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Recognition memory: What are the roles of the perirhinal cortex and hippocampus?

Abstract

The hallmark of medial temporal lobe amnesia is a loss of episodic memory such that patients fail to remember new events that are set in an autobiographical context (an episode). A further symptom is a loss of recognition memory. The relationship between these two features has recently become contentious. Here, we focus on the central issue in this dispute — the relative contributions of the hippocampus and the perirhinal cortex to recognition memory. A resolution is vital not only for uncovering the neural substrates of these key aspects of memory, but also for understanding the processes disrupted in medial temporal lobe amnesia and the validity of animal models of this syndrome.

Key Points

  • The potential roles of the hippocampus and perirhinal cortex in recognition memory (judgement of prior occurrence) are reviewed in relation to whether the evidence for a dual-process model of recognition memory is sufficient to reject the alternative, unitary model.

  • Recent results from animal recording, immunohistochemical imaging and ablation studies are summarized in relation to this issue, and then considered in relation to findings from human studies.

  • Most results from animal studies favour the view that recognition memory might be subdivided functionally and neuroanatomically within the temporal lobe into two main components:

    (1) One component is a familiarity and recency discrimination system centred on perirhinal cortex. This perirhinal system rapidly processes information about the novelty or prior occurrence of individual stimulus items.

    (2) The second component is a recollective system centred on the hippocampus. This hippocampal system is slower, associational and processes information concerning the prior occurrence of individual stimuli or collections of stimuli in relation to other stimuli, including, more generally, information about the prior occurrence of episodes or events.

  • The implications of such a proposed division in humans are that selective hippocampal damage should impair episodic memory, including recollective and associative aspects of recognition memory, while sparing aspects of recognition memory based on familiarity discrimination of individual items. By contrast, selective lesions of the perirhinal and adjacent cortices should impair familiarity discrimination for individual items, but may leave recollective aspects of recognition memory relatively unimpaired.

  • A review of human imaging and event-related potential (ERP) data indicates potential consistency with such a division, although not all studies support a qualitative as opposed to quantitative distinction. Moreover, this division remains to be clearly established in clinical lesion studies.

  • Critical studies into the neural basis of human and animal amnesia need to be designed and interpreted in the light of the different systems that might be employed to solve recognition memory tasks.

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Figure 1: Multiple routes for sensory information reaching the hippocampus.
Figure 2: Response decrements on stimulus repetition: separable encoding of recency and familiarity information.
Figure 3: The paired-viewing procedure for simultaneously presenting novel and familiar stimuli.

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Acknowledgements

Our work is supported by the MRC, BBSRC and Wellcome Trust. We are grateful to P. Machin and E. Wilding for helpful comments.

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ENCYCLOPEDIA OF LIFE SCIENCES

Amnesia

Learning and Memory

Neural Activity and the development of Brain circuits

Neural Networks and Behaviour

Long-term Potentiation

Glossary

RECOGNITION MEMORY TASKS

Tasks that rely on a judgement of prior occurrence for their solution.

DELAYED-MATCHING-TO-SAMPLE TASKS

In such recognition memory tasks, presentation of a stimulus is followed by a delay, after which a choice is offered. In matching tasks, the originally presented stimulus must be chosen; in non-matching tasks, a new stimulus must be selected. With small stimulus sets, the stimuli are frequently repeated, thus becoming highly familiar. Hence, typically, such tasks are most readily solved by short-term or working memory rather than by long-term memory mechanisms.

'TRIAL UNIQUE' STIMULI

Stimuli that are used on only one trial, or at least very infrequently, in a delayed matching task.

IMMEDIATE EARLY GENES

Immediate early genes control the transcription of other genes, and thereby provide the early stages in the control of the production of specific proteins.

C-FOS

An immediate early gene that is rapidly turned on when many types of neuron increase their activity. It can therefore be used to identify responsive neurons.

POSTRHINAL CORTEX

The region of rat cortex posterior to the perirhinal cortex, thought to be analogous to parts of the parahippocampal gyrus in primates.

CROSSED LESIONS

Unilateral lesions in two different sites in opposite hemispheres. Behavioural impairment following such lesions establishes that the regions are functionally dependent on each other.

EVENT-RELATED POTENTIAL

Neural recordings made on the scalp in which activity changes in populations rather than specific neurons can be temporally linked to an event.

DEPTH OF PROCESSING

As the processing of information moves from perception-based features ('shallow') to semantic features ('deep'), subsequent recall is aided even though priming is little affected.

REMEMBER–KNOW PARADIGM

A subjective decision is made about whether the previous occurrence of a recognized stimulus is linked with the retrieval of the learning episode ('remembered') or whether there is merely a feeling of familiarity ('knowing').

EVENT-RELATED fMRI

Functional magnetic resonance imaging (fMRI) in which it is possible to detect signal changes after single events.

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Brown, M., Aggleton, J. Recognition memory: What are the roles of the perirhinal cortex and hippocampus? . Nat Rev Neurosci 2, 51–61 (2001). https://doi.org/10.1038/35049064

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