Validating neural correlates of familiarity

Familiarity is a pervasive memory phenomenon that occurs in its most basic form when someone recognizes a repeated stimulus without recollecting other aspects of the requisite prior learning episode. Theoretical controversy currently abounds with respect to both the cognitive and neural characteristics of familiarity. Here, we show that the extant data, particularly brain-potential data, are insufficient for validating putative neural correlates of familiarity, and we outline strategies for making progress on this problem. Conceptual priming is an implicit-memory phenomenon that often occurs together with familiarity; experiments that conflate the two phenomena can be misleading. Avoiding this conflation is required to understand familiarity and to determine the extent to which the neurocognitive processes that support priming also drive familiarity.

Introduction

Imagine the ease with which neural substrates of cognition could be dissected if relevant brain processes could be toggled on and off at the mere flip of an experimenter's switch. In reality, much greater effort is required to link patterns of brain activity to elemental units of cognition. Such a challenge in the field of memory research is especially thorny owing to the concurrent emergence during various types of memory testing of multiple expressions of memory (Box 1). These include explicit memory, which entails a conscious memory experience, and implicit memory, which can occur without any awareness of remembering.

The problem of linking brain activity to memory is perhaps most pronounced with respect to one expression of explicit memory known as familiarity. This impression of previous occurrence can be strong, as in déjà vu or butcher-on-the-bus experiences 1, 2. In both cases, we might claim that an object or event is familiar even though we cannot remember specific details regarding a previous encounter. Despite a recent explosion of research on familiarity, many questions remain unanswered about the underlying neurocognitive mechanisms. A controversial stance that strikes at the heart of the distinction between explicit memory and implicit memory is the proposal that the neurocognitive processes that support implicit memory also drive familiarity [3].

Neurophysiological evidence purported to pertain to familiarity has been widely cited for its presumptive relevance not only for understanding familiarity but also for understanding fundamental relationships among various memory phenomena. In particular, many investigators have claimed that FN400 potentials (also known as midfrontal old/new effects; Figure 1a) reflect familiarity (see Ref. [4], and Rugg and Curran[5] in this issue). Here, we argue that implicit memory must be examined more extensively before accepting this claim.

To reach a valid understanding of familiarity, we must actively consider both familiarity and conceptual priming, a type of implicit memory wherein conceptual information cued by a given stimulus is processed differentially as a function of a specific prior experience. Conceptual priming might be operating under typical circumstances of investigations of familiarity, although this possibility has often been underappreciated. In this regard, FN400 potentials might or might not be good markers of familiarity – they might partly or in their entirety reflect co-occurring mnemonic processes that are responsible for conceptual priming effects. Unfortunately, conceptual priming has yet to be extensively investigated in this field.

Here, we outline the literature on familiarity and event-related brain potentials (ERPs), and we describe the sort of evidence needed to adjudicate between the opposing views on the status of FN400 as a putative neural correlate of familiarity. The strategies we advocate hold promise for making progress in this area and also more generally for building neurocognitive explanations for a variety of memory phenomena.