Intertrial interval as a contextual stimulus

Behavioural Processes 71 (2006) 307–317

Intertrial interval as a contextual stimulus Mark E. Bouton ∗ , Ana Garc´ıa-Guti´errez University of Vermont, United States Received 5 December 2005; accepted 5 December 2005

Abstract Four experiments with rats investigated whether the time between appetitive conditioning trials can serve as a discriminative cue for responding during the next conditional stimulus (CS). In Experiment 1, rats that received extinction trials with a 4-min intertrial interval (ITI) showed spontaneous recovery after a retention interval of 16 min, whereas rats that received extinction with a 16-min ITI did not. Experiments 2 and 3 investigated more explicit discriminations between the 4- and 16-min ITIs. When a 16-min ITI signaled that the CS would be reinforced and a 4-min ITI signaled that it would not, the ITIs modulated responding to the CS. But when the 4-min ITI signaled reinforcement and the 16-min ITI did not, there was less evidence of modulation by the ITIs. This asymmetry was due at least partly to a difficulty in performance rather than learning. Experiment 4 investigated similar discriminations with 1- and 4-min ITIs. Here the results took a different form: time in the reinforced ITI elicited responding directly, but did not modulate responding to the CS. ITI can function as a contextual cue, and the results suggest new similarities between the processes behind interval timing and associative learning. © 2005 Elsevier B.V. All rights reserved. Keywords: Intertrial interval; Conditional stimulus; Temporal discrimination

The fact that temporal variables have important effects on Pavlovian learning suggests that timing processes might be intimately involved in conditioning (e.g. see Gallistel and Gibbon, 2000, for one review). Recent research from several laboratories has confirmed the role of temporal factors in the magazine-entry conditioning procedure, in which a conditional stimulus (CS) is paired with delivery of a food pellet unconditional stimulus (US) and the rat learns to enter the foodcup during the CS. Over trials, conditioned responding in this method quickly anticipates the temporal point at which the US will be delivered (e.g. Holland, 2000; Kirkpatrick and Church, 2000). In delay conditioning, where the US is presented at the end of each CS presentation, the duration of the CS also matters; less overall conditioned responding develops with longer-duration CSs (e.g. Bouton and Sunsay, 2003; Holland, 2000; Lattal, 1999). This effect is scaled to the duration of the intertrial interval (ITI), the amount of time between successive trials, over some CS and ITI durations (e.g. Holland, 2000). That is, equivalent responding sometimes develops with equal ITI:CS duration ratios (Gallistel ∗ Corresponding author at: Department of Psychology, University of Vermont, Burlington, VT 05405, United States. Tel.: +1 802 656 4164; fax: +1 802 656 8783. E-mail address: [email protected] (M.E. Bouton).

0376-6357/$ – see front matter © 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.beproc.2005.12.003

and Gibbon, 2000). However, both CS duration and ITI duration have separable effects on conditioning (e.g. Holland, 2000; Kirkpatrick and Church, 2000; Lattal, 1999). Long ITIs support better conditioned responding than short ITIs (e.g. Bouton and Sunsay, 2003; Holland, 2000; Lattal, 1999; Sunsay et al., 2004). A related temporal variable that can influence conditioned responding is the retention interval, the time between exposure to some conditioning treatment and a subsequent test of the CS. We have recently emphasized the idea that retention intervals can affect responding by introducing context change (e.g. Bouton, 1993; Bouton et al., 1999). That is, as time within a retention interval passes, hypothetical stimuli in the background also change. Retention intervals may therefore cause forgetting because a change of context reduces memory retrieval (e.g. Spear, 1978; Smith and Vela, 2001). Interestingly, retention intervals of several days often have a stronger effect on the retention of extinction (the loss of responding that results from CS-alone presentations after conditioning) than on the retention of conditioning (see Bouton, 1993, for a review). This difference is the basis of spontaneous recovery, the phenomenon in which an extinguished response can recover if a retention interval is inserted after extinction. Related research indicates that extinction depends more on the

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context than does conditioning (e.g. Bouton, 1993); when the physical context is changed after extinction, extinction is not retrieved, and extinguished responding can be “renewed”. Thus, a retention interval inserted after extinction may cause a failure to retrieve extinction—and spontaneous recovery results (e.g. Brooks and Bouton, 1993). On this view, spontaneous recovery is the “renewal effect” that occurs when an extinguished CS is tested in a new temporal context (e.g. Bouton, 1993). Of course, intertrial intervals are also brief retention intervals, and conditioning that occurs over a series of conditioning trials must thus occur within a changing context of time. We have therefore turned our attention to the effects of intertrial interval on conditioning and extinction (Bouton and Sunsay, 2003; Moody et al., in press; Sunsay et al., 2004). One goal of that research has been to understand why long ITIs can create better conditioning than short ITIs. The present experiments are concerned with a somewhat different question, namely, can animals use an ITI of a given duration as a stimulus over which they generalize and discriminate? There is a small literature suggesting that animals do generalize (or fail to generalize) on the basis of ITI. For example, Ernhart (1960) showed that when appetitive runway training in rats was conducted with intertrial intervals of 10 or 120 s, a switch to the opposite interval caused a decrement in the level of responding. Such findings suggest that, in addition to influencing the strength or extent of conditioning, a record of the ITI might be encoded as part of the “context” in which conditioning and/or extinction occur (see also Capaldi and Morris, 1976). In the present Experiment 1, we therefore asked whether ITI is encoded as part of the context of extinction. If it is, then tests of responding after an interval that differs from the ITI used in extinction may yield spontaneous recovery of conditioned responding. Conversely, if extinction is carried out with an ITI that matches the retention interval, spontaneous recovery might not occur. The extensive literature on interval timing in animals (e.g. Church and Broadbent, 1990; Gibbon et al., 1984; Killen and Fetterman, 1988; Staddon and Higa, 1999) further indicates that time can be used as a discriminative stimulus. For example, in the well-known peak procedure (e.g. Roberts, 1981), animals readily learn to respond at the point in time when reinforcers are imminent as a consequence of exposure to reinforced reference trials and longer nonreinforced blank trials. In the temporal bisection procedure (e.g. Church and Deluty, 1977), animals learn to emit one response when it is reinforced after a signal of a given duration and a second response if it is reinforced after a signal of another duration. Although there is thus ample research indicating that a temporal interval can set the occasion for a response, we are not aware of any research that asks whether ITI can signal whether or not the next Pavlovian CS will be reinforced. Experiments 2–4 therefore began to investigate classical conditioning when animals are given a reason to discriminate between the intervals between trials. The experiments used intertrial intervals that we have used before in research on ITI effects in the magazine-entry conditioning preparation (e.g. Moody et al., in press; Sunsay et al., 2004).

