Doi:10.1016/j.neubiorev.2004.09.00

Neuroscience and Biobehavioral Reviews 28 (2004) 663–674 Memory processes in classical conditioning Department of Psychology, University of Vermont, Burlington, VT 05405, USA Classical conditioning provides a rich and powerful method for studying basic learning, memory, and emotion processes in animals.
However, it is important to recognize that an animal’s performance in a conditioning experiment provides only an indirect indication of whatit has learned. Various remembering and forgetting processes, in addition to other psychological processes, may intervene and complicatewhat investigators can infer about learning from performance. This article reviews the role of context, interference, and retrieval in a numberof classical conditioning phenomena (e.g. extinction), and provides an overview of how long-term and short-term memory processesinfluence behavior as it is studied in classical conditioning.
q 2004 Elsevier Ltd. All rights reserved.
Keywords: Learning vs. performance; Context; Extinction; Short-term memory; Long-term memory 1. Extinction, context, and interference . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 664 2. Long-term memory processes in animal conditioning and learning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 665 3. Short-term memory processes in conditioning . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 668 4. Conditioned stimuli as retrieval cues . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 669 5. Summary and conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 670 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 671 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 671 Classical conditioning in animals provides a powerful Given proper control groups for alternative nonassociative tool for studying the biological processes underlying processes such as sensitization and pseudoconditioning, the learning, memory, and emotion. In conditioning, once evocation of the CR is a reasonably good index of learning.
a conditional stimulus (CS) is associated with an uncondi- But it is important to realize that what an animal does in a tional stimulus (US), a constellation of conditioned conditioning experiment is not the same as what it knows.
responses (CRs) comes to be elicited by the CS.
Researchers in behavioral aspects of learning and memoryhave long separated learning, the hypothetical psychologi-cal and physical changes in the brain, from performance, * Corresponding author. Tel.: C1 802 656 4164; fax: C1 802 656 8783.
the manifestation of that change in behavior. The present E-mail addresses: mark.bouton@uvm.edu (M.E. Bouton), mbouton@ article selectively reviews the kinds of memory processes 0149-7634/$ - see front matter q 2004 Elsevier Ltd. All rights reserved.
doi:10.1016/j.neubiorev.2004.09.001 M.E. Bouton, E.W. Moody / Neuroscience and Biobehavioral Reviews 28 (2004) 663–674 that separate learning and performance, and thus compli- presenting CS without the US on a number of trials cate simple inferences about psychological processes eliminates (‘extinguishes’) that responding. The study of (learning, memory, emotion) from behavior.
extinction is interesting in its own right, because something The distinction between learning and performance was like it must be available to animals in order to allow them to an important part of the thinking of early learning theorists.
update and modify their behavior in a changing environ- For instance, Edward Tolman, one of the most important ment. In addition, it has been explicitly linked to various theorists of the 20th century, made a convincing case for it.
therapies designed to eliminate unwanted cognitions, For example, in the well-known latent learning experiment, emotions, and behaviors that themselves depend on learning Tolman and Honzik allowed rats to explore a 14-unit It is tempting to suppose that the loss of responding in T-maze on a series of trials. One group received reward each extinction merely reflects the destruction of the original time it reached the end of the maze, whereas another group learning that led to it. But we know this is not the case; the did not. Not surprisingly, the rewarded group moved original association is retained, perhaps fully intact. The through the maze more efficiently, making fewer errors extinction phenomenon is therefore another place where it is (entering fewer dead ends) over the first 11 trials. But when important to understand the distinction between learning the non-rewarded group was then rewarded, they began to (what the animal knows) and performance (what the animal move efficiently through the maze beginning on the next trial. According to Tolman and Honzik, the nonrewarded There are several ways to show that the original group had been learning about the maze the whole time, association is intact after extinction. First, there is even though that learning or knowledge had not been ‘reinstatement.’ In reinstatement, if the US is now presented evident in their behavior. The function of reward was not to a few times after extinction is complete, responding will stamp behavior in, but instead to motivate the animal to return to the CS when the CS is presented again One of perform. A motivational function of reward was widely the main reasons reinstatement occurs is that the animal accepted in subsequent theory . Learning is not the associates the US with the context (background stimuli same as performance. Motivation is required for the typically defined as emanating from the box in which the experiment is conducted) when the US is presented after Modern thinking has followed another of Tolman’s extinction. When the animal is subsequently tested with the ideas. He argued, at a time when it was not fashionable to do CS in the context, the contextual conditioning triggers so, that learning was not the simple attachment of a responding to the CS. One of the most important types of behavioral response to an environmental stimulus (so-called evidence supporting this view is that the US must be S-R learning). Instead, the animal represented its experience presented in the context in which the CS will be tested. If the in some sort of cognitive way. For instance, Tolman animal is presented with the US in an irrelevant context, it claimed that rats learned cognitive maps of the environment.
