contextual fear

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Predictability and Controllability: Differential Effects upon Contextual Fear ROBERT A. ROSELLINI,DONALD State

University

A. WARREN, AND JOSEPH P. DECOLA of New

York

at Albany

The independence of action of controllability and predictability has recently been questioned by research demonstrating that the effects of control over shock termination can be mimicked by feedback stimuli when a contextual fear measure is used. This suggests that the varied effects of controllability, particularly controllability of shock termination, may result not from controllability per se but from predictability of shock absence. The present experiments address this issue by examining whether controllability and predictability similarly affect contextual fear under several parametric conditions. In Experiment 1, control over shock termination was found to reduce contextual fear at an earlier point in training than prediction of shock absence. Experiment 2 demonstrated an effect of controllability under conditions in which the feedback effect is precluded. Experiment 3 examined the possibility that the group differences observed in the above experiments could be due to a potential difference in the conditionability of the response-produced stimulation and the external feedback stimulus. The outcome of this study makes it unlikely that this is the case, since no evidence of overshadowing of the feedback stimulus was observed on a test of its associative strength. These experiments suggest that the effects of controllability may not be reducible to those of predictability. Furthermore, they have important implications for theoretical proposals concerning the effect of feedback on contextual fear. 0 1987 Academic Press. Inc.

Exposure to uncontrollable aversive events has been demonstrated to have associative, motivational, neurochemical, and emotional consequences (for reviews see Maier & Jackson, 1979, Maier & Seligman, 1976). It proactively interferes with the organism’s ability to acquire a responseoutcome association when tested using electric shock termination as the outcome (Jackson, Alexander, & Maier, 1980; Minor, Jackson, & Maier, 1984) or even when the outcome is availability of food (Rosellini, 1978; Donald A. Warren is now at the Department of Psychology, University of Colorado. We thank Dr. Mark Plonsky and Joanne M. Rosellini for their cogent comments on the manuscript and Janet Stampler and Craig Parlato for assistance in the execution of this research. Requests for reprints should be sent to Robert A. Rosellini, Department of Psychology, SUNY-Albany, Albany. NY 12222. 392 0023-9690187 Copyright All rights

$3.00

Q 1987 by Acadermc Press, Inc. of reproduction in any form reserved.

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Rosellini, DeCola, & Shapiro, 1982). It results in decreased general activity and produces deficits in initiating responding in the presence of electric shock (Anisman, de Catanzaro, & Remington, 1978; Jackson et al., 1980; Minor et al., 1984). It has been shown to have a variety of neurochemical effects such as modification of cholinergic (Weiss et al., 1981), serotonergic (Sherman & Petty, 1980), and GABAergic (Petty, 1986) systems. Other physiological/neurochemical -effects have also been reported following exposure to uncontrollable shock, such as analgesia (e.g., Jackson, Maier, & Coon, 1979) and altered immune system function (e.g., Laudenslager, Ryan, Drugan, Hyson, & Maier, 1983, Visintainer, Volpicelli, & Seligman, 1982). An additional effect of exposure to uncontrollable shock which is of particular interest is the observation that such exposure has emotional consequences. Weiss (197 1) has shown that it can lead to increased ulcers as compared to an animal exposed to controllable shock or not exposed to shock. Osborne, Mattingly, Redmond, and Osborne (1975) have demonstrated such exposure to results in heightened levels of fear (see also Desiderato & Newman, 1971; Mowrer & Viek, 1948). Historically, these varied effects of uncontrollable aversive events have been interpreted by proponents of learned helplessness theory as resulting from the acquisition of an expectancy of response-reinforcer independence. This interpretation has been advanced and supported on the basis of the triadic design which is typically used to investigate learned helplessness effects. As argued by Maier and Seligman (1976), these effects should be attributed to the uncontrollable nature of the aversive event and not simply to exposure to the event per se. This is because they are only observed in animals for which the event is uncontrollable, and not in animals which have control over the event, or in animal not exposed to the event. Although, this argument has not been without its critics (e.g., Church, 1964; Levis, 1976), learned helplessness theorists have argued compellingly for its validity (see Maier & Seligman, 1976; Maier & Jackson, 1979). A number of recent findings question the basic claim of learned helplessness theory that the varied learned helplessness effects stem from the uncontrollability of the aversive event. Mineka, Cook, and Miller (1984) found that exposure to uncontrollable shock produces higher levels of fear to a context than does equivalent exposure to controllable shock. They also reported that if animals exposed to uncontrollable shock are provided with a brief stimulus following shock termination (i.e., a feedback stimulus), they show no more fear of the shock context than do animals exposed to controllable shock. These observations suggest that the effects of exposure to uncontrollable shock upon the conditioning of contextual fear, and possibly other “learned helplessness” effects, may stem from the unpredictability of shock absence and not from uncontrollability of the aversive event. Furthermore, Mineka et a/. (1984) have found that

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providing a feedback stimulus to an animal which has control over shock termination does not reduce fear of the context compared to an animal which has control but no feedback stimulus. Based on this finding, they suggested that these effects on contextual fear are due solely to the predictability of shock absence, since they would expect an additive effect if fear in this situation were independently affected by controllability and predictability (Mineka et al., 1984, see Experiment 3, p. 316). According to this view, the only function of controllability in this situation is that the emission of the response will result in proprioceptive stimulation which signals a period free of shock and thereby reduces the level of fear. Thus, in controllably shocked animals, the response-produced stimulation is held to function like the feedback stimulus in uncontrollably shocked animals. These data are particularly important for learned helplessness theory since they suggest that many-if not all-of the effects of exposure to uncontrollable aversive events which have been attributed to uncontrollability may indeed be due to the unpredictability of the absence of the event. The data reported by Mineka et al. (1984) are clear in demonstrating that the lowered level of fear in animals having control over shock termination compared to inescapably shocked animals can be mimicked by introduction of a feedback stimulus, and they suggest predictability as the responsible variable. However, given the theoretical importance of this possibility, the issue warrants further examination. One would have m-ore confidence in this conclusion if it were observed that experimental manipulations which are known to affect the power of a feedback stimulus have the same effect in animals which have control over shock termination. EXPERIMENT

1

In this experiment, the number of training trials was manipulated to determine whether this variable has the same effect on animals which have control over shock termination and those exposed to inescapable shock with a feedback stimulus. If the effect of controllability on the acquisition of fear to the shock context is indeed reducible to predictability, as suggested by Mineka et al. (1984), then this variable would be expected to influence contextual fear in the two groups in a similar manner. On the other hand, any differential effect would demonstrate an empirical separation of the effect of control and of the feedback stimulus which would begin to suggest that controllability and predictability exert their influence via separate mechanisms. An additional reason for choosing this variable is based on an examination of the considerable literature which has implicated the role of Pavlovian conditioned inhibition in the development of the effects of feedback stimuli on avoidance behavior (e.g., Belles, 1970; Belles & Grossen,