1. Experiment 1 As noted above, Bouton (1993, 2002, 2004) has argued that extinction performance is highly specific to the context in which it is learned, and that the “context” can involve many different types of stimuli, such as physical background cues, interoceptive state, and time. The first experiment was designed to extend this approach by asking whether the interval between extinction trials might also be coded as part of the extinction context. Two groups originally received conditioning with a mixture of ITIs averaging 4 and 16 min. One group then received a series of extinction trials with an ITI of 4 min. Once responding had declined, they were tested again after a retention interval of 16 min. If ITI can serve as part of the context of extinction, we might expect the response to recover when the interval between trials is changed. A control group received the same 16-min retention interval, but had received its extinction trials spaced by the same (16 min) interval. This group received no comparable change between the ITI and the retention interval, and if ITI is part of the context in which extinction is learned, then this group should show continued extinction performance after the retention interval, and no recovery. Recent research in our laboratory (Moody et al., in press) has shown that spontaneous recovery does occur when extinction with either 4- or 16-min ITIs is followed by a much longer 72-h interval. 1.1. Method 1.1.1. Subjects The subjects were 16 female Wistar rats purchased from Charles River Laboratories (St. Constance, Que.). 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 room on a 12:12 light:dark cycle. The rats were fooddeprived to 80% of their initial body weights throughout the experiment. 1.1.2. Apparatus The apparatus consisted of two sets of four conditioning chambers, each housed in a separate sound attenuation chamber. The two sets of boxes were housed in different rooms of the laboratory and have often been used as different contexts, although they were not used in that capacity here. Boxes in both sets measured 31.75 cm × 24.13 cm × 29.21 cm (l × w × h). The side walls and ceiling were made of clear acrylic plastic, while the front and rear walls were made of brushed aluminum. Recessed 5.08 cm × 5.08 cm food cups were centered in the front wall at about the level of the floor. For one set of boxes, the floor was composed of stainless steel grids (0.48 cm in diameter) spaced 3.18 cm center-to-center. One side wall had black horizontal stripes, 3.81 cm wide and 3.81 cm apart. The ceiling had similarly spaced stripes oriented in the same direction. For the other set of boxes, the floor was made of alternating stainless steel grids of different diameters (0.48 and 1.27 cm) separated by 1.59 cm center-to-center. One side wall and the ceiling were covered with rows of dark dots (1.9-cm diameter) with the adjacent dots separated by about 1.27 cm.

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The chambers were illuminated by two 7.5-W incandescent bulbs mounted to the ceiling of the sound attenuation chamber. The CS was a 10-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 US was provided by two 45 mg food pellets (Traditional formula, Research Diets, New Brunswick, NJ) delivered at the end of the CS. The apparatus was controlled by computer equipment located in an adjacent room. 1.1.3. Procedure 1.1.3.1. Magazine training. All rats were first assigned to a box and trained to retrieve food pellets from the food cup. Each rat received approximately 30 food pellets evenly distributed during a 20-min session. 1.1.3.2. Conditioning. On each of the next 6 days, the rats received 85-min conditioning sessions. In each session, the 10-s CS was paired with the US on eight trials. Trials were separated by either 16- or 4-min intervals, with each interval varying ±25%. The two intervals were double-alternated such that odd-numbered days employed an SSLLSSLL sequence and even-numbered days employed an LLSSLLSS sequence, where L and S denote long and short intervals. By the end of the phase, the rats had received 48 conditioning trials, half separated by 16-min and half separated by 4-min ITIs. The rats were then assigned to two groups (n = 8) matched on performance during the phase. 1.1.3.3. Extinction and spontaneous recovery test. On the following day, all rats received a single session containing eight extinction trials and four test trials. The first trial began 8 min into the session. One group then received the remaining extinction trials (tone without food) separated by an average of 16 min (±25%), and the other group received the same trials separated by an average of 4 min (±25%). After the 8th trial, both groups received a 16-min “retention interval” before four more tone-alone trials were presented. Each of these final test trials was separated by an ITI of 8 min (±25%), the geometric mean of the intervals used in extinction, which should generalize equivalently to them (cf. Church and Deluty, 1977). 1.1.3.4. Data analyses. The computer counted magazine entries during each 10-s CS and during the 10-s period that preceded the CS (the “pre-CS period”). The primary measure of conditioned responding was elevation scores of the form e = c − p, where c represents the number of responses recorded during the CS and p the number of responses in the corresponding pre-CS period. Elevation scores have been used extensively in this preparation (e.g. Bouton and Sunsay, 2003; Brooks and Bouton, 1993; Sunsay et al., 2004) because they separate CS responding from baseline responding. Elevation scores and pre-CS responses were analyzed with parallel analyses of variance (ANOVAs), using a rejection criterion of p < 0.05.

Fig. 1. Mean elevation scores (top) and pre-CS responding (bottom) during each trial of extinction (left) and spontaneous recovery testing (right) in Experiment 1. Group 4−16 received a 4-min extinction ITI and a 16-min retention interval before the test. Group 16−16 received a 16-min extinction ITI and a 16-min retention interval.

1.2. Results Conditioning in the two groups occurred without incident. The mean elevation scores on the first and final sessions of conditioning were 0.13 and 6.54, respectively. A Group × ITI × Session ANOVA uncovered only a Session main effect, F(5, 140) = 60.67; all other F’s < 1. The top panel of Fig. 1 shows the results of primary interest, the elevation scores during each trial of extinction (left) and spontaneous recovery testing (right). (The bottom panel shows pre-CS scores.) The groups showed a similar decline in responding during extinction. However, although the 16-min retention interval caused an increase in responding (spontaneous recovery) in the group that had received its extinction trials spaced by 4 min, it caused no increase in responding in the group that had received extinction trials spaced by 16 min. These impressions were confirmed by statistical analysis. A Group × Trial ANOVA on the eight extinction trials revealed a reliable main effect of Trial, F(7, 98) = 8.91, but neither the Group effect, F(1, 14) < 1, nor the Group × Trial interaction, F(7, 98) = 1.76, approached reliability. An identical ANOVA on the pre-CS scores revealed no main effects or interaction, F’s < 1. To analyze spontaneous recovery occurring over the 16-min retention interval, the mean of the last two extinction trials were compared with the mean of the first two test trials with a Group × Block ANOVA. [The groups did not differ on the