does not produce reinstatement Although the Although the idea that animals learn a literal map is contextual conditioning that causes reinstatement is not debatable, the cognitive view of what is learned in classical always evident in behavior directly elicited by the context, conditioning has become dominant This view assumes the strength of reinstatement correlates with the strength of that there is a distinction between what is learned and what contextual conditioning when it is measured with sensitive is manifest in behavior. For example, theorists now suppose context-preference tests . Reinstatement indicates that learning involves some sort of encoding of information, that extinction is not the same as unlearning. Responding to storage of that information in memory, and then the retrieval the extinguished CS can return depending on what the of it. Learning processes thus involve the encoding and storage of information. Performance, on the other hand, A second phenomenon indicating that extinction is not depends at least in part on successful retrieval. The current unlearning, and that the CS has become dependent on the article is mainly interested in considering how memory and context, is the ‘renewal effect’ In renewal, an memory retrieval processes operate in classical condition- animal might receive conditioning trials with the CS in one ing. An appreciation of these processes is essential for a context (Context A) and then extinction trials in another complete understanding of this deceptively simple learning (Context B). When the animal is then returned to the process. They are methodologically important because they original context and presented with the CS, responding to introduce a layer of complexity when inferring an animal’s the CS recovers (is ‘renewed’). Although most studies of learning or knowledge from behavior or performance.
renewal have used the ABA design (in which conditioning,extinction, and testing are conducted in Contexts A, B, andA, respectively), other work indicates that renewal can also occur if the contexts are ABC or even AAB Suchresults suggest that extinction is especially dependent on the Consider extinction, a learning phenomenon that has context. It would be a mistake to think, based on the been investigated in our laboratory for many years. Just as a animal’s lack of responding in the extinction context, that CS–US pairing comes to evoke responding, subsequently M.E. Bouton, E.W. Moody / Neuroscience and Biobehavioral Reviews 28 (2004) 663–674 One of the interesting things about research on the words. (The word ‘fire’ can mean different things, and evoke renewal effect is that it suggests that extinction depends different behaviors, depending on whether it is shouted in more on the context than conditioning does. Although it the movie theater or the shooting gallery.) Interestingly, seems relatively easy to find that extinction performance is occasion setters are not generally assumed to elicit lost after a context switch, conditioning performance is performance by themselves, as ordinary CSs might; rarely lost when the CS is switched to a familiar context, instead, they mainly operate by modulating performance which would minimize possible external inhibition effects created by novel contexts used in some experiments The occasion setting mechanism is similar to another . A change of context after conditioning does not possible role of context, namely, to enable retrieval of the attenuate conditioned fear to a CS as measured by CS’s association with the US. As mentioned above, when the animal is outside the extinction context, it might fail to appetitive conditioning or taste aversion condition- retrieve extinction, which can be taken as a CS–no US ing The fact that extinction is more context- association Consistent with this view, retrieval cues dependent than conditioning is consistent with the idea that that remind the animal of extinction can abolish the renewal the animal codes extinction as a kind of conditional exception to the rule—one that depends on the current this view, the context and memory retrieval processes are context When the context is changed, extinction necessary in the translation of knowledge into performance performance disappears and conditioning performance A growing literature on the brain processes involved in A related recovery-after-extinction phenomenon is extinction is broadly consistent with the behavioral research ‘spontaneous recovery’. In this phenomenon, if the just summarized (see for one review). For instance, experimenter merely allows time to pass after extinction, extinction appears to be linked to new brain plasticity the extinguished response can recover . Just as extinction is more sensitive to context than conditioning, voltage-gated calcium channels in the shorter term .
so it is more sensitive to the effects of the passage of time.
