Sampling behavior and contextual change

LEARNING

AND MOTIVATION

20, 97-114 (1989)

Sampling Behavior and Contextual Change LYNN

DEVENFQRT

University

of Oklahoma

The setting in which learning occurs has been ascribed many functions in recent years. One prominent role is the support of memory retrieval, and the attendant possibility of forgetting when the training context is changed. However, forgetting may sometimes be an overly strong interpretation of the performance decrements that attend a contextual change (CC). Instead, a critical analysis of the CC phenomenon suggests that contextual change effects (CCEs) might be more properly viewed as instrumental behavior, not impairments. This possibility was examined in two radial maze experiments that were designed to determine whether CCEs were flexible responses that could conform to opportunity, or if they were rigid failures of memory. Clear support was obtained for the adaptive alternative. When opportunity was provided, rats displaced their CC-induced “errors” to follow the correct response after the reward was collected. This would have been impossible if forgetting had occurred. Animals not provided with this opportunity displayed the “errors” expected by conventional accounts of CC. Analysis of vigilant behavior and running time revealed a dissociation between these dimensions of behavior and unbaited arm visits, indicating that the CC had an important impact upon the animal, but not upon its memory. These findings, and an examination of related literature, suggest that CCEs may often represent “sampling” behavior-investigative responses that could supply OCCaSiOn-Setting

infOITIIatiOn.

0 1989 Academic

Press.

Inc.

It is beyond doubt that animals perform best if they are tested in a setting that resembles as closely as possible the one in which they were trained. Evidence for this observation is extensive and spans classical conditioning (Pavlov, 1927/1960, p. 46), instrumental conditioning (Estes, 1970), and verbal learning (Bower, 1970). Striking instances can also be found in the behavioral pharmacology literature (Ho, Richards, & Chute, 1978) on drug-dissociated or state-dependent learning (SDL). The powerful role of context is indisputable, but there is a diversity of opinion as to how it actually exercises its influence. For instance, the This research was supported by USPHS Grant AA05699-05 and was prepared for publication while the author was a James McKeen Cattell Fellow. Address correspondence and reprint requests to Lynn Devenport, Department of Psychology, University of Oklahoma, Norman, OK 73019. 97 0023-969(X39 $3.00 Copyright 0 1989 by Academic Press. Inc. All rights of reproduction in any form reserved.

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training context can be regarded as functionally equivalent to a CS that either competes with the nominal CS (Gibbon & Balsam, 1981) or enters into a compound with it (Rescorla & Wagner, 1972; Wagner & Rescorla, 1972). Accounts such as these derive most of their support from Pavlovian conditioning procedures. Others, emphasizing instrumental learning, have offered more cognitive explanations of contextual change (CC). One of the most influential suggests that contextual stimuli convey information cibout the relationships that prevail in that setting, without actually taking part in those relationships. From this view, contexts could serve a memory retrieval function (Estes, 1973; Spear, 1973, 1978) by specifying the appropriate information to select from storage. This paper is primarily concerned with instrumental learning and therefore, retrieval theory. It is not the validity of retrieval theory that is in question; rather, its indiscriminate use. A consideration of retrieval theory’s limitations leads to the conclusion that there may be milder forms of CC that do not give rise to forgetting, but may lie on a continuum alongside those that do. One limitation concerns our previous finding that contextual change effects (CCEs) are often eliminated by mild ethanol intoxication (Devenport & Cater, 1985; Devenport, Devenport, & Holloway, 1981) and damage to the hippocampal formation (Devenport et al., 198 1; Wickelgren & Isaacson, 1963). The paradox here lies in the conflicting notions that CNS insult and the attendant impairment of processing could improve memory. We would not claim that it is impossible to reconcile these facts with retrieval theory, but simply that it requires a special effort to do so. Indeed, one might legitimately reinterpret these findings along more conservative lines and propose that CCEs are actively orchestrated by the intact CNS and lost when it is impaired. Another paradox is that the very action retrieval theory invokes to account for CCEs would seem to rob animals of an indispensable process. No situation ever presents itself in exactly the same way. The sensory and motivational features of a setting cannot be held perfectly constant; time also passes, new events intervene, and the subject ages. In the wild, the vagaries of weather, predation, competition, and inexorable daily and seasonal fluxes are the rule. Memory must always bridge these contextual dissimilarities. Thus, the adaptive value of experience depends entirely upon its generalizability. As Shepard (1987) recently observed “...an animal would be ill served by the assumption that just because it can detect a difference between the present and a previous situation, what it learned about that previous situation has no bearing on the present one” (p. 1319). As to its evidential foundation, the retrieval theory of CCEs is necessarily weak, In most reports, disruption of trained performance stands as the sole basis from which a forgetting interpretation is inferred. Such negative outcomes can rarely provide decisive support for any particular point of