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last two-trial block of extinction, F(1, 14) = 2.39.] The analysis found neither a Group effect, F(1, 14) < 1, nor a Block effect, F(1, 14) = 1.89. However, the Group × Block interaction was reliable, F(1, 14) = 5.65. The interaction took the form of a significant increase in elevation score for the 4-min group, F(1, 14) = 7.13, but no change in the 16-min group, F(1, 14) < 1. Thus, the 4-min ITI in extinction allowed a recovery effect that was not evident in the 16-min group. An identical analysis of the pre-CS scores revealed no main effects or interaction, F’s ≤ 1.63. The mean pre-CS responding for the 4- and 16-min groups were 0.18 and 0.21, respectively. 1.3. Discussion As in our previous experiments using similar methods (Moody et al., in press), groups extinguished with 4- and 16-min ITIs did not differ in the rate at which conditioned responding was lost over extinction. However, for the group that received extinction with 4-min ITIs, a 16-min retention interval allowed a modest but significant recovery of conditioned responding. However, no such recovery was observed in a group for which the retention interval was the same as the ITI used in extinction (16 min). It is worth noting that the 16-min ITI in extinction does not produce a permanent extinction effect; previous experiments with an even larger number of trials have indicated that extinction with 16-min ITIs still allows spontaneous recovery after a 3-day retention interval (Moody et al., in press). The current results are thus consistent with the hypothesis that the time since the last trial can play the role of a contextual stimulus in extinction. That is, spontaneous recovery appeared to occur when the retention interval was different from the intertrial interval, but not when the animal had learned to expect extinction at the tested interval of time. Although the results are thus consistent with the context hypothesis, two unpublished follow-up experiments were unable to produce the converse effect: when a 4-min retention interval followed extinction with ITIs of 4 or 16 min, neither group showed spontaneous recovery. The results seem inconsistent with the temporal context hypothesis. However, they might also suggest an asymmetry in how animals generalize between ITIs: for example, a 4-min period can be construed as part of a 16min interval, so that animals trained with 16 min might readily generalize to 4 min. In contrast, a 16-min period is not part of a 4-min interval, and animals trained with 4 min might not generalize to 16 min (the present results; this idea will be developed in Section 5). We therefore set out to study how animals generalize and discriminate between 4- and 16-min ITIs in more detail by using an explicit discrimination procedure. 2. Experiment 2 In the second experiment, after a conditioning treatment similar to that used in Experiment 1, rats received extensive exposure to a procedure in which 4- and 16-min ITIs differentially preceded trials on which the tone CS was reinforced or not. There were two groups. For Group 16+/4−, the tone was reinforced when it followed a 16-min ITI but nonreinforced when it fol-

lowed a 4-min ITI. Group 4+/16− received the opposite: the tone was reinforced when it followed the 4-min ITI and nonreinforced when it followed the 16-min ITI. Notice that Group 16+/4−, but not Group 4+/16−, received a treatment analogous to the one received by the 4-min group in Experiment 1: the shorter interval signaled extinction. 2.1. Method 2.1.1. Subjects The subjects were 16 female Wistar rats of the same age and from the same supplier as those in Experiment 1. The apparatus and maintenance conditions were also the same. 2.1.2. Procedure Magazine training and conditioning followed the procedure used in Experiment 1; the six conditioning sessions again each contained eight tone-food pairings spaced in an LLSSLLSS or an SSLLSSLL sequence. At the end of this phase, two groups were formed so as to match them on performance during conditioning. Over the next 18 days, each group now received a US at the end of the CS during trials that followed one ITI (i.e., 16 or 4 min), but not during trials that followed the other (i.e., 4 or 16 min). (The ITIs once again varied ±25% around each mean.) The ITIs were scheduled so as to control for the sequence of reinforced and nonreinforced trials over sessions. For both groups, on odd-numbered days the sequence was RRNNRRNN and on even-numbered days it was NNRRNNRR. The doublealternation schedule ensured that each trial type was preceded and followed by an R or N trial with equal probability (0.5). Rats generally do not learn to anticipate R and N based on such a schedule (Mackintosh, 1974). 2.2. Results Conditioning proceeded uneventfully, and a Group × ITI × Block ANOVA on the conditioning data indicated no difference in responding between the two groups or the two ITIs, F’s < 1. Fig. 2 summarizes the results of each session of the discrimination training phase. The top panels show the elevation scores, whereas the bottom panels summarize responding during the corresponding pre-CS periods. Overall, the results were consistent with the hypothesis that the discrimination was learned more readily in the 16+/4− group than in the 4+/16− group. A Group × Reinforcement (reinforced versus nonreinforced trials) × Trial-block ANOVA indicated no main effects of Group or Block, F’s < 1.16. The Group × Block and Group × Block × Reinforcement interactions were also nonreliable, F’s < 1.06. However, the Reinforcement main effect, F(1, 14) = 33.83, and the Reinforcement × Block interaction, F(8, 112) = 3.79, were both significant. And most important, the Group × Reinforcement interaction was reliable, F(1, 14) = 31.66. The interaction took the form of less responding in the 4− trials (Group 16+/4−) than any other condition: simple effects showed no differences in the reinforced intervals between groups, F(1, 14) < 1, but a difference between the nonreinforced trials between groups, F(1, 14) = 3.95. Separate

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to the passage of time itself as represented in the pre-CS periods just before each tone. Instead, the ITIs mainly functioned to influence the rat’s responding to the tone CS. However, the results also confirm that there is an asymmetry in how animals use the 4- and 16-min ITIs. With the methods used here, there was no evidence that the rats learned to use the 4-min ITI as the positive cue and the 16-min ITI as the negative cue (the 4+/16− procedure). Since responding was generally high in both groups except for the negative 4− interval (Group 16+/4−), the failure of Group 4+/16− to learn a discrimination appeared to take the form of a failure to inhibit performance after the 16-min ITI. 3. Experiment 3

Fig. 2. Mean elevation scores to the CS (top) and pre-CS responding (bottom) of the two groups during the discrimination phase of Experiment 2. Group 16+/4− received a reinforced tone CS after 16-min ITIs and a nonreinforced CS after 4-min ITIs. Group 4+/16− received the opposite.