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1969; Morris, 1975; Weisman & Litner, 1972). Feedback stimuli from avoidance training situations have been demonstrated to function as Pavlovian conditioned inhibitors (Weisman & Litner, 1972), and conditioned inhibitors can function as feedback stimuli in an avoidance situation (Morris, 1975). Furthermore, variables known to influence the development of conditioned inhibition to a CS, such as intertrial interval (ITI) length (Moscovitch & LoLordo, 1968; Weisman & Litner, 1971), are known to influence the power of a feedback stimulus to modify avoidance behavior (Morris, 1974). These studies strongly suggest that the development of Pavlovian conditioned inhibition to the feedback stimulus is essential to its ability to modify avoidance behavior. Furthermore, Rosellini, DeCola, and Warren (1986) have reported an effect of ITI length upon the ability of the feedback stimulus to reduce the amount of fear conditioned to the shock context. This implicates conditioned inhibition as important for the effect of feedback on reduction of fear to the shock context. Given this apparent link between the effectiveness of feedback stimuli and conditioned inhibition, the present experiment should also provide important data concerning the development of the feedback effect on contextual fear which can be compared to our knowledge of the effects of this manipulation on the development of Pavlovian conditioned inhibition. To this end, the present experiment was modeled after that of Weisman & Litner (1971) in manipulating number of training trials since they found that 80 trials were necessary to obtain fear inhibitory properties by a CS- in a Pavlovian conditioning situation. It is therefore of interest to determine whether the effects of control require a comparable number of trials. One of three levels of training (20,40, or 80 trials) was administered for each of three shock training conditions (escapable shock, yokedinescapable shock with a feedback stimulus, and yoked-inescapable shock with no feedback stimulus). Method Subjects. The subjects were 104 experimentally naive male Holtzman rats, approximately 100 days of age at the start of the study. All animals were housed individually under conditions of ad lib food and water. All procedures were conducted during the light phase of a 12-h light/dark cycle. Apparatus. The same four chambers were used to administer the shock training and the fear test for this study. Each measured 21.0 x 30.5 x 27.9 cm. The walls were constructed of aluminum, and the ceiling and door of clear Plexiglas. The floor consisted of stainless steel rods 3.0 mm in diameter and spaced 1.2 cm apart. A lever, measuring 3.0 x 1.0 cm, was centered on the front wall of the chamber, 3.8 cm above the grid floor and protruding 2.3 cm into the chamber. A 28-V dc house light was located 29 cm above the grid floor and was centered on the front

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wall. White noise (78 dB, scale A) was delivered to the chambers by an 8-ohm speaker mounted behind the front wall. Scrambled shock (0.90 mA) was delivered to the grid floor by solid-state shock sources (Coulbourn Instruments Model 13-16). Each chamber was housed in a light- and sound-attenuating container equipped with a ventilation fan. Control of the escape apparatus and the recording of data were implemented by a TRS-80 microcomputer. The same four chambers were used for both the preexposure and test phases of this study. However, for these phases the chambers were modified by inserting a wooden platform (19 x 12 cm) in the rear of the chamber. This platform was elevated 4 cm above the grid floor. A clear Plexiglas door was used to limit accesss to the chamber when appropriate. Procedure. This experiment consisted of three phases: (a) preexposure, (b) shock training, and (c) fear test. Preexposure. This phase was conducted on the first day of the study. The animal was placed on the platform and retained there for 15 min. The house light and the white noise were present during this phase. Subjects were then randomly assigned to each of the nine experimental groups. Shock training. The design of this phase of the study was a 3 x 3 factoria1 consisting of three shock training conditions-escapable (ES), yoked shock with a feedback stimulus (YS-FB), and yoked shock without a feedback stimulus (YS-NF)-crossed with three different amounts of shock training-20, 40, or 80 trials. The shock training was conducted on Day 2 of the study. The three escape groups were given either 20, 40, or 80 trials of shock escape training (ZVs = 12, 12, and 11, respectively). For each of these groups, the initial 15 trials required a single barpress to terminate shock (FR-1). and the remaining trials required two responses (FR-2). If an animal failed to meet the ratio criterion, shock was terminated 30 s from onset. Trials were administered on a random time 90-s schedule. The ITI values were equiprobable within a range of 60-120 s. The animals in the other two shock training conditions were exposed to yoked shock so that they received the same pattern and duration of shock as animals in the corresponding escape group (i.e., 20, 40, or 80 trial condition). The three groups in one of these two conditions (e.g., YS-FB-20, YS-FB-40, and YS-FB-80) were presented a feedback stimulus compound consisting of a 3-s interruption of the house light and white noise, which were otherwise present. Feedback stimulus onset was simultaneous with shock termination. The three groups in the other yoked shock condition (e.g., YS-NF-20, N = 12; YS-NF-40, N = 12; and YS-NF-80, N = 11) were not presented a feedback stimulus. Fear test. The last phase of the study commenced on Day 3 of the experiment and was conducted for 4 days. This test was identical to that

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employed by Rosellini et al. (1986). It consisted of placing the animal on the platform for a 15min period, then permitting 15min of access to the chamber. Both the white noise and the house light stimuli were present for the duration of the test. These sessions were recorded on videotape and were later scored by observers who were blind to the animals’ treatment conditions. A second observer, who was also blind to experimental conditions, scored a random sample of the test sessions to obtain a reliability check. The interrater reliability was .98 or greater for each of the present experiments. The dependent measure was the total amount of time the animal spent on the grid floor during each test session. Grid floor time was defined as the time from when the animal placed both rear paws on the grid to when it removed both rear paws from the grid (i.e., both rear paws on the platform). Since the raw data collected with this measure is skewed, it was normalized by means of a square root transformation (see Rosellini et al., 1986). Results Shock escape training. The three levels of training resulted in each of the three escape training groups, and consequently the two groups yoked to each of these, receiving different total amounts of shock. The 20-trial escape group received a mean total of 77.5 s of shock (SD = 23.4). The 40-trial escape group received a mean total of 191.7 s of shock (SD = 95.68). The go-trial escape group received a mean total of 253.5 s of shock (SD = 123.2). During the shock escape training, all animals in the escape condition acquired the escape response as indicated by the absence of failures to escape shock on the last five trials of training. In addition, the trials manipulation resulted in an orderly decrease in latency to escape, indicating the gradual acquisition of the escape response. The mean escape latencies on the last five trials of training for the 20-, 40-, and the go-trial escape groups were 5.67, 3.96, and 2.24, respectively. An analysis of variance (ANOVA) showed a significant difference among the three levels of training (F(2, 32) = 5.30, p < .Ol). Subsequent trend analyses revealed only a significant linear trend (F( 1, 32) = 10.23, p < .Ol), indicating that escape latencies decreased as a function of the increasing number of trials. Thus, the trial manipulation was successful in achieving its intended aim of bringing the three different escape groups to different levels of escape performance and presumably different levels of learning. Fear test. The amount of fear of the shock training chamber during the 4 days of the fear test varied both as a function of shock training condition (i.e., ESC, YS-FB, and YS-NF) and number of training trials administered (i.e., 20, 40, and 80). Figure 1 shows the mean transformed total grid time (TGT), the index of fear, as a function of the two experimental variables across the 4 test days. As can be seen in the left panel of Fig.

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FIG. I. Mean transformed time spent on the grids across 4 test days as a function of shock condition (ESC = escape, YNF = yoked shock, no feedback, YFB = yoked shock, feedback), and amount of training (20, 40, or 80 trials).