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view, including memory retrieval, as Spear (1978) has pointed out. Thus, there is ample opportunity for alternative interpretation. Contextual changes might precipitate activities that have nothing to do with memory failure, but could be misinterpreted as such. The presentation of novelty, whether in the form of new contextual stimuli, drugs, or time of day, is an incitement to attentional distraction, timidity, and, quite possibly, exploration. These behaviors, while degrading the performance of the target task, might nevertheless represent organized responses to change. In nature, change is common and animals devote considerable time to “sampling” relevant aspects of their environment, even at the expense of prey loss (e.g., Houston, Kacelnik, & McNamara, 1982; Smith & Sweatman, 1974). The gain from this activity is updated information about current resources and their comparative value which, in turn, is thought to guide decision-making toward optimality (Krebs, Kacelnik, & Taylor, 1978). There is no reason to believe that sampling behavior is withheld in laboratory settings (Lima, 1985; Mellgren, Misasi, & Brown, 1984). Indeed, even in the absence of physical CC, many of the incorrect responses (“errors”) commonly observed from session to session and ascribed to incomplete learning may be cases of spontaneous investigative behavior (Brown & Cook, 1986). It seems that perceived dissimilarity between one situation and another, or the same situation at different times, may prompt some uncertainty about whether previously learned relations still apply, not only to the formal task but to incidentals as well. Probably foremost among the latter is whether the apparatus and vicinity is still safe: Fear, up to a point, is a strong inducement to exploration (Blanchard, Kelly, & Blanchard, 1974; Halliday, 1966). This could explain why habituation (Hall & Channel], 1985) or other preexposure (Lovibond, Preston, & Mackintosh, 1984) to a prospective test context often diminishes its impact on behavior. The more privileged status that rats accord danger may also explain in a general way why fear-motivated behavior is sometimes impervious to contextual changes (Kaye, Preston, Szabo, Druiff, & Mackintosh, 1987) and may even become renewed from extinction carried out elsewhere (Bouton & Bolles, 1979). Localization is another factor. If the apparatus is a maze or other open piece of equipment, the new context has to be examined from a variety of positions in order to update relations among external stimuli and integrate them into “cognitive maps” of the area (O’Keefe & Nadel, 1978; Olton & Samuelson, 1976; Tolman, 1948). This activity, like the others mentioned, bears all the trappings of error and forgetting, but strictly speaking,, is neither. There is thus a host of factors that could precipitate temporary disruptions of appetitively motivated behavior following the introduction

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of a CC. Many involve the renewal of sampling behavior. A disruption of this kind does not necessarily imply a failure of memory retrieval or any other process. To the contrary, instigation of sampling critically depends upon the recognition of a mismatch between current conditions and a mnemonic representation of the past. Thus, recourse to a subtler account of CC may be needed for cases in which the CC affects performance but is not dramatic enough to impair memory. The modified account would not focus on retrieval of memories, but rather on the applicability of the remembered relations to the new situation. When stimuli change, expectations are likely to be thrown into doubt until sampling behavior confirms or disconfirms their continued utility. Among their other differences, there is a pivotal distinction between the strong (retrieval) and subtle (applicability) accounts of CCEs that is easy to recognize, and sets them completely apart. Context change effects are regarded as impairments-mistakes and errors-in the former, but as instrumental “sampling” responses in the latter case. This is the hallmark we will employ to differentiate the two processes in Experiment 1. EXPERIMENT

