Review
Interleaving brain systems for episodic and recognition memory

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Conflicting models persist over the nature of long-term memory. Crucial issues are whether episodic memory and recognition memory reflect the same underlying processes, and the extent to which various brain structures work as a single unit to support these processes. New findings that have resulted from improved resolution of functional brain imaging, together with recent studies of amnesia and developments in animal testing, reinforce the view that recognition memory comprises at least two independent processes: one recollective and the other using familiarity detection. Only recollective recognition appears to depend on episodic memory. Attempts to map brain areas supporting these two putative components of recognition memory indicate that they depend on separate, but interlinked, structures.

Introduction

There are two related debates about long-term memory. The first concerns the relationship between episodic memory and recognition memory. Some researchers see these components of long-term memory as part of the same continuum 1, 2, 3. Others argue that recognition memory involves two or more qualitatively different processes 4, 5, 6, one of which shares features with episodic memory. The second debate concerns the degree to which structures supporting long-term memory in the medial temporal lobe make qualitatively different contributions 3, 6, 7, 8, 9, 10. Advances in the resolution of functional magnetic brain imaging (fMRI), allied to key developments in the behavioural testing of memory in animals, have helped the debate to reach a consensus on some issues, with unresolved issues becoming more precisely formulated.

First, it is necessary to be clear about terminology. Episodic memory refers to our conscious memory for personal events and experiences occurring at a specific time in a specific place [11]. Recognition memory signals whether an event has previously been experienced. An immediate problem for animal studies is that it is unlikely that episodic memory could ever be demonstrated in animals according to its initial description [11]. This is because episodic retrieval requires active mental time travel: a process that can only be confirmed by introspection [11]. The response has been to develop tests of ‘episodic-like’ memory. Key features of such tests for animals include the simultaneous learning of the ‘what’, ‘where’ and ‘when’ of an event. Such tests were first created for birds [12] but recent tests of episodic-like memory have been devised for rodents 13, 14. The findings from these studies not only increase the likelihood that there are primitive forms of episodic memory in animals, but also provide a platform for future studies into the neural basis of episodic-like memory.

In contrast to episodic memory, testing recognition memory in animals should be straightforward, providing direct comparisons with human data. In fact, the situation is again complex: if human recognition memory comprises two different processes (recollection and familiarity discrimination), do animals only use one of them?

Here, we explore these possible divisions within long-term memory and, on the balance of evidence, support two-process models of recognition that allocate the different processes to separate, but interconnected, brain structures. The starting point is a consideration of anterograde amnesia because this condition should not only reveal those structures necessary for episodic memory, but also whether dissociations between episodic and recognition memory can exist.

Section snippets

Anterograde amnesias: a network for episodic memory?

Anterograde amnesia disrupts memory for new autobiographical information, and so always impairs episodic memory. Damage in one of two key regions, the medial temporal lobe or the medial diencephalon, is most frequently associated with amnesia. (The diencephalon comprises the thalamus and hypothalamus.) In addition, damage in the basal forebrain, the retrosplenial cortex and the prefrontal cortex can result in amnesia or elements of the condition.

Within the temporal lobe, bilateral hippocampal

Assumptions about the nature of recognition memory

Introspection tells us that when we recognize a name or a person, two different subjective experiences can occur. Recognition might solely reflect a feeling of familiarity (‘knowing’) or recognition might be verified by recollecting something about the episode when that name or person was last encountered (‘remembering’). This distinction is captured in two-process models of recognition that regard ‘knowing’ and ‘remembering’ as separate processes that both support recognition memory [5]. A

Evidence for dissociations between episodic and recognition memory

One source of evidence comes from event-related potentials. Two different anatomical populations have been identified that are functionally and temporally dissociable [4]. The first population is indexed by activity over the frontal scalp from 300–500 ms poststimulus, and the attributes of this scalp activity (e.g. insensitivity to levels of processing) make it a likely neural correlate of familiarity [4]. The second population is evident over the parietal scalp from 500–800 ms and might index

The role of the parahippocampal cortex and the neural basis of familiarity-based recognition

Recordings in monkeys performing visual recognition tasks indicate that up to 25% of neurones in the anterior parahippocampal region, centred in the perirhinal cortex, respond strongly to pictures or objects that are new but only weakly when items have been seen previously 6, 50, 51 (Figure 3a). The change is sometimes termed ‘repetition suppression’ but there is no evidence that response reductions rely upon a suppressive or inhibitory process; selective, activity-dependent synaptic weakening

Bringing familiarity and recollection together

In a prescient paper, Warrington and Weiskrantz [71] suggested that inputs to the prefrontal cortex from the mammillary bodies and medial thalamus ensured effective cognitive mediation for optimal encoding (e.g. elaboration, organization, imagery, embellishment), such that their disconnection could contribute to amnesia [71]. To their model, we can add direct prefrontal inputs [72] from the retrosplenial cortex, the anterior and rostral midline thalamic nuclei and the hippocampus (via the

Acknowledgements

The authors wish to thank Ed Wilding, Lorraine Woods and Seralynne Vann for their assistance. I. Nimmo-Smith kindly provided the normative data for Figure 2. Support from the MRC assisted in the development of the ideas in this review.

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