Reinforcement × Block ANOVAs on the data from each group supported the conclusion that the discrimination was reliable in Group 16+/4− but not 4+/16−. For Group 16+/4−, there was no Block effect, F < 1, but the Reinforcement effect, F(1, 7) = 48.17, and the Block × Reinforcement effect, F(8, 56) = 2.47, were both reliable. In contrast, in Group 4+/16−, neither effect approached significance, F’s ≤ 1.77. The corresponding ANOVA on the pre-CS scores indicated no main effects or interactions, all F’s ≤ 1.07. Fig. 2 summarizes responding at each ITI averaged over the R and N trials of the double-alternation procedure (RRNNRRNN or NNRRNNRR). Such averaging is appropriate and desirable because responding reported for each group at a given ITI always averaged over trials that followed both R and N trials. However, it is worth noting that the groups’ differential use of ITI as a cue was also evident when we isolated the first trial of each RR and NN pair. For example, during the last six sessions of discrimination training, Group 16+/4− had mean elevation scores of 7.25 and 4.79 on its first-of-each-pair R and N trials, whereas Group 4+/16− had scores of 6.56 and 6.57, interaction F(1, 14) = 11.48. Thus, the asymmetry evident in Fig. 2 was also evident on the first presentation of each ITI and was not an artifact of learning to respond on the second trial in a manner consistent with reinforcement or nonreinforcement of the first.

The third experiment was designed to extend Experiment 2 in several ways. First, because it was possible that the results were unique to a procedure in which discrimination training followed a conditioning phase, Experiment 3 examined 16+/4− and 4+/16− discriminations in which the contingencies were in place from the start. Second, the asymmetry between the 16+/4− and 4+/16− discriminations might be due to some inherent difference in the level of responding that is unconditionally supported by 4- and 16-min intervals. For example, a rat might be less fatigued, or more motivated to respond, if 16 min has elapsed since the last trial. To address such possibilities, Experiment 3 included control groups that received the same sequence of 4and 16-min ITIs without differential association with the US. That is, both ITIs ended in either a reinforced or nonreinforced tone 50% of the time (e.g. 4±/16±). Any unconditional difference in responding after the long and short intervals should be evident in such a “pseudodiscrimination” procedure. The results of the experiment did in fact replicate the asymmetry evident in Experiment 2: the 16+/4− procedure once again produced discriminative performance, whereas the 4+/16− procedure did not. To further ask whether this asymmetry was due to a failure to learn, Group 4+/16− and a pseudodiscrimination control then received an additional phase in which they were trained with the reversed 16+/4− procedure. If Group 4+/16− had learned the initial temporal contingencies, but was merely unable to respond appropriately, it might still be relatively slow to acquire the reversed 16+/4− discrimination. 3.1. Method

2.3. Discussion

3.1.1. Subjects The subjects were 32 female Wistar rats of the same age and from the same supplier as those in the previous experiments. The apparatus and maintenance conditions were also the same.

Rats that had the 16-min ITI as a positive cue and the 4-min ITI as a negative cue learned to discriminate between reinforced and nonreinforced trials. Thus, ITI can indeed function as a discriminative cue, as the context hypothesis expects. Notice that the primary effect of the ITI was to modulate, or set the occasion for, responding to the tone (e.g. see Holland, 1992, or Swartzentruber, 1995, for reviews); there was little responding

3.1.2. Procedure Magazine training was conducted as in Experiment 1. Beginning on the next day, a discrimination procedure exactly like that in Experiment 2 was conducted. Two experimental groups (16+/4− and 4+/16−) received the US after either the 16- or 4-min ITI. As before, the procedure controlled the sequence of reinforced and nonreinforced trials received by each group.

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Two new control groups (4±/16±) received half of the trials with each ITI reinforced and half nonreinforced. Each control received the same sequence of intertrial intervals as one of the experimental groups, but the R and N trials (which were still double alternated) were presented out of phase with the ITI. Thus, for example, on a day when ITIs were scheduled LLSSLLSS, the control group might receive an RNNRRNNR pattern. There were 18 daily sessions in this phase. After the last discrimination session, Group 4+/16− and its control received a 24-day reversal phase. During each daily session of the phase, rats in both groups received the discrimination treatment previously received by the 16+/4− group, in which trials after each 16-min ITI were reinforced and trials after each 4-min ITI were not. Trial sequence followed the patterns described above. The 16+/4− groups also received a reversal treatment at this time, but the results are not reported because rats never solved the 4+/16− discrimination in either phase (see also Experiment 2). 3.2. Results 3.2.1. Discrimination phase Fig. 3 summarizes the results of the discrimination phase. Group 16+/4− and its control are shown at left, whereas Group 4+/16− and its control are shown at right. In each case, the elevation scores and pre-CS scores are shown in the upper and lower panels, respectively. As in Experiment 2, the results suggest discrimination in the 16+/4− condition, but not in the 4+/16− condition. A Group × Reinforcement × Trial-block ANOVA comparing the two experimental groups (as in Experiment 2) revealed a significant effect of Block, F(8, 112) = 13.55, and a

Block × Reinforcement interaction, F(8, 112) = 4.81. No other interactions with Block were reliable, F’s ≤ 1.75. The Group effect was also not reliable, F(1, 14) < 1. However, both the Reinforcement main effect, F(1, 14) = 9.71, and the crucial Group × Reinforcement interaction, F(1, 14) = 16.73, were significant. Separate Reinforcement × Block ANOVAs conducted for each group revealed, for Group 16+/4−, that the effects of Reinforcement, F(1, 7) = 14.17, Block, F(8, 56) = 6.92, and the Reinforcement × Block interaction, F(8, 56) = 3.79, were significant. Thus, Group 16+/4− learned to respond more to the CS after the reinforced ITI. For Group 4+/16−, in contrast, there was no Reinforcement effect, F(1, 7) = 2.84, although there was a Block effect, F(8, 56) = 7.34, and a Block × Reinforcement interaction, F(8, 56) = 2.51. In this case, however, there was overall more responding in the nonreinforced, rather than the reinforced, ITI. As in Experiment 2, the Group × Reinforcement interaction was also apparent when we isolated the first R and N trials in the pairs of R and N trials involved in the double-alternation procedure. For example, during the last six discrimination training sessions, Group 16+/4− had elevation scores of 5.44 and 2.28 on its first-of-each-pair R and N trials, whereas Group 4+/16− had scores of 3.86 and 3.86, interaction F(1, 14) = 12.79. The experimental groups were also compared with their respective controls in additional Group × ITI × Trial-block ANOVAs. For the 16+/4− discrimination, there were reliable main effects of Block, F(8, 112) = 14.05, and ITI, F(1, 14) = 21.42. The Group × ITI interaction, F(1, 14) = 4.98, and the Group × ITI × Block interaction, F(8, 112) = 3.41, were also reliable. None of the other main effects or interaction approached significance, F’s ≤ 1.45. A separate ITI × Block ANOVA in the Control group indicated both a Block effect, F(8, 56) = 7.95,

Fig. 3. Mean elevation scores to the CS (top) and pre-CS responding (bottom) of the four groups during the discrimination learning phase of Experiment 3. Labels as in Fig. 2, except that Control groups received pseudodiscriminations in which tones after each ITI were reinforced half the time.