1, animals exposed to only 20 trials of training showed some extinction of fear as indicated by the increasing amount of time spent on the grid floor across days. It is also apparent that the amount of time spent on the grid floor was not affected by the type of training experienced in the chamber-whether animals received escape training (Group ESC), yoked shock with a feedback stimulus (Group YS-FB), or yoked shock without a feedback stimulus (Group YS-NF). More interestingly, as the number of training trials was increased to 40 and 80, an effect of training type emerged and did so differentially at each of these two levels of training. The middle panel of Fig. 1 shows that under the 40-trial condition, the group exposed to escapable shock was considerably less fearful of the shock context than either of the yoked shock groups (YS-FB or YSNF), which do not differ from each other. As the number of training trials was increased to 80, yet a different pattern emerged. The right panel of Fig. 1 shows that in this condition, the animals in Group YSNF were the most fearful and the Group ESC animals the least fearful. Each of these groups was approximately equal to their respective group under the 40-trial condition. However, after 80 trials, Group YS-FB animals appeared equivalent to Group ESC and less fearful than the yoked group without the feedback stimulus (YS-NF). These general impressions were confirmd by an ANOVA conducted on the transformed scores as a function of shock type (ESC, YS-FB, and YS-NF), amount of training (20, 40, and 80 trials), and days of the

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test (l-4). The effects of both days (F(3, 285) = 54.45, p < .OOl) and shock type were significant (F(2, 95) = 4.77, p = .Oll). More importantly, the shock type x amount of training interaction was also significant (F(4, 95) = 2.60, p = .040). The source of the two-way interaction was examined by conducting a separate ANOVA (3 x 4) at each level of training. The ANOVA conducted on the 20-trial condition showed only a significant effect of days (F(3, 99) = 12.42, p < .OOl). This resulted from the increasing amount of time spent on the grid floor across the test days, and indicates extinction of contextual fear. However, the three shock groups were statistically indistinguishable, since neither the shock type effect nor the shock type x days interaction was significant (Fs < 1.0). The ANOVA for the 40-trials groups showed the effect of days was significant (F(3, 96) = 20.61, p < .OOl), again indicating extinction of fear across days. In addition, this analysis showed the shock type (F(2, 32) = 7.54, p = .002), and the shock type x days interaction (F(6, 96) = 5.46, p < .OOl) was significant. Two orthogonal contrasts were conducted to assess the source of this interaction. The first of these showed Group YS-FB not to differ from Group YS-NF on any day of the test (Fs (1, 96) < 1.O) and the second showed Group ESC to differ from these two groups on Days 2, 3, and 4 (Fs (1, 96) > 5.9, ps < .Ol). Thus, the two-way interaction stems from the fact that Group ESC showed more rapid extinction of fear than did Groups YS-FB and YS-NF, which did not differ from each other. The ANOVA for the 80-trial condition also showed the effect of days was significant (F(3, 90) = 11.34, p < .OOl). Furthermore, both the shock type (F(2, 30) = 3.32, p = .049), and the shock type x days interaction (F(6, 90) = 2.31, p = .041) were significant. Two orthogonal contrasts were conducted to further assess the source of this interaction. The first of these showed Group YS-FB did not differ from Group ESC on any day of the test (Fs(1, 90) < 2.0, ps > .19), and the second showed these two groups combined to differ from Group YSNF on Days 2, 3, and 4 (Fs(1, 90) > 8.3, ps < .Ol). Thus, the two-way interaction stems from the fact that Group YS-NF showed less rapid extinction of fear than did Groups ESC and YS-FB, which did not differ from each other. Discussion The results of this study demonstrate that the amount of fear conditioned to the shock context is influenced both by the controllability of shock and by predictability of shock absence. The outcome of the fear test for the groups receiving 80 trials of training shows that animals exposed to yoked-inescapable shock with a feedback stimulus are no more fearful of the shock context than animals having control over shock termination, and are less fearful than animals exposed to yoke-inescapable shock

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without a feedback stimulus. This replicates our earlier findings under similar training conditions (Rosellini et al., 1986) and is consistent with the findings of Mineka et al. (1984). Considered in isolation, this finding does indeed suggest, as pointed out by Mineka et al. (1984), that the effects of controllability may be reducible to the effect of predictability of shock absence. If one considers the outcome of the fear test for the groups given 40 trials of training, however, a divergence between the group having control and the group given yoked-inescapable shock with the feedback stimulus is observed. In this case, exteroceptive feedback is not effective in reducing fear as indicated by the equivalence of Group YS-FB and YS-NF and the greater fear expressed by these two groups relative to Group ESC. This outcome demonstrates that controllability of shock exerts an influence on contextual fear at a level of training at which no effect of the feedback stimulus is evident. The present results are also important in that they provide further evidence for the potential involvement of Pavlovian conditioned inhibition in the effect of feedback stimuli on contextual fear. We specifically chose to manipulate the amount of training, since this has been demonstrated by Weisman and Litner (1971) to affect the development of conditioned inhibition in an orderly fashion. They reported that a backward CS does not gain appreciable conditioned inhibitory properties after 40 trials of training when a 60-s minimum ITI is used, but that at least 80 trials of training were necessary for the CS to acquire inhibitory properties as assessed by its ability to modify ongoing avoidance behavior. In spite of the fact that some of the shock training parameters of the present experiment, such as shock intensity (.75 mA vs .90 mA), were different than those employed by Weisman and Litner (1971), the general pattern of our results is consistent with their outcome. We also observed an effect of the feedback stimulus at 80 trials but not at 20 or 40 trials of training. This congruence of outcomes is suggestive of the importance of conditioned inhibition for the observance of an effect of feedback on contextual fear. EXPERIMENT

1B

If a feedback stimulus acquires its power to reduce contextual fear via the acquisition of conditioned inhibitory properties, then these properties should be evident on an independent test of inhibition. The purpose of Experiment 1B was to examine this possibility. This was accomplished by conducting a summation test (Rescorla, 1971) with the three groups of animals which had received shock training with the feedback stimulus in Experiment 1 (i.e., Group YS-FB from the 20-, 40-, and 80-trials conditions). This assessed the conditioned inhibitory properties of the feedback stimulus by testing its power to decrease the amount of suppres-

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sion produced by a separately established Pavlovian fear excitatory stimulus (for a review see LoLordo & Fairless, 1985). An additional group, which had not received feedback during the original shock training, was also tested. The group chosen was YS-NF from the 80-trial condition, since this group was identical to the group of primary interest (Group YSFB-80-trial condition) with respect to shock exposure. Thus, this group served as a control for possible nonassociative effects due to the original training or nonassociative accounts of the test outcome such as external inhibition. Method Subjects. The subjects for this experiment were those of Groups YSFB-80, YS-FB-40, YS-FB-20, and YS-NF-80 from Experiment 1. The animals in each of the four groups were equivalent in body weight prior to being placed on deprivation (F(3, 35) = 1.51, p = .227). Apparatus. Four operant chambers were used for all phases of this study. Each measured 28.3 cm long, 21.7 cm wide, and 20.5 cm high. The two side walls and ceiling were made of clear Plexiglas and the front and back walls were aluminum. The floor consisted of stainless steel rods 0.3 cm in diameter and spaced 1.O cm apart, through which electric shock was delivered (0.30 mA, l-s duration). Centered on the front wall, 2.0 cm above the floor, was a hole 5.0 cm in diameter. The food cup was recessed within this hole and was 3.4 cm deep. A photocell was located 1.5 cm behind the wall in which the food cup was recessed, such that each inspection of the food cup was recorded electronically. Food pellets were delivered to these chambers by pellet dispensers which were mounted outside of the sound-attenuating chambers. Tones ( 1800 cps, 85 dB, Scale A) and white noise (78 dB, Scale A) were delivered via an 8-ohm speaker which was centered on the ceiling of the chamber. Each chamber was enclosed in a sound- and light-attenuating box equipped with a house light and ventilation fan. Procedure. Following completion of Experiment 1, all animals were left undisturbed in their home cages for 1 week. Over the following 7 days, they were gradually reduced to 80% of their free feeding weight. This study consisted of three phases: (a) appetitive baseline training, (b) Pavlovian fear conditioning, and (c) summation test. Appetitive baseline training. The evening before the start of this phase, all animals were exposed to twenty 45-mg Noyes food pellets in their home cage. The first day of appetitive baseline training consisted of first allowing each animal 10 min to consume ten 45-mg Noyes pellets which were placed in the food cup of the chamber. Immediately following this lo-min period, a 60-min session was initiated during which food pellets were delivered on a random time 60-s schedule. The behavior of interest during this session and all subsequent sessions was the number of times

