Hippocampus and context in classical conditioning

doi:10.1016/S0959-4388(99)80027-0

Current Opinion in Neurobiology

Volume 9, Issue 2, 1 April 1999, Pages 195-202

https://doi.org/10.1016/S0959-4388(99)80027-0 Get rights and content

Abstract

Recent evidence suggests that contextual learning encompasses a variety of changes in learning and performance processes. Only some of these changes depend on the hippocampus. Specialized functions proposed for the hippocampus in contextual learning include the construction and consolidation of contextual memory representations, incidental contextual learning, and inhibitory contextual learning.

Introduction

In a typical classical fear-conditioning experiment, a rat is placed in a conditioning chamber and given one or more tone–shock pairings. As a result, the tone comes to evoke behavioral manifestations of fear, such as freezing. This acquisition of a conditioned response (CR) is used to infer the formation of associations between the tone (conditioned stimulus [CS]) and the shock (unconditioned stimulus [US]). At the same time, there is considerable learning about the context in which those CS–US pairings occurred (e.g. the conditioning chamber.) Many researchers have suggested that this contextual learning may differ from conditioning to explicit CSs in important ways. Most important for the purposes of this review, early evidence suggests that contextual learning may depend on hippocampal activity in a way that conditioning of explicit CSs is not. For example, many investigators 1, 2 have found that hippocampal lesions made after tone–shock conditioning interfere with the display of fear to the context but not to the tone. Indeed, contextual learning has been increasingly used as a convenient assay of hippocampus-dependent behavioral function, and has been used to explore the effects of aging, drugs and genetic variations on hippocampal processing 3•, 4, 5•, 6.

The recent literature, however, suggests a more cautious view. We favor the emerging view that contextual learning encompasses a variety of changes in learning and performance, some of which involve hippocampal processing and others of which do not. The purpose of this review is to integrate recent investigations of hippocampal function in contextual learning with the empirical and theoretical perspectives of behavioral research. First, we describe the common view that hippocampal processing is especially important for the formation of contextual memory representations. Then, we describe various other roles suggested for contextual cues within traditional learning theory and consider the evidence for hippocampal involvement in those roles. These distinctions may be independent of the nature of contextual stimuli themselves, and may thus provide additional insight into hippocampal function in contextual learning. Finally, after briefly presenting some persistent theoretical and methodological issues, we suggest some directions for future research.

Section snippets

Contextual memory representations

Contexts are ill-defined stimuli, comprising many individual features from multiple modalities, each of which might be perceived from several vantage points. Many researchers believe that contextual learning requires the integration of these multiple cues into a unified, configural representation of the context 7, 8, 9. Hippocampal processing may be necessary for the formation of these configural representations, much as it was thought to underlie the formation of spatial memory representations

The role of context in behavior theory

Learning theorists have described several ways in which contextual cues may influence learned behavior: they may become directly associated with the US; they may enter into a more hierarchical relation with explicit cues (e.g. as occasion-setters or retrieval cues); and they may be integrated with explicit stimuli to form context-specific stimulus configurations. Notably, hippocampal processing has been implicated in occasion setting and configural learning 21••, 22, as well as in various

Learning, performance or consolidation?

The behavioral consequences of post-training hippocampal lesions are typically attributed to effects on performance or expression of learning, whereas those of pre-training lesions are attributed to either learning or performance effects. The story may be more complex. First, several studies suggest that the deleterious effects of post-training lesions on conditioned responding to the context are temporally graded (see 1, 15••). Lesions made months after training have little effect on

Conclusions and future directions

Contextual learning is likely to involve a variety of learning and memory processes, some of which depend on the hippocampus and some of which do not. The idea that the hippocampus is critical to the abstraction and consolidation of a configural representation of the context has proved useful for accounting for broad-ranging deficits after hippocampal damage. However, this idea needs to be developed more fully. Despite its success, there have been few systematic attempts to describe the nature

Acknowledgements

Preparation of this article was funded in part by grants from the National Science Foundation (IBN 9727992 to ME Bouton) and the National Institutes of Mental Health (MH53667 to PC Holland).

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

• of special interest
•• of outstanding interest

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Hippocampus and context in classical conditioning

Abstract

Introduction

Section snippets

Contextual memory representations

The role of context in behavior theory

Learning, performance or consolidation?

Conclusions and future directions

Acknowledgements

References and recommended reading

Brain Res

Behav Biol

Neurobiol Learn Mem

Behav Brain Res

Behav Brain Res

Behav Brain Res

Behav Brain Res

Behav Biol

Behav Brain Res

Behav Brain Res

Neurosci Lett

Learn Motiv

Behav Brain Res

Trends Cogn Sci

Neurobiol Learn Mem

Modality-specific retrograde amnesia of fear

Science

Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning

Behav Neurosci

Age-related deficits on the radial maze and in fear conditioning: hippocampal processing and consolidation

Hippocampus

The dorsal hippocampus is essential for context discrimination but not for contextual conditioning

Behav Neurosci

Identification of quantitative trait loci involved in contextual and auditory-cued fear conditioning in BXD recombinant inbred strains

Behav Neurosci

Context and conditioning: a place for space

Physiol Psychol

Factors governing one-trial contextual conditioning

Anim Learn Behav

NMDA processes mediate anterograde amnesia of contextual fear conditioning induced by hippocampal damage: immunization against amnesia by context preexposure

Behav Neurosci

Dissociable effects of selective lesions to hippocampal subsystems on exploratory behavior, contextual learning, and spatial learning

Behav Neurosci

Lesions of the fornix but not the entorhinal or perirhinal cortex interfere with contextual fear conditioning

J Neurosci

Odor-guided fear conditioning in rats: 2. Lesions of the anterior perirhinal cortex disrupt fear conditioned to the explicit conditioned stimulus but not to the training context

Behav Neurosci

Place navigation impaired in rats with hippocampal lesions

Nature

Contingent versus incidental context processing during conditioning: dissociation after excitotoxic hippocampal plus dentate gyrus lesions

Hippocampus

Stimulus configuration, occasion setting, and the hippocampus

Behav Neurosci

Configural association theory and the hippocampal formation: an appraisal and reconfiguration

Hippocampus

A neural network approach to hippocampal function in classical conditioning

Behav Neurosci

Brain mechanisms for changes in processing of conditioned stimuli in Pavlovian conditioning: implications for behavior theory

Anim Learn Behav

A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement

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