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Event-related potentials and recognition memory

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According to dual-process models, recognition memory is supported by distinct retrieval processes known as familiarity and recollection. Important evidence supporting the dual-process framework has come from studies using event-related brain potentials (ERPs). These studies have identified two topographically distinct ERP correlates of recognition memory –the ‘parietal’ and ‘mid-frontal’ old/new effects – that are dissociated by variables that selectively modulate recollection and familiarity, respectively. We evaluate the extent to which ERP data support dual-process models in light of the proposal that recollection is a continuous rather than a discrete memory process. We also examine the claim that the putative ERP index of familiarity is a reflection of implicit rather than explicit memory. We conclude that ERP findings continue to offer strong support for the dual-process perspective.

Introduction

Recognition memory – the judgment that a stimulus event has been previously experienced – has been a major focus of interest among experimental psychologists and cognitive neuroscientists for more than two decades 1, 2. Among the issues addressed during this period one has stood out: whether recognition memory judgments are supported by one or by multiple kinds of mnemonic information. According to single-process accounts 3, 4, 5, recognition judgments are based on the evaluation of a single type of evidence, and a positive judgment is made when the strength of the evidence exceeds a criterion level. In common with the single-process account, dual-process accounts 6, 7, 8 propose that recognition is supported by an undifferentiated, strength-like form of information (usually referred to in the context of these accounts as familiarity). However, advocates of dual-process accounts argue that recognition relies on a second, functionally distinct, memory signal that results from the retrieval of qualitative information about the study episode. The retrieval of episodic information in response to a recognition test item, which is usually assumed to rely on a subset of the processes that also support recall, is referred to as recollection.

Although the relative merits of single- versus dual-process accounts of recognition continue to be debated, especially in the experimental psychology literature, it is probably fair to say that the majority of contemporary researchers adhere to some kind of dual-process model, although the details of the different models differ markedly 6, 7, 9, 10, 11. Most of these researchers would ascribe to the notion that familiarity-based recognition is fast-acting, relatively automatic and does not provide qualitative information about the study episode (see Box 1 for differing perspectives). Recollection, by contrast, is conceived as a slower, more effortful process that gives rise to consciously accessible information about both the prior occurrence of the test item and the context of that occurrence. Thus, recollection is often operationally defined as recognition accompanied by accurate source memory – memory for a specific feature of the study context, such as the location or color of an item. Another popular, albeit controversial 3, 11, method for segregating recollection- and familiarity-driven recognition relies on the ‘remember/know’ procedure, which requires the subject to report whether recognition is accompanied by specific details of the study episode [12].

The broad acceptance of dual-process models stems not only from the findings of psychological experiments, some of which are still the subject of vigorous debate (e.g. 13, 14). Dual process models are also favored because converging evidence suggests that recollection and familiarity can be dissociated at the neural level. This evidence includes investigations of patients with lesions thought to be restricted to the hippocampus 15, 16 (see Refs 17, 18 for opposing evidence), differential patterns of neural activity revealed by functional magnetic resonance imaging (fMRI) (e.g. Refs 19, 20, 21), and dissociations among retrieval-related event-related potential (ERP) effects. In this article, we briefly review the reasons why ERP findings are thought to support the dual-process perspective. We go on to consider how well these findings fare in the face of recent proposals that, one, recollection, in common with familiarity, is supported by a continuous rather than a discontinuous memory signal, and, two, a putative ERP correlate of familiarity has been mischaracterized and is in fact an index of implicit memory.

Section snippets

ERP correlates of recollection and familiarity

It is more than 25 years since the first reports that ERPs elicited by correctly classified old (studied) items are more positive-going than those elicited by correctly classified new (unstudied) test items 22, 23. It is these ERP ‘old/new effects’ that are the subject of this article. We focus here on studies conducted since the mid-1990s that have employed manipulations aimed at separating the ERP effects according to whether recognition was accompanied by recollection or was based on

Recollection as a continuous process

The relationship between familiarity, recollection and confidence is a hotly debated topic that might be informed by ERP studies. According to Yonelinas and colleagues 1, 6, 42, recollection is best conceptualized as representing a discrete, thresholded mnemonic state (that is, recollection is in some sense all or none’), whereas others have suggested that both familiarity and recollection are continuously varying memory signals that are combined before a recognition judgment is made [11]. From

The midfrontal effect and conceptual priming

The proposal that the mid-frontal effect is a neural correlate of familiarity has recently been challenged. An hypothesis has been advanced that the effect is linked to a form of implicit memory known as conceptual priming 24, 37, 43. Conceptual priming refers to a form of repetition priming that depends on repeated access to semantic, rather than perceptual, representations [37]. According to Paller and colleagues [37], most of the experimental manipulations used to isolate or modulate the

Functional significance of old/new effects

The evidence linking the mid-frontal and parietal old/new effects to familiarity and recollection is arguably strong; however, the cognitive operations reflected by these effects remain to be identified. In the case of the mid-frontal effect, there are grounds for thinking that the effect does not reflect familiarity directly. Tsivilis et al.[50] had subjects study visual objects superimposed upon background scenes. During the test, old and new objects were superimposed either on studied or

Neural generators of the mid-frontal and parietal old/new effects

Single-neuron studies in non-human primates and human fMRI studies have identified putative familiarity-sensitive neuronal populations in the perirhinal region of the medial temporal lobe 58, 59. However, the onset latency of these neuronal responses is of the order of 90 ms [59], which is considerably earlier than the onset of the mid-frontal ERP effect. Familiarity-sensitive neuronal responses have also been identified in the monkey in a variety of prefrontal regions [60], with onset latencies

Concluding comments

ERP studies of recognition memory provided some of the first evidence that recollection and familiarity have qualitatively distinct neural correlates. More recent ERP findings have added to this evidence and to the general weight of the evidence supporting dual-process models of recognition memory. Among the challenges for the future (Box 3) are the elucidation of the cognitive operations reflected by these ERP effects and the identification of their neural generators.

Acknowledgements

Research described in this article was supported by National Institutes of Health grants MH072966 (M.D.R.) and MH64812 (T.C.).

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