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and an ITI effect, F(1, 7) = 8.47, although the interaction was not reliable, F < 1. The control group responded more during the 16-min ITI during early sessions. However, by the end of the phase (e.g. the last four blocks), that difference no longer approached significance, F(1, 7) = 1.79. The comparison of Group 4+/16− and its control revealed only a Block main effect, F(8, 112) = 15.43. The Reinforcement effect approached reliability, F(1, 14) = 4.20, suggesting a trend toward more responding in the 4-min ITI. However, there was no Group effect or an interaction with the Group variable, F’s ≤ 2.02. Thus, the procedure in which the CS was reinforced after 4-min ITIs and nonreinforced after 16-min ITIs did not support discriminative performance that could be differentiated from a group that received the same intervals nondifferentially associated with reward. Corresponding ANOVAs on the pre-CS scores (lower panels) indicated no reliable effects, except for a Group × Block interaction in the 16+/4− versus 4+/16− ANOVA, F(8, 112) = 2.05, and a Block effect in the 16+/4− versus Control ANOVA, F(8, 112) = 2.38. Neither of these effects is confounded with the pattern in the elevation scores and thus does not suggest an alternate explanation of them. 3.2.2. Reversal phase The results of the reversal phase, where the 4+/16− group and its control now received the 16+/4− discrimination, are summarized in Fig. 4. The elevation scores suggest that the control

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group learned to discriminate rapidly, whereas the group that had received 4+/16− training did not; if anything, the experimental group inappropriately began to respond more during the 4-min ITI. A Group × Reinforcement × Trial-block ANOVA revealed nonsignificant effects of Block, Group, Block × Group, and Block × Group × Reinforcement, F’s < 1. However, the Reinforcement effect was significant, F(1, 14) = 22.48, as was the Reinforcement × Block interaction, F(8, 154) = 1.88. Most important, the Group × Reinforcement interaction, F(1, 14) = 7.21, was also reliable, and suggests that the groups differed in their discriminative performance. This was further supported by Reinforcement × Block ANOVAs conducted for each group. For Group Control, there was a reliable Reinforcement effect, F(1, 7) = 15.55, indicating that the rats responded more after the 16-min ITI than the 4-min ITI. The interaction and block effects were not reliable, F’s ≤ 1.64. In contrast, for Group 4+/16, although the Reinforcement effect was also reliable, F(1, 7) = 9.34, the animals in this case responded more during the incorrect 4-min ITI than in the 16-min ITI (Block and Block × Reinforcement F’s < 1). These results indicate that although Group 4+/16− failed to differentiate the ITIs in the first phase, they learned something in the sense that it caused greater interference with the new, reversed, 16+/4− discrimination. The corresponding ANOVA on the pre-CS scores revealed no effects that compromised interpretation of the elevation scores. There was a significant Group × Block interaction, F(8, 154) = 1.96. No other effects or interactions approached significance, largest F(1, 14) = 3.35. 3.3. Discussion Despite the absence of an initial conditioning phase in which the 16- and 4-min intervals were both reinforced, the 16+/4− discrimination was again acquired more readily than the 4+/16− discrimination. The results thus suggest that the asymmetry uncovered in Experiment 2 (and implied in Experiment 1) is replicable and apparently robust. Furthermore, although there was a modest trend toward more responding in the 16-min interval at the beginning of training in one of the pseudodiscrimination groups, the sustained discriminative performance shown by 16+/4− depended on the differential reinforcement contingency rather than some unconditional tendency to respond more after the 16-min ITI. The results of reversal training further suggest that rats exposed to the unsolved 4+/16− procedure learned something that was not evident in performance in the first phase. Specifically, these animals were slower to acquire the reversed 16+/4− discrimination than the pseudodiscrimination control. This result suggests that the asymmetry evident in the first phase depends at least in part on some performance difficulty rather than a complete failure to learn. 4. Experiment 4

Fig. 4. Mean elevation scores to the CS (top) and pre-CS responding (bottom) for Groups 4+/16− and its pseudodiscrimination control during the reversal phase in Experiment 3. At this time, both groups received a reinforced tone CS after 16-min ITIs and a nonreinforced CS after 4-min ITIs.

One explanation of the asymmetry evident in Experiments 2 and 3 might emphasize memory failure during the ITI. In the successful 16+/4− discrimination, the rat appeared to learn

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to withhold responding to the tone after the negative 4-min interval. In the difficult 4+/16− procedure, which involves a longer 16-min negative interval, the rats did not learn to withhold responding, perhaps because it is more difficult to remember the ITI onset marker (the previous trial) over the longer interval of time. Responding in the long 16-min interval in Group 4+/16− might reflect uncertainty about the previous interval. This consideration suggests that discrimination learning might be more successful, and perhaps show less asymmetry, with shorter intervals in which ITI onset might be easier to remember. The fourth experiment therefore compared discriminations that involved 1- and 4-min ITIs. One group received a 1+/4− procedure and another received 4+/1−. These preserved the 4:1 ratio used in the previous procedures, but since the previous experiments had clearly shown that the 4-min interval could be an effective cue, the memory hypothesis suggests that both discriminations might be soluble. The experiment also included a pseudodiscrimination control. 4.1. Method 4.1.1. Subjects The subjects were 24 female Wistar rats of the same age and from the same supplier as those in the previous experiments. Apparatus and maintenance conditions were also the same. 4.1.2. Procedure Magazine training was conducted following the usual procedure. Beginning on the next day, the rats received 30 days of discrimination training. The procedure was essentially the same as that in Experiment 3, except that the intertrial intervals were now either 1 or 4 min. Group 1+/4− received trials after the 1-min interval reinforced and the 4-min nonreinforced, while Group 4+/1− received the opposite. The single control group received half of the trials with each ITI reinforced. As in previous experiments, the experimental groups received trials in either an RRNNRRNN or NNRRNNRR and an LLSSLLSS or SSLLSSLL sequence; the control group received RNNRRNNR or NRRNNRRN sequences and the ITI pattern received by the 4+/1− group. 4.2. Results Fig. 5 summarizes the results of the experiment. The groups’ elevation scores and pre-CS scores are shown over each 8-trial block in the upper and lower panels, respectively. As in the previous experiments, the two experimental groups were first compared with a Group × Reinforcement × Trialblock ANOVA. There was a significant effect of Block, F(20, 280) = 1.75, and a Group × Block interaction, F(20, 280) = 2.78. No other interactions or effects were reliable, F’s ≤ 1.14, including the Reinforcement effect and its interactions with Group and Block. Somewhat unexpectedly, Group 4+/1−’s responding reached a peak and then began to decline after the initial sessions; for example, there was a significant decrease in responding from Block 4 through Block 21, F(17, 119) = 1.95, and by the last two blocks, Group 4+/1− responded less than Group 1+/4−,