1

The aim of this experiment is to bring about CCEs by means of a room change after training is complete. To this extent the study is conventional. Where it differs is in a feature that permits characterization of the “errors” precipitated by the environmental change. The custom of removing an animal from its apparatus following goal attainment (or an otherwise “correct” response) places a constraint upon sampling behavior. It obliges animals to conduct their information-gathering prior to executing the correct response, for there is no opportunity afterward. This has the effect of completely confounding error with sampling. Since this is exactly the problem we wish to unconfound, a group of animals is included in this experiment that is consistently afforded an opportunity to explore the apparatus after completing a trial. This extra time provides an opportunity for the animals to explore the maze after running directly to the baited arm. If CCEs are instances of sampling, then at least some of this sampling should be displaced to the extra time that is set aside. Thus, when conditions change, animals in this group can confirm the continued presence of food in the marked arm, ingest it, and then reinvestigate the maze without conflict. Rats treated in the usual manner, however, would be forced to commit an error in order to update maze conditions. Such a procedure should fairly cleanly separate errors based on forgetting from those based on information-gathering. Method Subjects and apparatus. Fifteen Sprague-Dawley rats (280-320 g) were food-deprived and maintained at 80% of free-feeding body weight by

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supplemental feeding of Purina chow. They were housed individually in cyclic light (LD 12:12) and were run in the middle of the lights-on phase. The animals were trained on one of two identical eight-arm radial mazes. A radial maze task was selected because of the multiple avenues for sampling it presents (see Devenport & Merriman, 1983; or Devenport & Cater, 1985). The mazes were constructed of wood and painted flat black according to specifications detailed elsewhere (Devenport & Merriman, 1983; Olton & Samuelson, 1976). A yellow carpet insert (cuing method adopted from Jarrard, Okaichi, Steward, & Goldschmidt, 1984), 20.3 x 8.9 cm, fitted snugly into the entrance of an arm and marked the route to the single site of reward (BioServe precision pellets, 90 mg). Procedure. The rats were trained in one of two rooms, both of which contained a radial maze. The rooms differed slightly in their dimensions (2.75 x 5 m vs 3.75 x 5 m) but most especially in their furnishings (desk and chairs in one, stored equipment in the other), wall attachments (differing calendars and posters), and presumably their olfactory characteristics. After being introduced into the distal end of a randomly selected arm of the maze (and not into the central compartment, as is typical), the rats were allowed to move freely from arm to arm for up to 2 min until they found the reward and consumed it. Some of the animals (no extra time-NET, n = 8) were removed to a plastic holding cage at this time, while the others (ET, II = 7) remained in the maze where they were free to explore until 1 min had elapsed. Beginning in session 8, the extra time was reduced to 30 s. After the alloted time, ET rats were also returned to a holding cage were they awaited a new trial. Every session comprised three such trials, the start arm shifting randomly. With each new session, the location of reward shifted randomly as well, except that the start arm and baited arm never coincided. The carpet insert always tracked the correct arm and provided a reliable place cue. The cuing of the place task was necessary because a planned contextual change would have eliminated the means of locating the reward on the basis of extramaze cues. During two preliminary shaping sessions procedures were relaxed, allowing time for the extensive exploration that typically occurs. The animals were allowed up to 10 min to consume the 90-mg reward which was at first placed near the entrance of the baited arm, but with successive trials, was moved closer to its final position at the distal end of the arm. During the preliminary session, ET animals were also accustomed to receiving their additional minute post-reward. Data were not collected during these shaping sessions. Sixteen formal sessions followed. They were conducted daily at the same time, 6 days a week. On Day 17 (test), the training context was changed. The rats exchanged rooms and mazes (counterbalanced) and testing continued for 7 days. Otherwise procedures remained unchanged, including the ET-NET conditions.