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the animal inspected the food cup. This procedure is modeled after that of Channel and Hall (1983) and has been used successfully in our laboratory to assess appetitive Pavlovian conditioning (see Plonsky & Rosellini, 1986). The second baseline session was identical to the first with the exception that during this session, the stimulus compound which had been used as the feedback stimulus during shock training (i.e., house light and white noise removal), and the tone which was to be used as the conditional excitatory stimulus (CS +), were each presented four times with an IT1 of 480 s. Pavlovian fear conditioning. This phase consisted of three sessions. During each session, four conditioning trials were administered with an ITI of 810 s. Each trial consisted of presentation of a tone of 30-s duration and a l-s shock which occurred during the last 1 s of the CS + , Summation test. The day following the last conditioning session, a summation test was conducted. This consisted of four presentations of the CS + and four summation trials, during which the feedback stimulus was presented in compound with the CS + . The CS + was never reinforced during this phase of the study. Trials were administered with a 480-s ITI. Food pellets were delivered on a RT 60-s schedule throughout the 60-min session. The data were transformed using Annau and Kamin’s (1961) suppression ratio. This ratio takes the form of A/(A+B) where A refers to the number of food cup inspections which occurred during the presence of the 30-s CS, and B refers to the number of inspections occurring during the 30-s period prior to CS presentation. Results Appetitive baseline training. The four groups were equivalent in their level of responding on the 2 days of baseline training (mean Group YSFB-20 = 798.38, Group YS-FB-40 = 853.75, Group YS-FB-80 = 888.33, and Group YS-NF-80 = 829.70; F(3, 35) < 1.0). Pavlovian fear conditioning. As expected, the repeated pairing of the CS+ with the US resulted in a typical pattern of acquisition of fear to the CS as a function of days of training. The suppression ratios for the 3 days of conditioning were 0.43, 0.31, and 0.27, respectively. This yielded a significant effect of days of training (F(2, 70) = 7.65, p < 031). This analysis did not reveal any significant effect of group or a group x days interaction (F(3, 35) < 1.0; and F(6, 70) = 1.43, p = .22). Furthermore, the groups did not differ in their baseline response levels during this phase (Fs < 1.5, ps > .25). The four groups therefore did not differ in their acquisition of fear to the CS + . Summation test. Although no differences between the groups were evident during either baseline or fear conditioning, group differences emerged on the summation test. Figure 2 shows the results of this test for each of the four groups as a function of test stimulus-the CS+ or

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FIG. 2. Mean suppression ratios to the CS+ and the Compound on the summation test as a function of shock condition (YNF = yoked shock, no feedback, YFB = yoked shock, feedback), and amount of training (20, 40, or 80 trials).

the compound stimulus. As is evident in the figure, the groups did not appear to differ in the amount of suppression to the CS + in isolation. However, substantial differences between the groups emerged when the compound stimulus was presented. An ANOVA conducted on these suppression ratios as a function of Group (i.e., YS-FB-20, YS-FB40, YS-FB-80, and YS-NF-80), CS type (i.e., CS + or compound), and trials of test (4) showed a significant effect of trials (F(3, 105) = 5.77, p < .OOl). Inspection of the individual trial mean suppression ratios indicated this stemmed from a general tendency for an increase in suppression ratios (i.e., approach to .50) which was neither differential across groups nor a function of CS type, since no significant interactions with these variables and the trials factor were observed. This analysis also showed a significant effect of group (F(3, 35) = 3.04, p = .042), and most importantly a group X CS type interaction (F(3, 35) = 4.00, p = .015). Inspection of Fig. 2 suggests that this interaction stems from the fact that whereas Groups YS-NF-80 and YS-FB-20 showed almost identical amounts of suppression to the CS+ and the compound, increasing divergence in reaction to the two types of stimuli was observed in Groups YS-FB-40 and YS-FB-80. Newman-Keuls post hoc comparisons confirmed this suggestion. As expected from the similarity of the groups during acquisition of fear to the CS + , the groups also did not differ in amount of suppression to the CS + on the summation test (ps > .lO). Furthermore, Group YS-NF-80, which had not been exposed to the feedback stimulus

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during the original shock training and for whom this stimulus was relatively novel, showed no difference in suppression to the compound and the CS+ (p > .lO). Similarly, Group YS-NF-20, which received only 20 trials of shock training with the feedback stimulus, showed no significant differential reaction to the two types of stimuli (p > .lO). Group YSFB-40, which received 40 trials of training with the feedback stimulus, showed some divergence in reaction to the CS+ and the compound, suggesting that the feedback stimulus did mitigate some suppression to the CS + . However, this difference was only marginally significant (.OS < p < .lO) and as can be seen in Fig. 2, stems primarily from a divergence on the last two trials of the test and not from the initial test trials as would be expected if the feedback stimulus had acquired conditioned inhibitory properties during training. Most importantly, Group YS-FB80, which received more extended training with the feedback stimulus, showed a statistically significant difference in amount of suppression to the CS + and the compound @ < .05), indicating that the feedback stimulus had acquired conditioned inhibitory properties during training. Discussion

The results of this experiment show that the feedback stimulus in the YS-FB-80 animals acquired conditioned inhibitory properties as indicated by its ability to decrease the amount of suppression produced by the CS + . Further evidence for this claim is obtained by a comparison of this group with the YS-NF-80 group, which experienced the same pattern and amount of shock during the yoked shock training. While these two groups showed virtually identical suppression to the CS + , they differed in responding to the compound, with Group YS-NF-80 showing as much suppression to the compound as to the CS + . This difference also indicates that the outcome of the inhibition test is not due to external inhibition or other nonassociative factors. In addition, the results indicate that conditioned inhibition to the feedback stimulus is acquired gradually over the 80 trials of training. This is suggested by the increasing divergence in reaction to the CS+ and the compound as a function of increasing the number of training trials. This pattern of results is in agreement with those of Weisman and Litner (1971). More importantly for purposes of the present experiments, the results of Experiment 1 and IB considered in combination strongly implicate Pavlovian conditioned inhibition in the effectiveness of a feedback stimulus’ ability to reduce fear to the shock context. The feedback stimulus reduced fear only in animals for whom it also functioned as a conditioned inhibitor on the summation test. This finding is consistent with the general results of experiments which have examined the relationship of Pavlovian conditioned inhibitors and feedback stimuli in avoidance situations (e.g., Morris, 1974, 1975; Weisman & Litner, 1971, 1972).