One implication is that facilitation of these synaptic In fact, we have argued that the passage of time affects processes should help facilitate extinction, which has been extinction precisely because it is a kind of context Just shown with administration of an NMDA partial agonist, as the renewal effect indicates that extinction is sensitive to D-cycloserine It is not known whether facilitated the physical context, spontaneous recovery suggests that it extinction results from deeper extinction learning that is less is sensitive to the context provided by time.
context-dependent or merely learning that is easier to Research thus clearly indicates that the current perform- retrieve in the right context. At the systems level, fear ance elicited by a CS can underestimate what the animal extinction may be linked in part to activity in the infralimbic actually ‘knows’ about the CS. The major factor that region of the medial prefrontal cortex or to influences performance after extinction—besides the latent possible GABAergic interneurons in the lateral amygdala CS–US association—appears to be the current context. How A role for hippocampus, an area long thought to be does the context operate? Conditioning theorists have had involved in context learning is also suggested by data much to say about this. First, several influential conditioning indicating that the ABC renewal effect is suppressed by models assume that the context enters into direct associ- inactivation of the hippocampus although the ABA ations with the US, just as a CS might . These renewal effect is not affected by lesions . The pattern context-US associations would be expected to summate may be consistent with the idea that negative occasion with the CS–US association to generate performance.
setting by Context B, which is presumably a major source of Unfortunately, an emphasis on this idea cannot explain the ABC effect, is especially dependent on the hippocampus details of the results just reviewed . For example, it is . Reinstatement, which depends on direct associations not consistent with the fact that an extinguished CS is between the context and the US, also depends on an intact especially sensitive to context-US associations and hippocampal system in fear conditioning , though measurable context-US associations do not seem to be not in appetitive conditioning The various brain processes are likely to contribute in different ways to the A second possibility is that the contexts have the acquisition of new learning in extinction and its suppression properties of ‘occasion setters’ (see for reviews). On this view, the context is not merely associatedwith the CS (or the absence of the CS), but instead selects oractivates the CS’s own current association with the US 2. Long-term memory processes in animal conditioning Thus, the extinction context activates something like the animal’s CS–no US association It is as if the contextdetermines the current meaning of the ambiguous CS, much It is interesting to note that the extensive literature on as verbal contexts disambiguate the meaning of ambiguous long-term memory in animals also reinforces the view that it M.E. Bouton, E.W. Moody / Neuroscience and Biobehavioral Reviews 28 (2004) 663–674 is important to distinguish between learning and perform- It is worth observing that the weakness of the context ance. The word ‘forgetting’ describes a behavioral switch effect in humans has a parallel in the animal research.
phenomenon in which performance assessed at Time 2 is As we noted above, a change of context after simple shown to be inferior to that shown at Time 1, typically the excitatory conditioning usually produces little effect on time when the task is originally learned. Although it is responding to the CS . This sort of result can perhaps tempting to assume that the behavioral phenomenon is be seen as a case of outshining: The animal is responding to explained by the decay or erosion of the original memory a highly salient cue for the US (the CS) that overcomes the trace, we know that this often is not true. For example, it is absence of contextual support in the changed context.
often possible to reverse forgetting (and apparently recover Conditioning theories essentially argue that the CS is a more a forgotten memory) by exposing the animal to a retrieval informative cue than the context Other experiments in cue This sort of result has been taken to mean that which context switches have been said to impair memory forgetting often results from an inability to access or retrieve retrieval often have not included an overt CS; for example, the target trace (see for some of the relevant investigators may test passive avoidance , in which the animal refrains from entering a compartment where it Research on remembering and forgetting is often had previously been shocked, and thus responds directly to consistent with Tulving’s Encoding Specificity Principle, contextual (apparatus) cues. With few cues that can which emphasizes the importance of the similarity between potentially outshine them, it may not be surprising to see background contextual cues present during learning and an effect of switching the apparatus. Interestingly, in many testing . The general idea, which has been implicitly cases an extant context switch effect can still be attenuated if accepted in the extinction research presented above, is that the animal is given an extra retrieval cue —a retrieval depends on a match between the conditions present potential parallel to mental reinstatement in humans. The during learning and the conditions present during testing. In parallel between the animal and human literatures is even the original research with human participants, the specificity stronger than this. The fact that the context is especially was defined by subtle semantic shadings of target, to-be- important after extinction is consistent with other parts of remembered words. Tulving and Thomson showed that the human memory literature, which indicate that context the memory for words on a list was affected by weakly- switch effects are similarly easier to detect in interference associated words that were present at input, which designs in which the participant learns a conflicting word apparently influenced the semantic meaning encoded for list in a second phase . Apparently analogous to the target. Their experiments dramatically showed that these extinction, the second word list produces context-specific weakly-associated input words were better able to retrieve interference with memory for the first.
