Review
The form and function of hippocampal context representations

https://doi.org/10.1016/j.neubiorev.2014.01.005Get rights and content

Highlights

  • Contextual information plays a critical role in memory.

  • Contexts are represented by coherent ensembles of hippocampal neurons.

  • Activity in these ensembles primes the retrieval of context appropriate memories.

  • Priming the relevant memories prevents interference by other, irrelevant memories.

Abstract

Context is an essential component of learning and memory processes, and the hippocampus is critical for encoding contextual information. However, connecting hippocampal physiology with its role in context and memory has only recently become possible. It is now clear that contexts are represented by coherent ensembles of hippocampal neurons and new optogenetic stimulation studies indicate that activity in these ensembles can trigger the retrieval of context appropriate memories. We interpret these findings in the light of recent evidence that the hippocampus is critically involved in using contextual information to prevent interference, and propose a theoretical framework for understanding contextual influence on memory retrieval. When a new context is encountered, a unique hippocampal ensemble is recruited to represent it. Memories for events that occur in the context become associated with the hippocampal representation. Revisiting the context causes the hippocampal context code to be re-expressed and the relevant memories are primed. As a result, retrieval of appropriate memories is enhanced and interference from memories belonging to other contexts is minimized.

Introduction

The context plays an undeniably profound role in memory. Learned information is bound to the learning context, and the context can be a remarkably potent retrieval cue (Smith, 1988). Anyone who has returned to their childhood neighborhood after decades away can attest to the striking experience of long lost memories that come flooding back in vivid detail. Empirical studies of contextual cueing of memory have a long history in psychology. Items learned in one context are better recalled when testing takes place in the same context (Godden and Baddely, 1975). The context can also serve as a disambiguating cue that allows subjects to retrieve information associated with one context without interference from items learned in other contexts. For example, subjects who learn two lists of items in distinct contexts exhibit better recall than those who learn both lists in the same context (for review see Smith, 1988). In fact, the association between context and memory is so strong that simply asking subjects to think about the learning environment is sufficient to improve recall (Smith, 1979).

The hippocampus has been known to be involved in processing contextual information since the 1970s (Hirsh, 1974). In the decades since, several theories of hippocampal context coding have been proposed. Several authors have noted the similarity between spatial mapping functions of the hippocampus and representations of the environmental context (Mizumori, 2007, Nadel et al., 1985). Another theory holds that the hippocampus binds the various components of the context into a complex multimodal configural cue (Sutherland and Rudy, 1989). Yet another theory suggests that context representations are a natural consequence of the relational memory encoding functions of the hippocampus (Cohen and Eichenbaum, 1994). Despite these theoretical accounts, detailed knowledge about the form of these hippocampal context representations has only recently become available, with the advent of large scale neuronal population recording and ensemble stimulation techniques. In this article, we review new findings about the nature of hippocampal context representations and present evidence that each context a subject encounters is encoded by a unique ensemble of hippocampal neurons. With experience, these hippocampal ensemble context codes become associated with the memories and behaviors that are appropriate for that context. When subjects revisit a familiar context, the hippocampal context code is automatically re-expressed, thereby priming the relevant memories and reducing the interference from memories associated with other contexts.

Section snippets

The hippocampus and context

In this article, we focus our discussion on the nature of hippocampal context representations and their functional significance for preventing interference. More general discussion of the hippocampal role in contextual memory can be found in several comprehensive reviews (Eichenbaum et al., 2012, Holland and Bouton, 1999, Lee and Lee, 2013, Maren et al., 2013, Mizumori, 2013, Mizumori et al., 1999, Rudy, 2009). Current ideas about the hippocampal role in context coding have come primarily from

Hippocampal ensembles represent the context

Recent findings have suggested that each context is encoded by a distinct ensemble of hippocampal neurons. Keleman and Fenton (2010) found that the hippocampus can hold two distinct representations of the same apparatus and alternate between them when they are placed in conflict. Rats were trained in a rotating arena that allowed the experimenters to establish two distinct reference frames, or contexts, defined by unmarked danger zones where shocks were delivered (Fig. 2A). One danger zone was

Direct manipulation of hippocampal ensembles

Although the kinds of ensemble firing patterns described above are correlated with the context and with context appropriate behaviors, the causal links have been uncertain. Do hippocampal ensemble codes drive the retrieval of context appropriate memories as we have suggested? Or does sensory input from the current context drive both the hippocampal representation and context appropriate behavior? Although it is difficult to conclusively establish a direct causal link between neural firing and

The adaptive value of hippocampal context representations: preventing interference

Converging evidence from large scale neuronal recordings, immediate early gene expression and direct manipulation of neural firing suggests that hippocampal neural ensembles represent contextual information. But what is the adaptive value of these context representations? The ability to encode new contexts and recognize familiar ones is important in itself. However, we suggest that the primary utility of context coding is that contextual information provides an important mechanism for

Conclusions and remaining questions

Although many studies have shown a hippocampal role in contextual memory, there has not been a detailed account of the form and function of hippocampal context representations. The evidence reviewed above suggests that the hippocampus encodes contexts that are defined by a variety of environmental, behavioral and motivational factors. These representations take the form of a coherent ensemble code that changes as a whole rather than in a piecemeal fashion. The generation of a new context

Acknowledgements

This work was supported by NIH grant MH083809 to D. Smith. The authors thank Rachel Swanson for her work on the illustrations of Fig. 4.

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