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The results of the fear test in Experiment 1 demonstrate that the effects of predictability and controllability are differentially affected by the number of training trials. While the effects of controllability can be mimicked, as Mineka et al. (1984) have suggested, by providing prediction of shock absence, our findings demonstrate that their effects on reduction of fear to the shock context develop at different rates. In the present experiment, we employed a different approach to address the same general issue of the independent action of predictability and controllability on contextual fear conditioning. A more powerful demonstration of the independence of these two factors would be provided by an experimental result which shows the effect of one of these factors in a situation in which the other has no demonstrable effect. A relatively long minimum IT1 is necessary for a CS to acquire inhibitory properties. Moscovitch and LoLordo (1968), using dogs, found that a CS did not acquire inhibitory properties if the next US could occur at any time during the 2.5min ITI. Similarly, Weisman and Litner (1971) failed to observe the development of conditioned inhibition when the minimum IT1 was 30 s, even when 100 trials of training were administered. This variable is also known to influence the ability of a feedback stimulus to modify ongoing avoidance behavior. Morris (1974) failed to observe conditioned inhibition to a feedback stimulus when a 30-s minimum ITI was used. We have recently demonstrated the importance of the minimum IT1 for the effect of a feedback stimulus on conditioning of fear to the context (Rosellini et al., 1986). A feedback stimulus reduced fear of the context only if a 60-s minimum IT1 was used. When a 5-s minimum ITI was used, animals receiving the feedback stimulus showed as much contextual fear as animals receiving no feedback stimulus. Thus, we chose to assess the effects of controllability of shock termination under the 5-s minimum ITI conditions which preclude, or at least greatly mimimize, an effect of predictability of shock absence. We expected this manipulation not to affect the influence of shock controllability on the escape behavior. This expectation was based on the fact that animals trained to escape shock with a 60-s minimum ITI, as in Experiment 1 and in Rosellini et al. (1986), show acquisition of the escape response which does not appear to differ from that of animals trained to escape shock with a 5-s minimum IT1 (e.g., Rosellini et al., 1982, 1986; Warren, Rosellini, Plonsky, & DeCola, 1985). However, it is not known whether such a manipulation will affect the level of fear conditioned to the shock context or whether controllability could interact with predictability of shock absence under these conditions. Thus, in the present study, we employed a 2 x 2 factorial design to assess the effects of controllability (escapable shock vs yoked shock) and predictability (feedback vs no

406 feedback) condition.

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upon fear of the shock context

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under a 5-s minimum

IT1

Method Subjects and apparatus. The subjects were 48 experimentally naive male Holtzman rats approximately 100 days of age at the start of the experiment. Housing conditions were the same as those of Experiment 1. The shock training apparatus described in Experiment 1 was used for all phases of the present study. Procedure. This study consisted of three phases-preexposure, shock training, and fear test. The preexposure and test phases were identical to those used in Experiment 1. Shock training. This consisted of a 2 x 2 factorial design yielding four groups of animals (Ns = 12). Two groups received 80 trials of bar-press shock escape training. One of these groups (ES-FB) experienced the feedback stimulus following shock termination, whereas the other did not (Group ES-NF). Each of the two other groups was yoked to one of the escape groups for both shock and feedback exposure. All experimental procedures and parameters were identical to those of Experiment 1 with one important exception. In the present study, a 5-s minimum IT1 was used for all groups instead of the 60-s minimum employed in Experiment 1. It should be noted that the average IT1 was 90-s in both of these studies. Results Shock escape training. Both groups trained to escape shock acquired the escape response as indicated by a decrease in response latency across blocks of five trials (F(12, 264) = 8.71, p < .OOl). Groups ES-FB and ES-NF did not differ in this respect as demonstrated by the lack of a significant effect of group or group x trial block interaction (Fs < 1.2, ps > .35). The mean amount of shock received per trial by these two groups and consequently the yoked groups (YS-FB and YS-NF) was 4.2 and 3.9 s, respectively. Fear test. As in Experiment 1, all data were subjected to a square root transformation. A three-way ANOVA was conducted with feedback (FB or NF), shock type (ES or YS), and days of test (4) as the factors. The mean total amount of time spent on the grid floor as a function of group and days of test is shown in Fig. 3. All groups tended to increase the amount of time spent on the grid floor across the 4 test days, yielding a significant effect of days (F(3, 132) = 35.66, p < .OOl). More importantly, the type of shock training administered had a powerful influence on the amount of time spent on the grids, but the feedback manipulation had no influence on this measure. This pattern of results yielded a significant effect of shock type (F(1, 44) = 14.00, p < .OOl) and a shock type x

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FIG. 3. Mean transformed time spent on the grids across 4 test days for the four groups (ES = escapable shock, YS = yoked shock, FB = feedback, NF = no feedback). A 5-s minimum ITI was used in this study.

days interaction (F(3, 132) = 3.03, p = .031). The feedback manipulation, as expected due to the use of a 5-s minimum IT1 (Rosellini et al., 1986), did not influence the amount of time spent on the grid as indicated by the lack of a significant effect of this variable or any interaction of feedback with either shock or days (Fs < 1.5, ps > .25). An orthogonal set of contrasts was conducted to determine the source of the interaction between shock type and days. This showed that Group ES-FB did not differ from Group ES-NF on any day of the test (Fs(1, 132) < 2.0, ps > SO); Group YS-FB did not differ from Group YS-NF on any test day (Fs(1, 132) < 1.O, ps > .50); and the two ES groups did differ significantly from the two YS groups on Days 2, 3, and 4 @(I, 132) > 10, ps < .Ol), indicating that the ES groups showed more rapid extinction of fear than the YS groups. Discussion

The outcome of this experiment demonstrates that when a 5-s minimum IT1 is used, the feedback stimulus does not reduce fear of the shock context, as indicated by the equivalence of the groups given feedback to those not receiving feedback. This fact, when considered in combination with the effect of feedback when a longer minimum IT1 is used (i.e., 60 s in Experiment l), essentially replicates our earlier work (Rosellini et al., 1986). This observation is also consistent with other experiments demonstrating the importance of the IT1 length for the effective development

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of both a feedback effect (Morris, 1975) and Pavlovian conditioned inhibition (Moscovitch & LoLordo, 1968; Weisman & Litner, 1971). Thus, in order for a feedback stimulus to acquire the ability to reduce fear to the shock context it must predict a relatively long period of shock absence. While feedback is not effective under the present parameters, it is equally clear that control over shock termination is effective in influencing the amount of contextual fear even with the short minimum ITI. Groups ES-FB and ES-NF were less fearful of the context than Groups YS-FB and YS-NF. This observation extends the generality of the result reported by Mineka et al. (1984). Rosellini et al. (1986), and those of Experiment 1 of the present series, in demonstrating the effectiveness of controllability in reducing fear to the context even when a short minimum ITI is used, in contrast to the longer minimum IT1 employed by the earlier studies. EXPERIMENT

3

The results of Experiments 1 and 2 are clear in showing two conditions where the effects of controllability are not mimicked by the presentation of a feedback stimulus. However, it is possible that the feedback stimuli manipulated in these experiments do not capture some important aspect of the stimulation produced by the response. While we cannot empirically overcome the fundamental difference between the internal nature of response-produced stimulation and external stimuli, we can address empirically the possibility that the two types of stimuli may differ along some dimension which is known to be important for conditioning to external stimuli. One such dimension is the relative saliency of the two types of stimuli. If one assumes that response-produced stimulation is a more salient event than the external feedback stimulus, and that this parameter controls the rate of learning (Mackintosh, 1975; Rescorla & Wagner, 1972; Wagner, 1981), then the apparent effects of controllability observed in the above experiments may still be mediated by predictability. The fact that animals having control show reduced fear at an earlier point in training than animals given feedback could then be due to the postulated difference in saliency, since the more salient event would be expected to reach asymptotic conditioning at an earlier point in training (e.g., Rescorla & Wagner, 1972). The results of Experiment 2 could, using this line of reasoning, be due to an interaction between saliency and minimum ITI. Although this type of account is post hoc, it does gain credibility by the observation, reported by Mineka et al. (1984), that the effects of controllability do not summate with the effect of a feedback stimulus in providing any additional decrease in fear over that observed in animals having only control or having only feedback. This fact could be explained by proposing that the higher saliency of the response-produced stimulation