the target words than were more strongly-associated words One important implication of this work, of course, is that that were not present at input. Even though the presence of forgetting is not necessarily due to the erasure of the learned the strongly-associated words at the test almost certainly information. Instead, forgetting may be the result of a generated the target word through free association, the retrieval failure caused by a change of context .
target words were not recognized. Although the initial work Forgetting might also be caused by interference emanating manipulated input cues that could profoundly affect the from conflicting information learned at an earlier or later meaning of target words, subsequent work has shown that point. Interference has a long and distinguished history memory depends on a variety of contextual stimuli, in human learning theory When first-learned information interferes with memory for second-learned Consistent with this idea, memory for verbal material in information, we have ‘proactive interference.’ When humans is often inferior when the room is switched second-learned information interferes with first-learned between learning and testing However, it is often information, we have ‘retroactive interference’. In the disappointingly difficult to detect this effect In a domain of animal learning, retroactive interference is recent meta-analysis, Smith and Vela found overall represented by several possible paradigms, including evidence of such context-dependent memory, but extinction or counterconditioning (where Phase 2 interferes suggested that it is sometimes difficult to find owing to a with Phase 1). Proactive interference is perhaps represented number of other processes that can help support recall at by phenomena like latent inhibition, in which initial the time of the test. For example, ‘outshining’ refers to the exposure to the CS without the US can interfere with idea that if other cues besides the context can support conditioning when the CS and US are subsequently paired.
memory retrieval, and if they are present in both the Interestingly, it has been common in the animal learning training and testing context, then they will diminish any tradition to assume that proactive and retroactive inter- context switch effect. Contexts that are not particularly ference effects occur because of a failure at the level of salient also would not support a context switch effect. And learning. As we have already seen, extinction is sometimes humans can also defeat a context switch effect by thinking thought to result from a destruction of the original learning.
about (mentally reinstating) the original context when they Similarly, latent inhibition is often attributed to a failure to learn during the second (conditioning) phase owing, for M.E. Bouton, E.W. Moody / Neuroscience and Biobehavioral Reviews 28 (2004) 663–674 example, to the habituation of attention to the CS , and deprivation state Mood effects have been Nonetheless, extinction and latent inhibition may both reported in humans, but, perhaps as we have seen with follow from performance processes Consistent with exteroceptive context effects they can be influenced by this idea, these and other proactive and retroactive a number of other factors that make their effects small and interference phenomena are dependent on context (e.g.
difficult to demonstrate . In animals, there is evidence renewal effects have been obtained in both domains) and that stress hormones that could be correlates of emotion can time (e.g. spontaneous recovery effects have been reported play the role of context in a renewal design. Specifically, in both domains) (see for a review). For example, in Ahlers and Richardson showed that administration of latent inhibition, if Phase 2 conditioning is assessed after a ACTH after passive avoidance extinction renewed avoid- delay in the latent inhibition paradigm, the conditioned ance behavior. The idea that ACTH provided a context is response becomes stronger, as if conditioning had been consistent with the fact that dexamethasone (which learned but performance was obstructed by a memory of suppresses ACTH production) delivered during condition- latent inhibition, which was forgotten over the delay ing nullified this effect; ACTH needs to be part of the . In addition, if preexposure and conditioning are conditioning context to recover behavior after extinction.
conducted in different contexts, a return to the preexposure We have argued that the passage of time itself provides a context after conditioning is complete can renew latent gradually changing context discussed above, inhibition performance . Once again, it would be a spontaneous recovery can be understood this way .
mistake to assume that the performance evident at a Certain forgetting phenomena have been suggested as particular point in time is a simple product of the CS’s posing a challenge for this type of view , although the challenge has been addressed and arguably resolved .