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Measurements and statistics. Unbaited arm entries (“errors”) that occurred before (for ETs and NETS) and after (ETs only) correct arm selection were counted, and the time elapsing between placement in the maze and entry into the correct arm was recorded. Also, the incidence of vigilant behavior was noted. These were cases of attention directed to non-goal sources of stimuli which interrupted the routine of mazerunning. They typically consisted of orienting or rearing responses accompanied by scanning and sniffing. The objective criterion used in scoring vigilance was that the attentive behavior be accompanied by a temporary halt of locomotion (stoppages without vigilance, such as grooming, were not counted). The vigilant responses were counted during each trial and the total taken as a rough index of renewed attention. All data were submitted to analysis of variance (ANOVA), and when justified, to individual comparisons. All test values cited, except when otherwise noted, meet the criterion of (Y = 0.05.

Results Analysis of errors (prior to the correct response) made across training sessions found the ET treatment to significantly reduce their commission (F(1, 13) = 5.71), and as can be seen in Fig. 1, to flatten the slope of the acquisition curve plotted across sessions (F(15, 195) = 1.9). Within sessions, unbaited arm entries diminished somewhat by the last of the three trials, but this trend did not attain statistical significance, nor were these trial effects reduced or amplified across successive sessions or between experimental treatments. Running time and vigilance (measured up to the occurrence of the correct response) diminished across sessions (Fs(1.5, 19.5) = 5.85 and 4.9, respectively), but were not signficantly differentiated between groups or trials. These results are illustrated in Fig. 2. During the transitional period (Days 16-17, Fig. 3), when the room

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FIG. 1. Mean errors (unbaited arm entries prior to a baited arm entry) per trial across the 16 training sessions of Experiment 1.

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and maze change occurred, error commission by ETs was unchanged, but that of NETS was significantly increased, resulting in a significant interaction (F(1, 13) = 5.34). However, if the total errors (both pre and post correct response) committed by ET rats during transition is included in the analysis, the groups X room change interaction disappears, for the ET subjects also increased their total visits from a mean of 0.62 per 08r o--o 06.

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FIG. 3. Mean errors (unbaited arm entries prior to a baited arm entry) per trial across the last day of training (session 16) and the first day of contextual change (session 17) of Experiment 1.

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trial (session 16) to 1.58 per trial (session 17). The extra visits to empty arms occurred almost exclusively during the extra time allotted. The initial run itself was nearly errorless. Running time across the transitional sessions paralleled the error data: the increase in time taken to obtain the reward otherwise brought about by the room change was eliminated by ET, resulting in a significant interaction with group (F(1, 13) = 5.09). In contrast, an increase in vigilance was observed in both groups (F( 1, 13) = 12.0). Although less dramatic in ETs, the difference between the groups was not significant in either an absolute or interactive sense. The effects of CC on running time and vigilance are depicted in Fig. 4. The effects of the CC were transient. During the remaining 7 days following the room change, groups were practically undifferentiated, with only a marginally reliable group x session effect, (F(1, 13) = 1.61, p < .15), for errors, and a matching decline in running time and vigilance. Discussion Context-change effects were exhibited by rats trained and tested in the usual manner. The animals increased their error rate, slowed their

16

17

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FIG. 4. Mean running time (A) and vigilant responses (B) per trial across the last day of training (session 16) and the first day of contextual change (session 17) of Experiment I.