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results in overshadowing of the external feedback stimulus, thus preventing it from acquiring any appreciable inhibitory strength. The purpose of Experiment 3 was to assess empirically this possibility by using a design similar to that of Experiment 2 but with a 60-s minimum ITI. This should result in an effective feedback stimulus (Rosellini et al., 1986). We employed a 2 x 2 factorial design with controllability as one factor (ES vs YS) and feedback as the other (FB vs NF). Following this shock training, the four groups were given a context fear test, followed by a test for the inhibitory power of the feedback stimulus. If the above line of reasoning is correct concerning the differential saliency of the stimuli, then one would expect to observe the following pattern of results. First, no summation of controllability and feedback should be observed on the fear test, which would be indicated by the equivalence of the ESFB and ES-NF conditions. This would replicate the findings of Mineka et al. (1984, Experiment 4). Second, the test for inhibition should reveal overshadowing of the feedback stimulus by the response-produced stimulation in animals which have control over shock termination. This would be indicated by the feedback stimulus showing stronger conditioned inhibitory properties in the YS-FB than in the ES-FB condition. Indeed, one would expect that while the feedback stimulus might acquire some initial associative strength, it would lose it with additional training as suggested by the demonstration of loss of associative strength by a less salient stimulus reported by Hall, Mackintosh, Goodall, and Martello (1977). Method Subjects and apparatus. The subjects were 43 experimentally naive male Holtzman rats approximately 100 days of age at the start of the experiment. Housing conditions were the same as those in Experiment 1. The apparatus described in Experiment 1 was used for all phases of this study. Procedure. This study consisted of four phases (a) preexposure, (b) shock training, (c) fear test, and (d) conditioned inhibition test. The preexposure and test phases were identical to those used in Experiments 1 and 2. Thus, only those phases which differed are described. Shock training. Shock training procedures were identical to those of Experiment 2 with the exception that a different shock schedule was used. As in Experiment 2, this study consisted of a 2 x 2 factorial design yielding four groups of animals. Two groups received 80 trials of barpress shock escape training. One of these groups (ES-FB; N = 11) experienced the feedback stimulus following shock termination, whereas the other did not (Group ES-NF; iV = 11). Each of the two remaining groups was yoked to one of the escape groups for both shock and feedback exposure (i.e., Group YS-FB, N = 10; and Group YS-NF, N = 11). In the present

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study as in Experiment 1, a 60-s minimum IT1 was used for all groups instead of the 5-s minimum employed in Experiment 2. The average IT1 was 90 s as in both of the above experiments. Conditioned inhibition test. As did the inhibition test in Experiment lB, this test consisted of three phases-appetitive baseline training, Pavlovian excitatory fear conditioning, and a test for conditioned inhibition. All animals received two sessions of appetitive baseline training followed by three sessions of fear conditioning to the CS -t for a total of 12 trials. All training parameters for each of these phases were identical to those of Experiment IB. The inhibition test was also similar to that of Experiment 1B with two exceptions. In this study, in order not only to assess existing levels of inhibition to the feedback stimulus but also to examine its further development, we conducted 6 days of inhibition testing during which the CS + continued to be reinforced while the compound (tone + feedback) was never reinforced, (i.e., an A+/ABdesign). Results Shock Training. All animals in the two escape training groups acquired the escape response as indicated by decreasing latencies to escape across the 5-trial blocks of training (F(12, 240) = 3.80, p < .OOl). During this phase, the animals in Group ES-NF, and therefore their yoked partners (Group YS-NF), received an average of 5.4 s of shock per trial while Group ES-FB, and its yoked partners (Group YS-FB), received 4.3 s of shock per trial. While the two escape groups did not differ in the overall amount of shock received as indicated by a lack of a main effect of group (F( 1, 20) = 1.73, p > .15), the pattern of shock received by these two groups and consequently the two yoked groups differed as a function of trials as indicated by a significant group x trial block interaction (F(12, 240) = 3.19, p < .OOl). This interaction stems from the fact that while the two groups showed equivalent escape latencies during the first block of 5 trials (means = 7.2 and 8.0 for Groups ES-NF and ES-FB, respectively, Group ES-FB showed a more rapid decline in escape latencies than did Group ES-NF, so that on the last trial block Group ES-FB had shorter escape latencies than did Group ES-NF (means = 1.9 and 3.8 s respectively). Fear test. As in the above experiments, the total grid time measure was submitted to a square root transformation. As expected on the basis of the results of the 80-trial condition of Experiment 1 and the results of Mineka et al. (1984) and Rosellini et al. (1986), animals exposed to yoked shock without a feedback stimulus (Group YS-NF) showed the most fear of the shock situation, while the other three groups were virtually indistinguishable from each other. An ANOVA conducted on these data as a function of shock type (ES vs YS), feedback (FB vs NF). and days (l-4) showed a significant effect of days (F(3, 117) =

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of

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FIG. 4. Mean transformed time spent on the grids across 4 test days for the four groups (ES = escapable shock, YS = yoked shock, FB = feedback, NF = no feedback). A 60-s minimum ITI was used in this study.

37.16, p < .OOl) and a marginally significant three-way interaction (F(3, 117) = 1.74, p = .087). The source of this interaction was examined by orthogonal contrasts. As Fig. 4 shows, Groups ES-FB and ES-NF show the same pattern of increasing amounts of time spent on the grid floor across the 4 test days (F(3, 117) < l.O), indicating that the presence of the feedback stimulus during training did not reduce fear any more than simply having control over shock termination. This is the case even though Group ESFB showed more rapid acquisition of the escape response than did Group ES-NF. While this difference observed during escape training might be expected to bias the fear test in a direction suggesting summation of controllability and predictability in Group ES-FB, this was not the case. Group YS-FB was statistically indistinguishable from these two escape groups (F(3, 117) < l.O), indicating that the feedback stimulus, as in prior experiments, was successful in reducing fear of the context. These three groups did significantly differ from Group YS-NF (F(3, 117) = 14.59, p < .OOl). It should be noted that this comparison with the YSNF group must be considered with caution due to the differential pattern of shock received by the feedback relative to the no feedback groups. In this case, the difference may have contributed to Group YS-NF showing more fear than the other groups. However, if we compare the performance of Group ES-NF to that of Group YS-NF, which did receive the same pattern of shock, a significant difference is still observed (F(3, 117) =

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FIG. 5. Mean suppression ratios to the CS+ and the compound on the 6 days of the conditioned inhibition test (ES = escapable shock, YS = yoked shock, FB = feedback, NF = no feedback).