Other research supports the idea that memory also Ultimately, it is almost universally held that ‘context’ can be depends on internal contexts provided by drugs . In provided by many kinds of cues and all should ‘state-dependent retention’, memory is inferior when there is a mismatch between interoceptive drug state at the time of Our understanding of what kinds of events reactivate learning and testing. For example, when fear extinction is memories is not complete. As implied above, one of the conducted while the rat is under the influence of a main ideas is that presenting aspects of the original training benzodiazepine (chlordiazepoxide or diazepam), fear is situation is best for reactivating a target memory. Often, an renewed when the animal is subsequently tested in the sober effective cue can be thought of as part of the original state Fear extinction can thus be dependent on the drug context. Thus, the extinction cue in the experiments context. State-dependent retention has important methodo- mentioned earlier worked to retrieve extinction logical implications for studies of the biological basis of because it was coded as part of the extinction context; learning and memory, where it is common to give a drug presentation of even a part of a context can presumably during or soon after training and then test memory in the trigger completion of the entire pattern of the context that it absence of the drug. Although the drug may often be of has been associated with As we will discuss in a later interest because it potentially disrupts a biological con- section, a CS is often thought to evoke behavior because it solidation process, if memory is being tested without a drug retrieves or activates a representation of the US. This that was otherwise present during learning and storage, then implies that the laws of associative learning as developed in retrieval failure is also a candidate explanation for poor research on classical conditioning may be relevant to performance during testing. For example, chemicals that are understanding how retrieval cues are learned and estab- supposed to disable learning and consolidation processes, lished However, the effectiveness of different cues at such as the protein synthesis inhibitor anisomycin and the time of testing might depend further on poorly- several NMDA antagonists (e.g. MK-801, ketamine, understood details about the timing of their presentation phencyclidine, and CGS 19155) can also generate state- with respect to the memory test , the duration of their dependent retention effects under some conditions (aniso- presentation , and what other cues are presented along with them In addition, the effectiveness of means that performance tests in the absence of the chemical different cues may wax and wane as the retention interval might overestimate its impact on learning as opposed to increases The area would benefit from more retrieval. Such a possibility highlights the importance of systematic, theory-driven research on the specific factors using control conditions in which learning is tested in the presence of the same drugged state; if a drug affects learning Another complication is that activation of a forgotten or consolidation when given at the time of conditioning, it memory is not a neutral event, but itself enables further should later affect performance in either the drugged or the learning. For instance, when forgotten memories are reactivated in a new context, the new context becomes Other research suggests that context effects can be effective at retrieving the memory, as if it has been added created by a variety of contextual cues, including hormones to the original training memory . (The word (particularly in non-physiological doses) , time of day ‘reactivation’ is sometimes meant to imply susceptibility M.E. Bouton, E.W. Moody / Neuroscience and Biobehavioral Reviews 28 (2004) 663–674 to further modification.) In addition, events that disrupt themselves, until all the baits have been removed .
memory when they are administered soon after learning can These literatures provide insights into the nature of short- also disrupt memory when they are administered soon after term memory processes in animals. For example, in both reactivation. For example, Misanin et al. found that delayed match-to-sample and the radial maze, animals seem exposure to electroconvulsive shock soon after a reactiva- able to code short-term information either retrospectively tion treatment made the memory difficult to retrieve. Similar (they remember the previous sample or previous arms that evidence has been produced more recently by Nader et al.
have been visited) or prospectively (they remember the who found that introduction of anisomycin likewise correct upcoming comparison stimulus or arms that are abolished a reactivated memory (see also for a related yet to be visited) The implications for studies effect of MK-801). The findings suggest that reactivation of classical conditioning have mainly been discussed in can make a memory susceptible to disruption again, and that studies of occasion setting, where a feature CS informs the similar neurobiological processes are engaged after initial subject of whether or not a subsequent target CS will be learning and reactivation, although they say little about the mechanisms of retrieval itself One danger is to assume There is also evidence that short-term memory processes that the amnestic effect of any agent (e.g. ECS, anisomycin, are important even in simple cases of classical conditioning.