Fig. 5. Mean elevation scores to the CS (top) and pre-CS responding (bottom) during discrimination training in Experiment 4. Group 4+/1− received a reinforced tone CS after 4-min ITIs and a nonreinforced tone after 1-min ITIs. Group 1+/4− received the opposite, and Group Control received a pseudodiscrimination in which tone CSs after each ITI were reinforced half the time.

F(1, 14) = 3.97, p < 0.07. Separate Reinforcement × Trial-block ANOVAs conducted for each group revealed a Block effect in both groups, F(20, 140) ≥ 2.17. No other effects or interaction were reliable in either group, F’s ≤ 1.39. An analysis comparing Group 4+/1− and the Control revealed a significant effect of Block, F(20, 280) = 3.70, and a Group × Block interaction, F(20, 280) = 2.88. No other effect or interaction approached significance, F’s ≤ 1.16. A separate analysis for the control group indicated a reliable Block effect, F(20, 140) = 3.80, and no ITI effect or ITI × Block interaction, F’s ≤ 1.28. The analysis comparing Group 1+/4− and the control also revealed a significant effect of Block, F(20, 280) = 5.32, and a Group × ITI × Block interaction, F(20, 280) = 1.64. Once again no other effects or interactions were significant, F’s ≤ 1.34. In contrast with the previous experiments, the analysis of the pre-CS scores revealed important differences. The Group × Reinforcement × Trial-block ANOVA comparing the two experimental groups revealed a significant effect of Block, F(20, 280) = 2.07, and a Reinforcement × Block interaction, F(8, 280) = 2.89. The Reinforcement main effect was also reliable, F(1, 14) = 16.58; the groups learned to respond more in the pre-CS periods before reinforced trials. No other effects were reliable, F’s ≤ 3.00. Group 4+/1− appeared to respond more than Group 1+/4− did during its reinforced ITI, although

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the difference was not significant, F(1, 14) = 3.08, p = 0.10. Separate Reinforcement × Trial-block ANOVAs for each group revealed, for Group 4+/1−, significant effects of Reinforcement, F(1, 7) = 9.46, Block, F(20, 140) = 1.75, and a Reinforcement × Block interaction, F(20, 140) = 2.07. For Group 1+/4−, there was no Block effect, F(20, 140) = 1.00, although there was a Reinforcement effect, F(1, 7) = 11.19, and a Block × Reinforcement interaction, F(20, 140) = 2.14. Interestingly, the asymmetry suggested in the experimental groups’ discriminative responding during the pre-CS period was even more evident when we examined the first R and N trials of the RR and NN pairs of the double-alternation procedure. For example, during the last two sessions of training, Group 4+/1− had average scores of 6.17 and 1.47 during the first-of-each-pair of R and N trials, whereas Group 1+/4− had scores of 2.42 and 1.53, interaction F(1, 14) = 4.69. If anything, a stronger interaction was possible when we examined first trials (rather than all trials, as analyzed above and presented in Fig. 5) because for Group 1+/4− responding during the second R trial was exaggerated by delivery of the US only 1 min before. The experimental groups were also compared with the control group with additional Group × ITI × Trial-block ANOVAs. For the 4+/1− discrimination, there was a reliable Group × Block effect, F(20, 280) = 1.82, Reinforcement effect, F(1, 14) = 4.72, and a Group × Reinforcement interaction, F(1, 14) = 14.77. The Group effect, F(1, 14) = 4.22, the Block effect, F(20, 280) = 1.49, and the ITI × Block interaction, F(20, 280) = 1.56, each approached the significance (p’s = 0.06, 0.08, and 0.06, respectively). The ANOVA comparing 1+/4− with the control revealed a reliable Block effect, F(20, 280) = 5.32, and a Group × Reinforcement × Block effect, F(20, 280) = 1.64, although no other effect or interaction approached significance, F’s ≤ 1.34. The separate ITI × Block ANOVA in the Control group indicated significant ITI effect, F(1, 14) = 15.85, although the Block effect or the Block × ITI interaction were not, F’s ≤ 1. 4.3. Discussion Based on the elevation scores, it is clear that the rats in the present experiment did not use the ITI to modulate responding to the tone. There was no difference in elevation scores in the positive and negative intervals of either the 4+/1− or the 1+/4− discrimination. Interestingly, although the positive elevation scores indicate that the rats had learned that the tone was a signal for food, its power as a signal declined over the course of training in the 4+/1− group. Equally important, although there was little evidence that the 1- and 4-min intervals modulated responding to the tone, the animals clearly did learn the temporal aspects of the procedure. In this experiment, unlike the others (where longer ITIs were used), the rats responded more during the pre-CS period that preceded trials that were about to be reinforced. In this experiment, time in the ITI was thus used as a direct signal, or CS+, for food. In effect, instead of using ITI as an occasion setter, the rats used it as an eliciting cue. And interestingly, especially in the 4+/1− discrimination, the temporal signal appeared to reduce the control of responding by the tone, which systematically declined