10.13, p < .OOl). This observation is consistent with the results of the fear test of Experiment 1 and the results reported by Mineka et al. (1984) and Rosellini et al. (1986). Conditioned inhibition test. As in Experiment lB, the four groups did not differ in body weight at the beginning of this phase of the study (all Fs < 1.O, all ps > SO). The groups were also equivalent in total number of food cup inspections during the two appetitive baseline sessions (all Fs < 1.4, all ps > .5). There was a general increase in responding across these two days of baseline training (F(1) 39) = 24.35, p < .OOl). Acquisition of fear to the CS + proceeded in a gradual manner with increasing levels of suppression across the 3 conditioning days (mean suppression ratios for Days 1, 2, and 3 = 0.35, 0.27, and 0.23) resulting in a significant effect of days (F(2, 78) = 10.02, p < .OOl). No differences in acquisition to the CS + were observed as a function of either type of shock (ES vs YS), feedback (NF vs FB), or any interactions between them (Fs < 1.4, ps > 30).

The results of the conditioned inhibition test are presented in Fig. 5. As can be seen, the two groups which had not been exposed to the feedback stimulus during the shock training (Groups ES-NF and YSNF) showed equivalent levels of suppression to the CS + and the compound

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stimulus on the first day of the test, and divergent suppression across the additional days. Groups ES-FB and YS-FB showed differential suppression to the CS+ and the compound on the first day of the test with relatively small divergence on subsequent days. These data were analyzed by a shock type (ES vs YS), feedback (FB vs NF), CS type (CS + vs compound), and days (l-6) ANOVA. It revealed a significant shock x feedback x CS interaction (F(l) 39) = 4.56, p = .039), and a marginally significant four-way interaction including days (F(5, 195) = 1.97, p = .084). In order to assess the existence and/or development of conditioned inhibition, simple effects analyses were conducted for each of the four groups at each day as a function of CS type to determine at which points suppression to the compound differed from that to the CS + . Group ESNF (top left-hand panel of Fig. 5) showed equivalent suppression to the two stimuli on Day 1 (p > .20), significantly less suppression to the compound than the CS + on Day 2 0, < .02), and continued divergence on the remaining days (ps < .OOl). Group YS-NF (top right-hand panel of Fig. 5) showed equivalent suppression to the CS + and the compound on the first 3 days of the test (ps > .20) and less suppression to the compound than the CS + on the final 3 days (ps < .Ol). This demonstrates the acquisition of inhibition to the CS- in the two original learning control groups. Groups ES-FB and YS-FB (bottom two panels of Fig. 5) showed significantly less suppression to the compound than to the CS + on the first day of the test 0, < .Ol) demonstrating that the stimulus had acquired inhibitory properties during shock training. They also showed a slight increase in differentiation between the CSs .on the remaining 5 days (ps < JOI). Since the major purpose of the conditioned inhibition test was to assess the occurrence of overshadowing, we conducted three additional sets of orthogonal contrasts as a function of CS type and days. The first and most important set showed Groups ES-FB and YS-FB were statistically indistinguishable in suppression to the CS+ and compound on each of the 6 test days (ps > .lO). This demonstrates equivalent inhibition to the feedback stimulus in the two groups and therefore a lack of overshadowing. The second set of contrasts comparing the suppression to the CS + and the compound for Groups ES-NF and YS-NF on each of the days showed these two groups to differ significantly on the third test day (p < .Ol) and to be equivalent on all other days (all ps > .15). Finally a comparison of the groups which had received feedback (ESFB and YS-FB) to those not exposed to feedback (ES-NF and YS-NF) showed the first two groups differed from the latter two on the first test day as a function of CS type (p < .03), indicating that the FB groups showed significantly more differential suppression to the two CS types than the NF groups. Thus, this between-group contrast reinforces the

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suggestion of the above within-group comparisons and indicates that the FB stimulus had acquired inhibitory properties during the original training in the ES groups. Discussion The results of the fear test replicate our work in two respects. As in Experiment 1 of the present series and of Rosellini et al. (1986), animals exposed to yoked shock with a feedback stimulus show no more fear of the shock context than do animals exposed to escapable shock, while animals receiving yoked shock without a feedback stimulus show more fear than either of these two groups. Furthermore, the fact that Group ES-FB animals do not show any less fear than Group ES-NF or YS-FB replicates Mineka et al. (1984, Experiment 4). This equivalence of fear indicates that the exteroceptive feedback stimulus and control of shock termination do not summate on this type of test. In spite of this lack of summation on the fear test, the feedback stimulus was effective in two respects in animals which had control over shock termination. First, the feedback stimulus facilitated the acquisition of the escape response as demonstrated by the more rapid decrease in escape latencies in Group ES-FB than in Group ES-NF. To our knowledge, this is the first demonstration of such an effect of feedback on the acquisition of an escape response. It is, however, reminiscent of the report by Bolles and Grossen (1969) that a feedback stimulus facilitated the acquisition of an avoidance response. It is also consistent with previous observations from our laboratory (e.g., Warren et al., 1985) and the facilitation of escape learning by stimuli interposed between the response and shock offset reported by Tarpy and Koster (1970). Second, and more importantly, the feedback stimulus did acquire significant inhibitory properties even when shock termination was controllable, indicating that it was not overshadowed by the response-produced stimulation. Groups ES-FB and YSFB were indistinguishable in the amount of inhibition observed to the feedback stimulus. This demonstration undermines the hypothesis that lack of summation on the fear test is due to the overshadowing of the external feedback stimulus by the response produced stimulation. Furthermore, since it shows no empirical evidence of overshadowing under these conditions, at present it would seem most reasonable to conclude that the effects of controllability observed in the above experiments are due to processes separable from prediction of shock absence. It should be noted that a temporal difference may exist between responseproduced stimulation and the external, experimenter-provided feedback stimulus. That is, the response-produced stimulation antedates the termination of shock, whereas the onset of the external feedback stimulus is coincident with shock termination. Given this temporal difference, it might be proposed that, in some unspecified manner, it makes the response-

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produced feedback a better stimulus for acquiring conditioned inhibition than the external feedback stimulus. Although the present experiments cannot empirically discount this argument, it receives little support from reports in the literature. Mowrer and Aiken (1954) found that a CS which overlapped the final portion of a shock US suppressed appetitive responding, suggesting that it acquired fear excitatory properties. Moscovitch and LoLordo (1968), in their comparison of the effect of backward temporal conditioning relative to the cessation procedure in which the CS onset shortly precedes US termination, have found that a backward conditioning stimulus accrues more inhibitory strength than does the cessation CS. Indeed, the presentation of the cessation CS did not significantly decrease ongoing avoidance behavior. These results suggest that the potential temporal difference between response-produced and externally provided stimulation is not a viable account of the outcome of the present experiments. If anything, the Mowrer and Aiken (1954) results suggest that the difference should be in favor of the response-produced stimulation acquiring fear excitatory, not fear inhibitory, properties. Furthermore, it should be noted that this type of proposal would have dimculty accounting for the fact that response-produced stimulation did not overshadow the external feedback stimulus. If it is assumed to be a more salient, or otherwise a more conditionable stimulus, then overshadowing should have been evident. This would be expected on the basis of (1) current theories of conditioning (cf. Rescorla & Wagner, 1972; Wagner, 1981), (2) the demonstrated loss of associative strength by less salient stimuli (Hall et al., 1977), and (3) the demonstrated competition between stimuli in conditioned inhibition paradigms (Suiter & LoLordo, 1971). GENERAL

