Review
Memory search and the neural representation of context

https://doi.org/10.1016/j.tics.2007.10.010Get rights and content

A challenge for theories of episodic memory is to determine how we focus memory search on a set of recently learned items. Cognitive theories suggest that the recall of an item representation is driven by an internally maintained context representation that integrates incoming information with a long time-scale. Neural investigations have shown that recalling an item revives the pattern of brain activity present during its study. To link these neural and cognitive approaches, we propose a framework in which context is maintained and updated in prefrontal cortex, and is associated with item information through hippocampal projections. The proposed framework is broadly consistent with neurobiological studies of temporal integration and with studies of memory deficits in individuals with prefrontal damage.

Introduction

An attempt at reminiscence can comb recent moments or revive episodes long past, sometimes producing a flood of detail, and other times a mere impression of familiarity. Here, we review the behavioral investigations, computational modeling and neuroimaging studies of memory search for recently learned items, and the insights these investigations give us for cognitive processing in general. Most of the theoretical development in this area has arisen from laboratory-based investigations of human behavior during memory search and the use of these data to construct computational models of human memory. These models suggest that slowly changing representations in the cognitive system can be used to sweep the past for desired representations. These internal context representations enable the individual to probe memory in tasks such as free recall, in which a list of words (or other items) is studied and the individual is later asked to recall as many items as possible, in any order. In this view, context representations have the role of an internal stimulus associated with each of the items to be remembered, and the manipulation of the context representation enables us to flexibly search memory for behaviorally relevant information. Recently, neural investigations have started to characterize the patterns of brain activity associated with the retrieval of information during memory search. We suggest that the above-mentioned cognitive theories will have a crucial role in interpreting the significance of these neural signals, and might provide a framework enabling detection of the neural correlates of these hypothesized context representations.

Section snippets

Episode and context – a cognitive perspective

The human memory system can do more than simply recognize that a particular item was encountered. Its flexibility arises from its ability to determine when, and in what context, a particular memory occurred. Thus, a primary responsibility of the memory system during learning is to bind together elements of a stimulus representation with co-active contextual features, such that during later memory search the individual can infer much about the circumstances of a prior observation of an item by

The reactivation of neural representations during memory search

To recall an experienced item, some component of the pattern of cortical activity that accompanied its original presentation must be revived. Several neurorecording studies have shown reactivation of cortical patterns of activity during memory search 13, 14, 15, 16, 17, 18, 19, 20. The majority of these studies use recognition and cued-recall paradigms. In these paradigms, participants are shown a series of words, each of which is paired with a stimulus chosen from two distinct modalities (such

Neural integration, active maintenance and temporal context

As reviewed here, a neural representation of temporal context must integrate information across time. Recently, research teams have identified mechanisms of neural integration at several time-scales and in several neural systems, ranging from the goldfish oculomotor system to monkey parietal cortex 29, 30, 31, 32, 33. However, many of these systems integrate in the millisecond-to-second range, whereas a system with a slower time-course is needed to give rise to the behavioral findings outlined

Concluding remarks

Recent developments in computational models of episodic memory and the cognitive neuroscience of human memory retrieval suggest that a unification of cognitive and neural memory theory is on the horizon (Box 3). Neuroimaging researchers are developing ever more sensitive techniques for probing the state of the neural system,while computational models of episodic memory are converging on the importance of context in guiding self-initiated retrieval of episodic memory. As highlighted in this

Acknowledgements

This work was supported by the National Institutes of Health grants MH055687, MH062196, MH078513, and National Science Foundation grant SBE0354378. We thank M. Howard, P. Sederberg and C. Weidemann for helpful comments on the manuscript.

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