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during training. In associative learning terms, the ITI cue was a more valid predictor of the reinforcer and began to “block” (Kamin, 1969; Wagner et al., 1968) conditioning to the tone. 5. General discussion The results of Experiment 1 suggest that the ITI is coded as part of the “context” that can be connected with, and control, extinction. When rats received extinction trials separated by a mean of 4 min, there was a recovery of responding after a 16-min retention interval. When there was no change in the interval between trials (that is, when extinction was conducted with a 16-min ITI before the 16-min retention interval), there was no recovery of responding. The results were thus consistent with the possibility that the ITI of extinction trials may play the role of a context, which theoretically functions as a negative occasion setter and suppresses responding to the CS (e.g. Bouton, 2004). Experiments 2–4 further investigated this effect of the “ITI context.” Experiments 2 and 3 both compared explicit conditional discriminations trained with the 4- and 16-min ITI. In both experiments, a 16+/4− discrimination was learned and took the form of occasion setting by the ITI: the time since the last trial modulated responding to the next CS, but did not elicit responding on its own prior to presentation of the tone. However, the results of Experiments 2 and 3 also suggest that the 16+/4− and 4+/16− discriminations were asymmetrical. That is, although the 16+/4− discrimination was readily learned, there was little evidence that exposure to the contingencies of the 4+/16− discrimination came to control performance. The fact that pseudodiscrimination controls in Experiment 3 (for which the ITIs were equally associated with reinforced and nonreinforced trials) showed no persistent difference in responding to the tone after 16- and 4-min ITIs suggests that difficulty with the 4+/16− discrimination was not merely due to a conflicting unconditional tendency to respond more in the 16-min ITI. Moreover, the results of the reversal phase in Experiment 3 indicated that the difficulty with the 4+/16− discrimination was at least partly a difficulty with performance rather than learning. When the contingencies were reversed, rats that had first received the 4+/16− discrimination had more difficulty learning 16+/4− than a control group that had received the pseudodiscrimination. The group’s difficulty with the reversal suggests that they had in fact learned something during 4+/16− training that interfered with 16+/4−. Experiment 4 examined discriminations with shorter ITIs. Since the 4-min ITI had been an effective cue in the preceding experiments, it seemed likely that the rats would learn either the 4+/1− or the 1+/4− discrimination. In Experiment 4, both discriminations were in fact learned. However, performance took a new and different form: in either discrimination, the animals used the ITI to anticipate the reinforcer directly, before the CS itself was presented, and responded indiscriminately in the presence of the CS. The tendency to anticipate reinforcement during the pre-CS period was especially pronounced in the 4+/1− discrimination, where the temporal cue further “blocked” conditioning with the CS in the sense that responding to the CS began to decline. In effect, the animals in Experiment 4 used the 1- and

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4-min ITIs as simple CSs, rather than modulators or occasion setters, as they had with the 4- and 16-min ITIs in the earlier experiments. And the stronger control and stronger blocking in the 4+/1− condition suggests that the previous L+/S− and S+/L− asymmetry was not eliminated here. The shift to more direct control by time in Experiment 4 is consistent with the idea that shorter ITIs are more “salient” stimuli than longer ones. In fact, there is a parallel between the present pattern and earlier research on occasion setting with brief auditory and visual CSs (e.g. see Holland, 1992, or Swartzentruber, 1995 for review). In experiments in which a target auditory CS (A) was reinforced when it was in simultaneous compound with a visual cue (X), but not when it was presented alone (i.e., XA+/A−), Holland (1989) found that occasion setting by X (where X modulated responding to A rather than merely eliciting performance of its own) developed when X was less salient than A. In contrast, when X and A were more equal in salience, X became a simple excitatory CS that elicited responding on its own and blocked conditioning of CS A. The parallel is as follows. When relatively long ITIs were used in the current method (Experiments 2 and 3), they functioned as occasion setters: they modulated responding to the tone, but elicited little responding in the pre-CS period on their own. In contrast, when short ITIs were used (Experiment 4), there was relatively little occasion setting, and strong control of responding in the pre-CS period. The parallel suggests that ITI cues may function like stimuli from auditory and visual modalities. Just as with auditory and visual cues, relatively salient temporal intervals are more readily used as CSs rather than occasion setters. What type of temporal coding would lead to the current results? It is possible that the start of each ITI started a clock in which time was represented as a count in an accumulator (e.g. Gibbon et al., 1984), the behavioral state in a sequence of behavioral states (e.g. Killen and Fetterman, 1988), or the read-out of an array of oscillators that cycle through different states with different periods (e.g. Church and Broadbent, 1990). However, without additional assumptions, it is not clear that the models that use these codes are ready to explain why: (1) shorter ITIs seem more salient than longer ones, and thus operate as CSs rather than occasion setters, or (2) why the 16+/4− discrimination was easier to solve and/or express in performance than the 4+/16− discrimination. One explanation might be the following. We might suppose that the strength of a memory trace of the CS presented on a trial might gradually decline over time in the ITI that follows. The strength of that trace at any point in time would be proportional to the duration of the current interval, and timing might be accomplished by associating the contemporary strength of the trace with reinforcement or nonreinforcement (cf. Staddon and Higa, 1999). Let us call the strength of the shorter of the two ITIs S, and the strength of the trace at the longer of the two ITIs L. Although S and L are both available to code different ITI durations, it is important to recognize that presentation of L (e.g. the strength of the trace at 16 min) always first requires going through S (the strength of the trace at 4 min). Thus, a 16-min ITI always involves the serial compound S → L. Thus, the 16+/4− discrimination took the form of a S → L+/S− dis-

crimination, a feature-positive discrimination in which L is the positive feature. In contrast, the 4+/16− discrimination took the form of S+/S → L−, a feature-negative discrimination in which L is a negative feature. Although feature-positive and featurenegative discriminations can both be learned, it has been shown that feature-negative discriminations are inherently more difficult (e.g. Hearst, 1978; Jenkins and Sainsbury, 1970), and that the difference is at least partly due to a difficulty in performance (Hearst, 1987). Thus, if time is coded as a serial compound, then the current asymmetry in the 16+/4− and 4+/16− discriminations has a precedent in the “feature-positive effect”, a phenomenon that appears general across different stimuli, preparations, and species (e.g. Hearst, 1978, 1984). This emphasis on the strength of the memory trace as the temporal code has a further advantage. If one further supposes that the memory trace literally fades systematically over time, then the trace corresponding to a very short ITI would be relatively strong and salient—and able to function as a simple CS (Experiment 4; see discussion above). In contrast, with longer intervals, the trace would become correspondingly faint and less salient, and thus more ready to function as an occasion setter (Experiments 1–3; see discussion above). Of course, time provides more than just a stimulus; it can have many other effects, because many crucial conditioning processes change as a function of time. For example, Bouton and Sunsay (2003) and Sunsay et al. (2004) have previously shown that when conditioning trials in this preparation are separated by 1-min ITIs (but not 4-min ITIs), presentation of the CS or US on trial n may interfere with learning and performance on trial n + 1 through a mechanism consistent with “self-generated priming” in Wagner’s “sometimes opponent process” theory (e.g. Wagner, 1981). That is, presentation of a CS or US may briefly put it in a refractory state on trial n + 1 such that learning or performance may be hampered. Such priming of the US may have played a role in Experiment 4, where less temporal conditioning appeared to develop in the reinforced 1-min ITIs (Group 1+/4−) than in the reinforced 4-min ITIs (Group 4+/1−). Whatever the value of these ideas, the results of the current experiments suggest that intertrial interval can indeed play the role of context in determining performance to a CS. They also provide some new constraints on how animals might code the passage of time in the ITI. Conceptualizing the passage of time as a fading trace or sequence of stimuli that operates according to familiar laws of associative learning may go some distance in capturing the results reported here. Acknowledgments This research was supported by Grant RO1 MH64847 from the National Institute of Mental Health. We thank Richard Morris and Amanda Woods for their discussion. References Bouton, M.E., 1993. Context, time, and memory retrieval in the interference paradigms of Pavlovian learning. Psychol. Bull. 114, 80–99.