or MK-801) is necessarily to abolish reconsolidation. For Consistent with thinking about human memory processing, example, although the delivery of ECS soon after learning current theory assumes that conditioning requires some was originally thought to abolish consolidation processing of the CS and US together in short-term memory subsequent work suggested that it merely made the memory after individual conditioning trials for the association to be more difficult to retrieve Thus, the trace had been stored in long-term memory. In a classic experiment, encoded after all. We have already seen that anisomycin and Wagner et al. showed that learning of a particular MK-801 might affect retrievability of a memory rather than CS–US relation was damaged in rabbits if a surprising merely disrupting consolidation . The point is that if episode was presented within 300 s after each learning trial.
reactivation treatments initiate new learning, an amnestic The role of short-term memory in conditioning has agent may either interfere with reconsolidation or make figured importantly in the influential theories of Wagner the reconsolidated memory more difficult to retrieve.
The original formulation of his model, which The distinction between learning and performance is paralleled models of human information processing explicitly proposed that storage of the CS–US It is also interesting to note that reactivation treatments association in long-term memory depended on the CS and that involve exposure to a CS operationally resemble US being processed (‘rehearsed’) in short-term memory extinction trials. Typically, however, CS exposures that after each conditioning trial. Importantly, surprising CSs reactivate and engage reconsolidation do not create extinc- and USs—specifically, those that are not already ‘primed,’ tion (the CS improves performance, rather than weakens it, or currently represented in short-term memory, when they compared to control groups that receive no CS). It is possible are presented in a trial—were assumed to command more that extinction learning, which involves the learning of new rehearsal than those that are not surprising. Priming can conflicting information, simply depends on more exposure to occur either through recent presentation of the event itself or the CS. The relationship between these processes is through recent presentation of a retrieval cue associated interesting and important, but poorly understood at present.
with the event (which would retrieve the item from long-term memory and put it into short-term memory).
Furthermore, consistent with an important characteristic of 3. Short-term memory processes in conditioning working memory in humans, the capacity of short-termmemory was assumed to be limited. These ideas and Short-term memory processes have also been important assumptions allowed the model to explain am impressive in studies of animal learning. For example, there is a amount of new data (see for review).
substantial amount of interest in variations of the delayed In a more recent version of the model, Wagner matching to sample procedure, in which animals are given a put the ideas in a connectionist framework. In this sample stimulus at one point in time and then given that model, known as the ‘sometimes opponent process’ model, stimulus and another a few seconds later, when they are or ‘SOP,’ CSs and USs are assumed to have corresponding required to respond to the stimulus that matches the sample ‘nodes’ in memory. The presentation of a CS or US is in order to acquire reinforcement With typical assumed to activate the node. Initially, the node is activated methods, the pigeon’s choice returns to chance when the to a highly active state (‘A1’), but this quickly decays to a interval between the presentation of the sample and then the less active state (‘A2’), where it stays a bit longer before choice stimuli is in the order of many seconds Short returning to the inactive (I) state. (An activated node is term memory for recent choices similarly influences essentially one that is represented in short-term memory.) behavior on the radial maze, where rats choose among The animal learns about the CS only when it has been put a number of baited arms, almost without repeating into its maximally active state (A1). If the US node is M.E. Bouton, E.W. Moody / Neuroscience and Biobehavioral Reviews 28 (2004) 663–674 simultaneously activated to the same A1 state, then the presented on trials that are more spaced in time, there may animal will learn a connection or association between the be a significant increase in conditioned responding on the two. As a consequence of conditioning, the CS is able to spaced trials On the other hand, the increase in activate the US node into the A2 (not the A1) state; this responding does not reach the level in animals that have activation ultimately produces a conditioned response.
received spaced trials throughout training . This Notice that if time were to elapse between presentation result might suggest that massed trials also have an enduring of the CS and US, the CS could decay from A1 to the less- effect on learning, although it is also possible that the active A2 state and therefore be unavailable for learning.