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running time, and displayed bursts of vigilant behavior. Rats accustomed to exploring the maze after taking their reward (ETs) made no mistakes in arm selection. They did, however, exhibit the tentativity one would expect of animals thrust into a new setting-they exhibited more stoppages and greater attention to their surroundings. Then, after taking the reward, they actively explored unbaited arms, expending about the same amount of time that it took NET rats to complete their prereward investigations. These findings yield clear evidence of the impact of the CC. That the dissociation between heightened vigilance and formal performance (i.e., “error” commission) was obtained in the ETs implies that the room change was not sufficient to impede memory retrieval, but enough to encourage information-gathering. When this sampling occurred depended upon the groups’ respective opportunities. The conventional practice of removing animals from the apparatus or performance site before they have explored obliges them to displace this activity anterior to the correct response. This falsely lends the appearance of error. Most of the “errors” committed by NETS can now be reinterpreted as exploratory acts that arise as a joint consequence of uncertainty and an arbitrary procedural convention. The potential confound arising from the practice of removing the subject after a correct response was not restricted to the CC session. It also made an appearance during the training phase: NET rats generated about twice as many prereward “errors” as a result of the laboratory constraint. Slow to decline, and never disappearing entirely, the unbaited arm entries can misleadingly depict learning as an extended struggle. These findings confirm the conclusions of Brown and Cook (1986) that rats (and other species, see Wilkie & Spetch, 1980) sometimes make errors despite an anticipation of nonreward... (p. 270). That is, their mistakes are in some sense “deliberate.” Of course, we cannot conclude that all these unbaited arm entries are organized responses. Some of them are true errors. By the same token, of the few prereward entries exhibited by ETs, many may have been instances of sampling; our method provided opportunity for postreward investigation, but no proscription against similar prereward activities. What we can conclude is that the contribution of sampling is at the very feast equal to the difference between the respective values lying along the NET and ET curves in Fig. 1, i.e., 50-66% of NET errors. This experiment attempted to hold maze exposure time constant. The extra time provided (postreward) to the group of the same name was calculated in advance to approximate the time expended (prereward) by conventionally trained animals. However, in accomplishing this aim (total maze time did not differ significantly between groups), another difference emerged. Procedurally speaking, NET rats learned the maze by preceding the correct response with a string of errors; ETs learned by following

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the correct response with a similar string. Moreover, the performance differences apparent in session 1 imply that the sequence explore-seek food (NETS) vs seek food-explore was adopted during the preliminary training sessions. It is therefore at least superficially true that ET rats learned to run the maze differently from NETS. Experiment 2 was designed to assure that the elimination of CCEs by the ET group was owing to opportunity to explore during the CC and not simply to differences in the way they learned the maze. The following experiment held prereward errors and running time constant across both groups. EXPERIMENT

2

If the unbaited arm entries of conventionally trained rats (NETS) are mostly errors, little can be done to eliminate them. On the other hand, if they are instrumental responses in the service of information-gathering, as assumed, then the rats should be at least moderately sensitive to a contingency placed against such activities. In this experiment a dependency was established such that a trial was ended and reward lost if an incorrect arm was chosen. Thus, unlike the previous experiment in which animals were allowed to “correct” themselves, a noncorrection (NC) rule was in force. The chief aim of this experiment, if successful at reducing unbaited arm visitation, was to determine if animals that learned to perform errorlessly throughout training were susceptible to CCEs. A companion group of animals were run subject to these same NC conditions. They, however, were afforded the same postreward ET as rats in the previous experiment. Method Subjects and procedure. Twenty animals of the same age, strain, and sex as those in Experiment 1 were maintained in similar housing conditions. They were deprived and held at 80% free-feeding body weight for the duration of the experiment. The light-dark cycle was as in the previous experiment, and the rats were run during the middle of the light phase. The subjects were trained in the same pair of apparatus and room combinations previously described. During the two initial shaping sessions, the noncorrection rule was suspended. The animals were allowed 5 min to obtain their reward without interference. These rewards were placed near the central compartment at first and were gradually moved nearer the food reservoir at the end of the arm. As previously described, the reward arm was randomly shifted with each session and the start arm was randomly changed with every trial. The baited arm was marked with the yellow carpet insert. With the beginning of formal sessions, a noncorrectidn rule was in force that proscribed unbaited arm entries. In the event of such an entry, the animal was removed from the maze, the trial ended, and the potential

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reward was lost. Three trials separated by 60 s were permitted during each of the 16 sessions. The same procedures were applied to ET rats, except they were provided with a 60-s (after session 8, a 30-s) opportunity to investigate any part of the maze, provided that at first they ran directly to the baited arm. After completion of training (session 16), the animals were tested as before in a new context and maze. And as before, this contextual change was counterbalanced (A to B = B to A) within groups. Beginning with CC, the noncorrection rule was suspended. The animals were free to visit as many unbaited arms prior to the baited one as permitted by the 2-min trial limit. Running time was now defined as that amount elapsing prior to baited arm selection. Behavioral measures were as before, except that during training, running time was defined as the time taken to run to the correct or incorrect arm of the maze. Statistical analysis was as in Experiment 1, with (Y = 0.05. All test values cited meet this criterion. Results