M.E. Bouton, A. Garc´ıa-Guti´errez / Behavioural Processes 71 (2006) 307–317 Bouton, M.E., 2002. Context, ambiguity, and unlearning: sources of relapse after behavioral extinction. Biol. Psychiat. 52, 976–986. Bouton, M.E., 2004. Context and behavioral process in extinction. Learn. Memory 11, 485–494. Bouton, M.E., Sunsay, C., 2003. Importance of trials versus accumulating time across trials in partially reinforced appetitive conditioning. J. Exp. Psychol. Anim. Behav. Proc. 29, 62–77. Bouton, M.E., Nelson, J.B., Rosas, J.M., 1999. Stimulus generalization, context change, and forgetting. Psychol. Bull. 125, 171–186. Brooks, D.C., Bouton, M.E., 1993. A retrieval cue for extinction attenuates spontaneous recovery. J. Exp. Psychol. Anim. Behav. Proc. 19, 77–89. Capaldi, E.J., Morris, M.D., 1976. A role of stimulus compounds in eliciting responses: relatively spaced extinction following massed acquisition. Anim. Learn. Behav. 4, 113–117. Church, R.M., Broadbent, H.A., 1990. Alternative representations of time, number, and rate. Cognition 37, 55–81. Church, R.M., Deluty, M.Z., 1977. Bisection of temporal intervals. J. Exp. Psychol. Anim. Behav. Proc. 3, 216–228. Ernhart, C.B., 1960. Response strength as a function of changed intertrial interval. J. Exp. Psychol. 60, 208–215. Gallistel, G.R., Gibbon, J., 2000. Time, rate, and conditioning. Psychol. Rev. 107, 289–344. Gibbon, J., Church, R.M., Meck, W.H., 1984. Scalar timing in memory. In: Gibbon, J., Allen, L. (Eds.), Academy of Sciences, vol. 423. New York Academy of Sciences, New York, pp. 52–77. Hearst, E., 1978. Stimulus relationships and feature selection in learning and behavior. In: Hulse, S.H., Fowler, H., Honig, W.K. (Eds.), Cognitive Processes in Animal Behavior. Erlbaum, Hillsdale, NJ, pp. 51–88. Hearst, E., 1984. Absence of information: some implications for learning, performance, and representational processes. In: Roitblat, H.L., Bever, T.G., Terrace, H.S. (Eds.), Animal Cognition. Erlbaum, Hillsdale, NJ, pp. 311–332. Hearst, E., 1987. Extinction reveals stimulus control: latent learning of feature-negative discriminations in pigeons. J. Exp. Psychol. Anim. Behav. Proc. 13, 52–64. Holland, P.C., 1989. Occasion setting with simultaneous compounds in rats. J. Exp. Psychol. Anim. Behav. Proc. 15, 183–193. Holland, P.C., 1992. Occasion setting in Pavlovian conditioning. In: Bower, G. (Ed.), The Psychology of Learning and Motivation, vol. 28. Academic Press, Orlando, FL, pp. 69–125.

317

Holland, P.C., 2000. Trial and intertrial durations in appetitive conditioning in rats. Anim. Learn. Behav. 28, 121–135. Jenkins, H.M., Sainsbury, R.S., 1970. Discrimination learning with the distinctive feature on positive or negative trials. In: Mostovsky, D. (Ed.), Attention: Contemporary Theory and Analysis. Appleton-Century-Crofts, New York, pp. 239–273. Kamin, L.J., 1969. Predictability, surprise, attention, and conditioning. In: Campbell, B.A., Church, R.M. (Eds.), Punishment and Aversive Behavior. Appleton-Century-Crofts, New York, pp. 279–296. Killen, P.R., Fetterman, J.G., 1988. A behavioral theory of timing. Psychol. Rev. 95, 274–295. Kirkpatrick, K., Church, R.M., 2000. Independent effects of stimulus and cycle duration in conditioning: the role of timing processes. Anim. Learn. Behav. 28, 373–388. Lattal, K.M., 1999. Trial and intertrial durations in Pavlovian conditioning: issues of learning and performance. J. Exp. Psychol. Anim. Behav. Proc. 25, 433–450. Mackintosh, N.J., 1974. The Psychology of Animal Learning. Academic Press, London. Moody, E.W., Sunsay, C., Bouton, M.E. (in press). Priming and trial-spacing in extinction: effects on extinction performance, spontaneous recovery, and reinstatement in appetitive conditioning. Quart. J. Exp. Psychol. Roberts, S., 1981. Isolation of an internal clock. J. Exp. Psychol. Anim. Behav. Proc. 7, 242–268. Smith, S.M., Vela, E., 2001. Environmental context-dependent memory: a review and meta-analysis. Psychon. Bull. Rev. 8, 203–220. Spear, N.E., 1978. The Processing of Memories: Forgetting and Retention. Erlbaum, Hillsdale, NJ. Staddon, J.E.R., Higa, J.J., 1999. Time and memory: towards a pacemakerfree theory of interval timing. J. Exp. Anal. Behav. 71, 215– 251. Sunsay, C., Stetson, L., Bouton, M.E., 2004. Memory priming and trial spacing effects in Pavlovian learning. Learn. Behav. 32, 220–229. Swartzentruber, D., 1995. Modulatory mechanisms in Pavlovian conditioning. Anim. Learn. Behav. 23, 123–143. Wagner, A.R., 1981. SOP: a model of automatic memory processing in animal behavior. In: Spear, N.E., Miller, R.R. (Eds.), Information Processing in Animals: Memory Mechanisms. Erlbaum, Hillsdale, NJ, pp. 5–47. Wagner, A.R., Logan, F.A., Haberlandt, K., Price, T., 1968. Stimulus selection in animal discrimination learning. J. Exp. Psychol. 76, 171–180.