animals trained with massed trials and tested with spaced The theory actually supposes that nodes are composed of ones might not generalize perfectly between trials presented many elements that move from A1 to A2 and then on the two schedules. The evidence suggests that recent Inactivity in a probabilistic fashion. Given these dynamics, presentations of the conditioning events can generate a the theory explains the results of ‘trace conditioning’ short-term suppressive effect on performance and might experiments, in which one observes increasingly poor conditioning as the temporal gap between CS offset and US Of course, priming in short-term memory can only onset increases 1 The US node similarly decays from account for the effects of trial massing within the range of A1 to A2 to Inactivity after each US presentation, although short intertrial intervals. In our appetitive conditioning here the consequences are somewhat different. If the US is experiments in which rats are given pairings of 10- or 30-s in A2 at the time the CS is in A1, an inhibitory CS–US CSs with food pellet USs, priming effects are clearly evident association is learned. This is one account of inhibitory when the trials are separated by 60 s, but not when they are conditioning that can occur in ‘backward conditioning,’ separated by 240 s It is worth noting that when the CS is presented relatively soon after the offset of additional spacing of trials beyond 240 s can have additional positive effects on conditioning This fact implies that The dynamics of short-term memory in SOP can go some additional mechanisms do contribute to trial-spacing effects distance in explaining a number of other interesting effects (see for review). Our own research suggests that long in conditioning. For example, recent work in our own intertrial intervals may create better conditioning because laboratory has investigated the well-known trial-spacing they allow extinction of contextual cues that receive effect, in which trials that are spaced relatively widely in conditioning during CS–US pairings These otherwise time produce better conditioning than trials that are massed compete with (or block conditioning of the CS.
in time Although a number of explanations of Quantitative conditioning models suppose exactly this this effect have been proposed recent research process . SOP gives the process psychological suggests that massing trials closely together in time may flesh by arguing that conditioned contextual cues wouldblock CS conditioning because they activate the US node make conditioning inferior because the presentation of CS to A2, and thus reduce the surprisingness of the US when it and US on one trial primes their representations into short- term memory (the A2 state) and makes them less surprising intertrial intervals weakens the context’s ability to put the on the next trial The results were not consistent To summarize the trial-distribution findings, very short Interestingly, although it is once again tempting to intertrial intervals can hurt conditioning because they prime assume that priming reduces learning, massed training may the CS and US in short-term memory, making them less have its clearest effect on performance. For example, likely to command performance and/or learning on the next presentation of the CS a few seconds before it is presented trial. At longer intertrial intervals, the context becomes less again can reduce responding on the second CS presentation likely to retrieve the representation of the US (and perhaps after conditioning has already occurred . When the CS) and therefore allows better conditioning. Several conditioning occurs in a within-subject procedure that psychological mechanisms thus play a role in trial-spacing intermixes short and long intertrial intervals, there may be effects. But a productive way to conceptualize them is to less responding in the short intertrial intervals a emphasize the influence priming effects in short-term learning deficit caused by the short intervals should be manifest in behavior at all intervals. And when a CS that hasreceived conditioning in a massed-trial procedure is 1 SOP also allows other mechanisms to contribute to the trace conditioning deficit. If the US occurs alone at the end of a very long gap Our discussion to this point has accepted the idea that (‘trace interval’), it could be associated with contextual cues that are present once conditioning has occurred, the CS functions as a at the time Contextual conditioning would reduce any possible retrieval cue that activates a US node or representation. The conditioning of the CS, because it would allow the context to activate idea has received direct empirical support. For example, (prime) the US node to the A2 state, reducing its surprisingness andtherefore causing blocking Rescorla conditioned fear in rats by pairing a light CS M.E. Bouton, E.W. Moody / Neuroscience and Biobehavioral Reviews 28 (2004) 663–674 with a loud noise (created by a klaxon). In a subsequent Also importantly, how the animal currently values the phase, he presented the klaxon repeatedly by itself to representation of the outcome in instrumental learning habituate fear to it. During a third phase, he presented the CS depends upon a subtle process known as ‘incentive alone. At this point, the CS elicited less fear than it did in a control group that did not receive habituation to the noise.