Figure 5 plots the progression of error elimination during training. As can be seen, the NC procedure equalized the two groups’ performance, with no difference now attributable to the ET/NET variable. The NET animals were slghtly less vigilant in their early, but not late, sessions as indicated by a significant group x session interaction (F(15, 270) = 2.21). An opposite group x session pattern obtained for running time (F(15, 270) = 2.07), with ETs taking slightly longer at first. The vigilance and running time results for training are depicted in Fig. 6. The ET/NET factor once again differentiated the groups’ reactions to CC as indicated by a significant group x session interaction for errors (F(1, 18) = 6.14). As can be seen in Fig. 7, the NET rats appeared to react more strongly than the ET rats. The interaction is lost if the postreward

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FIG. 6. Mean running time (A) and vigilant responses (B) per trial across the 16 training sessions of Experiment 2.

errors of the ET group are added. Total “errors” are then equivalent. Despite the fact that errors were greatly reduced by allowing extra time, the ET rats did display a slight, but clearly significant, CC-induced increase in error commission (t(9) = 3.64) relative to their prechange baseline. Both groups displayed a substantial increase in running time (F( 1, 18) = 31.1) and vigilant behaviors (F(1, 18) = 67.2) when the room was I 1r 10; 0.9 0.8 !

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FIG. 7. Mean errors per trial across the last day of training (session 16) and the first day of contextual change (session 17) of Experiment 2.

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changed (see Fig. 8). The effects of the change were equivalent for the two groups. As in the previous experiment, the CC effect was fleeting. No ET/NET differences were obtained in the seven post-CC sessions for any variable except errors (prereward unbaited arm entries, F(6, 108) = 2.31) which gradually declined for NET animals, but remained relatively stable (low) for ETs. Discussion

This experiment placed a strict contingency against errors. The possibility of a reward was lost if the animals did not proceed directly to the correct arm of the maze. This produced the desired effect of reducing errors. The procedure was so successful as to virtually eliminate any further reduction lent by the addition of the ET option. Thus, conditions were met to test the possibility that highly accurate trained performance protects against CCs. If true, the NC/NET group should have been relatively unaffected by CC. This was not the case. The CCEs they displayed were as extreme as those of their counterparts in Experiment 1. Once again, however, the

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FIG. 8. Mean running time (A) and vigilant responses (B) per trial across the last day of training (session 16) and the first day of contextual change (session 17) of Experiment 7

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ET procedure greatly reduced CCEs. Thus, no parsimonious account of the CCEs obtained in our radial maze can be expressed in terms of memory disruption. GENERAL DISCUSSION That extensive contextual change disrupts memory is beyond doubt. The phenomenon has extensive documentation as well as subjective experience in its behalf. Besides this, the literature contains unique observations (e.g., “cuing” effects, Gordon, McCracken, Dess-Beech, & Mowrer, 1981) that would be quite improbable otherwise. However, small CCs are not only ubiquitous, they are unavoidable. Animals always experience varying degrees of CC upon reexposure to any setting where learning has occurred. Nevertheless, they profit from experience and transfer their training. This contextual variation is especially prevalent in the wild where change is more unremitting. Yet there is every indication that memory remains accessible across these changes. For example, all accounts of foraging behavior (e.g., Pyke, Pulliam, & Chamov, 1977; Stephens & Krebs, 1986) suggest that animals must remember the prey density of the successive patches that they visit, for their persistence in any given patch of food is determined by their experience in other previously visited patches. Efficiency requires that the yield from the current context be compared with others retrieved from memory. Thus, ecological perspectives practically require experience to span CCs of modest magnitude. The present results, at least for the relatively simple maze task used in the present experiments, bore out this expectation. The contextual shift was not entirely uneventful, however. A bout of updating-unbaited arm visits and heightened attention-accompanied the CC. The basis upon which this result can be interpreted as information-gathering and not failed retrieval is its plasticity: forgetting is inflexible, it cannot wait until the correct response is emitted; exploration is more plastic. I suggest that an examination of a wide continuum of contextual change will prove valuable. There is apparently a breakpoint at which cues do become insufficient to support retrieval. This would probably be especially true for laboratory training in which the apparatus itself as well as more distal stimuli underwent drastic modification. However, with lesser changes I suspect that memory is in fact retrieved, that a mismatch between this memory and present conditions is detected, and that the disparity prompts a burst of sampling, not forgetting. Remembering that the application of experience requires, at least in a formal sense of long-standing recognition (Hume, 1777/1975; Russell, 1948), an effort of faith-the invocation of a premise to the effect that the there-and-then applies to the here-andnow-1 suggest that an animal’s only conceivable guide in this inductive