DISCUSSION

In agreement with earlier work from our and others’ laboratory, the present experiments demonstrate that animals which have control over shock termination are less fearful of the shock context than animals which do not have control (Desiderato & Newman, 1971; Mineka et al., 1984; Osborne et al., 1975; Rosellini et al., 1986). Furthermore, Experiments 1 and 3 show that this reduction in contextual fear can also be observed in animals which do not have control but which are provided with an external feedback stimulus (see also Mineka et al., 1984; Rosellini et al., 1986). These two observations, taken in isolation, offer the possibility that the effects of control upon contextual fear can be attributed to the predictive value of response-produced stimulation, as suggested by Mineka et al. (1984). While replicating the observations which have led to this theorizing, the results of the present studies show that the effects of control over shock termination are not isomorphic to those of feedback stimuli. Experiment 1 demonstrated that controllability of shock reduces fear of the context at a level of training insufficient for the observation

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of an effect of external feedback. Experiment 2 showed that it produces lower levels of contextual fear under conditions where the effect is not mimicked by presentation of the external feedback stimulus. Furthermore, Experiment 3 showed that while control and feedback presentation do not summate to reduce fear of the context, the feedback stimulus does gain associative power in animals which have control over shock. It is, therefore, unlikely that the notion of differential saliency of responseproduced versus exteroceptive stimuli can account for the observed dissociation between control over shock termination and the effect of external feedback stimuli. The results of these studies bring into question the proposal that the effects of controllability are reducible to the predictive nature of responseproduced stimulation. To the extent that the equivalence of action of control and feedback stimuli can be taken as evidence for a common mechanism, the observed empirical dissociation suggests that control and prediction exert their influence on contextual fear by distinct mechanisms. This suggestion of a dissociation of mechanism is consistent with and receives additional support from current data from several laboratories. Maier and Warren (in press) have reported that while exposure to controllable shock does immunize against the detrimental effects of subsequent exposure to uncontrollable shock, presentation of a feedback stimulus during uncontrollable shock does not immunize the animal. Furthermore, they report a double dissociation between the effects of control and those of feedback on shock induced analgesia. Animals exposed to controllable shock are analgesic immediately following the shock session but are not analgesic following a subsequent session of uncontrollable shock. In contrast, presentation of a feedback stimulus blocks the analgesic response immediately following the shock but not that observed following a subsequent uncontrollable shock session. A dissociation of effects is also evident in a recent study from our laboratory (DeCola, Warren, & Rosellini, 1987). We have found that while a feedback stimulus can block conditioning of fear to the context and the FR-2 shuttle escape deficit produced by uncontrollable shock exposure, it does not block the effect observed on a noncontingent appetitive test. A dissociation of controllability and predictability is also implied by a comparison of the reported decrease in adrenocortical system output as a result of restraint following exposure to controllable shock (Murison & Isaksen, 1982) and an increase in output following exposure to uncontrollable shock with a feedback stimulus (Overmier, Murison, Skoglund. & Ursin, 1985). The outcome of the present experiments is also important in that they may allow us to differentiate between the different theoretical proposals which have been advanced to account for the effects of feedback stimuli on contextual fear. Generally, our findings are consistent with the proposals which stress the associative or predictive functions of the feedback stimulus,

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since these positions anticipate that (a) the number of trials of training should be an important determinant of the effectiveness of the feedback stimulus on contextual fear as seen in Experiment 1 and 3, (b) the feedback stimulus should acquire conditioned inhibitory properties and should be influenced by amount of training, as demonstrated in Experiments 1B and 3, and (c) the minimum IT1 should have important consequences for the observance of a feedback effect as seen in Experiment 2. This suggests that there is a concordance in the conditions under which the feedback stimulus has an effect on contextual fear and those under which it acquires conditioned inhibitory properties. Thus, they strongly implicate conditioned inhibition in the effects of feedback on contextual fear. This pattern of findings is in particular agreement with the Mineka et al. (1984, p. 32 1) proposal that the feedback stimulus becomes a strong conditioned inhibitor, thereby reducing the total amount of fear conditioned to the context. It should be noted that, while the present findings strongly implicate conditioned inhibition in the effect of feedback stimuli on contextual fear, they leave open the possibility that other effects of feedback stimuli may be independent of conditioned inhibition. For example, Maier & Keith (1987) have found that not only feedback stimuli but also random stimuli are capable of blocking the analgesia typically produced by exposure to uncontrollable shock. Finally, when considered in combination with other demonstrations of the importance of the minimum IT1 for the observance of feedback effects and the development of inhibition (Morris, 1974, 1975; Rosellini, et al., 1986; Weisman & Litner, 1971), the results of the present experiments appear inconsistent with nonassociative interference accounts. As suggested by Mineka e? al. (1984), the effects of feedback may result from their function as distractor stimuli (Wagner, 1981), which disrupt ongoing rehearsal and hence reduce the amount of fear conditioning of contextual cues on the prior trial. If this were the case, however, one would not expect manipulation of the IT1 to modify this distractor effect. Similarly, one would not expect the minimum IT1 to have such a powerful influence on the effect of feedback, if it exerts its influence by disrupting the ongoing UR (e.g., Starr & Mineka, 1977). However, the present findings would be consistent with an interference or distractor hypothesis, which assumes that interference produced by a stimulus is a function of its associative strength. REFERENCES Anisman, H., decatanzaro, D., & Remington, G. (1978). Escape performance deficits following exposure to inescapable shock: Deficits in motor response maintenance. Journal of Experimental Psychology: Animal Behavior Processes, 4, 197-218. Annau, Z., & Kamin, L. J. (1961). The conditioned emotional response as a function of the intensity of the US. Journal of Comparative and Physiological Psychology, 54, 428-432.

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Belles, R. C. (1970). Species-specific defense reactions. Psychological Review, 77, 32-48. Belles, R. C., & Grossen, N. E. (1969). Effects of an informational stimulus on the acquisition of avoidance behavior in rats. Journal of Comparative and Physiological Psychology,

68, 90-99.

Channell, S., & Hall, G. (1983). Contextual effects in latent inhibition with an appetitive conditioning procedure. Animal Learning and Behavior, 11, 67-74. Church, R. (1964). Systematic effect of random error in the yoked control design. Psychological Bulletin,

62, 122-131.

DeCoIa, J. P., Warren, D. A., & Rosellini, R. A. (1987). Controllability and predictability equivalent and differential effects as a function of test type. Paper presented at the meeting of EPA, Arlington, VA. Desiderato, O., & Newman, A. (1971). Conditioned suppression produced in rats by tones paired with escapable or inescapable shock. Journal of Comparative and Physiological Psychology,

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Hall, G., Mackintosh, N. J., Goodall. G.. & Martello, M. (1977). Loss of control by a less valid or by a less salient stimulus compounded with a better predictor of reinforcement. Learning and Motivation, 8, 145-158. Jackson, R. L., Alexander, J. H., & Maier, S. F. (1980). Learned helplessness. inactivity, and associative deficits: Effects of inescapable shock on response choice escape learning. Journal of Experimental Psychology: Animal Behavior Processes, 6, I-20. Jackson, R. L., Maier, S. F., & Coon, D. J. (1979). Long-term analgesic effects of inescapable shock and learned helplessness. Science, 206, 91-93. Laudenslager, M. L., Ryan, S. M., Drugan, R. C.. Hyson, R. L., & Maier. S. F. (1983). Coping and immunosuppression: Inescapable but not escapable shock suppresses lymphocyte proliferation. Science, 221, 568-570. Levis, D. J. (1976). Learned helplessness: A reply and alternative S-R interpretation. Journal

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