trained rats to lever-press for food pellets while they were Rescorla argued that habituation had modified the rat’s satiated and then tested lever pressing in extinction. At memory representation of the noise; when the CS was then this time, the rats were either hungry or not. Hunger had presented again, it activated a less frightening US represen- no effect on the level of responding. But if the rats had tation. Other experiments revealed a corresponding inflation been given a separate opportunity to eat the pellets while effect rats that received fear conditioning with a they were hungry, hunger strongly increased responding in weak-intensity shock US showed augmented fear of the CS the extinction test. The animal needed to learn about the if they were then exposed to more intense shocks. The effect of food on hunger. Hunger thus motivates behavior argument is thus that the response evoked by a CS depends in a subtle way; the organism will perform an action while in part on the status of the animal’s US representation. A CS hungry if the behavior has been associated with a may generate behavior at least in part because it serves as a particular reinforcer, and if the reinforcer has been retrieval cue for that representation.
associated with something like amelioration of the hunger These findings have been extended in a number of ways.
For instance, Holland has presented striking evidence The evidence thus suggests that animals form relatively that the rat forms a rich representation of the US, and that rich representations as a result of conditioning. One effect of responding to the CS depends on the status of that a CS is to retrieve a representation of the US. Consistent representation. In the basic experiment, rats receive pairings with this, conditioned responding (or performance) is a of different tone CSs with differently-flavored sucrose product of the animal’s knowledge of a CS–US or response- solutions. When one of these is then separately paired reinforcer association and how the animal currently values with illness (which creates a conditioned aversion to the the US. The assignment of value, especially in the operant flavor), the rat exhibits less appetitive responding to the situation, involves motivational as well as memory paired tone during final tests. Remarkably, as if the tone processes, which brings us full circle to the ideas of Tolman evoked an almost palpable image of the flavor it was that we mentioned at the start of this article.
associated with, rats reacted to novel combinations of tonesin a way that paralleled what they had separately learnedabout the corresponding combinations of flavors. In addition, the effect of taste-aversion revaluation of the USappears to be less noticeable when conditioning involves a This short review has only scratched the surface of the more extended number of CS–US pairings, as if conditioned complexity of classical conditioning. In addition to responding becomes more ‘automatic,’ rather than rep- describing some of the many roles for memory in resentation-mediated, with extended exposure to the conditioning, we have repeatedly noted that any study of conditioning must always distinguish learning from per- Related findings have been reported in operant con- formance. We have seen that extinction does not depend on ditioning, where animals learn to associate a behavior (such unlearning; erased performance at the end of extinction does as lever pressing) with a reinforcer instead of a CS with a not reflect erased knowledge. Instead, performance after US. In this case, there is a similar literature indicating that extinction is a product of the animal’s knowledge of two the animal associates one event (the response) with a conflicting associations, and how the context selects representation of the outcome. In a simple experiment, if a between them. Similarly, forgetting in studies of long- rat is trained to lever-press for a food pellet, separate term memory does not necessarily result from erasure or pairings of the pellet and illness will condition an aversion decay, but instead often results from reduced access, either to the pellet—and will also cause the rat to suppress its due to retrieval failure or interference. Once again, the performance of the operant when it is tested in extinction context plays a role. Short-term memory effects are also As in classical conditioning, the current amount evident in classical conditioning; in this case, recent of responding depends on the strength of a hypothetical presentations of events can temporarily suppress perform- association and the extent to which the animal currently ance and learning. Finally, the idea that a CS functions as a values the outcome. Interestingly, extended training in retrieval cue provides another link between conditioning which the rat has many response-outcome pairings can and memory, as well as a further separation between what decrease the sensitivity of the response to the devaluation Although we have focused primarily on memory behavior has become ‘automatized,’ i.e. more habit-like and processes, a number of other factors also matter in the less dependent on the current status of the representation of translation of learning into performance. We have barely mentioned motivational factors (see for one recent M.E. Bouton, E.W. Moody / Neuroscience and Biobehavioral Reviews 28 (2004) 663–674 review). In addition, the qualitative nature of the CS can [12] Bouton ME, Bolles RC. Role of conditioned contextual stimuli in influence the type of conditioned response one observes reinstatement of extinguished fear. J Exp Psychol Anim BehavProcess 1979;5:368–78.
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