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process is the relative stability of the context in which those expectations apply, sufficient change leading to uncertainty. A small extension of the notion of “occasion-setting” (Holland, 1983; Ross, 1983) seems sufficient to place this activity within modern learning theory. The occasion-setting (OS) function is equivalent to that of instrumental discrimination (Ross & LoLordo, 1987) and is descriptively apt. For example, in serial feature-positive discrimination learning, a stimulus (the OS stimulus) preceding a nominal CS can supply information about (i.e., mark the “occasion”) when that CS is predictive of irregularly delivered reinforcement. This function is readily performed by contextual cues (Bouton & Swartzentruber, 1986). Occasion-setting stimuli apparently convey information about the relations that prevail in a setting without actually taking part in those relations. If contexts specify which relations or contingencies are in force, then it is a very small step-practically a logical necessity-to suppose that exposure to a new context would precipitate the investigative behavior necessary to discover what, if any, changed relations are to be occasioned there. Of course, nongoal visits need not take the highest priority. The present results corroborate the assumption implicit in the experimental design that, when opportunity is afforded, the sites that previously yielded food will be visited first, and then other parts of the maze. There is an informational and biological reason for this: the continued availability of food itself needs confirming, and even a remote prospect of feeding is likely to take priority over other exploratory trips for deprived animals. After that, concerns of safety and the possibility that formerly unbaited sites may now yield food can be addressed. If an obstacle is placed against this sequence of activities, as with conventional training procedures, the order of activities must be reversed, and “errors” committed. An implication of these results is that investigative behavior may not be directed exclusively toward sources of novel stimulation, as classical exploratory theory (Fowler, 1965) suggests. Instead, incidental novelty may precipitate bouts of sampling that explore the possibility of new relations among otherwise familiar stimuli. Objects, places, and cues would not necessarily be examined for their own sensory merits, but for the relations in which they may participate. With this account, the paradoxical effect of drug injection and brain damage on CCEs vanish. These very different manipulations never have been demonstrated to improve memory retrieval, but they do share one characteristic. Each strongly depresses sampling behavior (alcohol: Cox. 1970; Devenport, 1984; Devenport & Hale, in press; Devenport & Merriman, 1983; Maier & Pohorecky, 1986; hippocampal damage: Devenport & Holloway, 1980; Devenport, Hale, & Stidham, 1988; Leaton, 1965; O’Keefe & Nadel, 1978). Thus, to the extent that CCEs consist of sampling

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responses, a straightforward explanation for their elimination by CNS impairment is at hand. Procedural attention in the laboratory to weaker CCs and the sampling behavior they instigate should be useful in marking the boundary between true forgetting and the superficially similar, but profoundly different, outcome of uncertainty. REFERENCES Blanchard, R. J.. Kelly, M. J., & Blanchard. D. C. (1974). Defensive reactions and exploratory behavior in rats. Journal of Comparative and Physiological Psychology, 87, 1129% 1133.

Bouton, M. E., & Belles, R. C. (1979). Contextual control of the extinction of conditioned fear. Learning and Motivation. 10, 445-466. Bouton, M. E., & Swartzentruber, D. (1986). Analysis of the associative and occasionsetting properties of contexts participating in a Pavlovian discrimination. Journal of Experimental

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