Brain substrates of implicit and explicit memory: the importance of concurrently acquired neural signals of both memory types

Abstract

A comprehensive understanding of human memory requires cognitive and neural descriptions of memory processes along with a conception of how memory processing drives behavioral responses and subjective experiences. One serious challenge to this endeavor is that an individual memory process is typically operative within a mix of other contemporaneous memory processes. This challenge is particularly disquieting in the context of implicit memory, which, unlike explicit memory, transpires without the subject necessarily being aware of memory retrieval. Neural correlates of implicit memory and neural correlates of explicit memory are often investigated in different experiments using very different memory tests and procedures. This strategy poses difficulties for elucidating the interactions between the two types of memory process that may result in explicit remembering, and for determining the extent to which certain neural processing events uniquely contribute to only one type of memory. We review recent studies that have succeeded in separately assessing neural correlates of both implicit memory and explicit memory within the same paradigm using event-related brain potentials (ERPs) and functional magnetic resonance imaging (fMRI), with an emphasis on studies from our laboratory. The strategies we describe provide a methodological framework for achieving valid assessments of memory processing, and the findings support an emerging conceptualization of the distinct neurocognitive events responsible for implicit and explicit memory.

Figure 1. ERP correlates of explicit memory and perceptual implicit memory (Paller et al., 2003)

The ERP difference between remembered faces and new faces is displayed in A. The ERP difference between primed-but-not-remembered faces and new faces is displayed in B. Waveform differences are averaged over 100-ms intervals starting at the latency indicated underneath each topographic map. Each map represents amplitudes on the scalp as viewed from above. Light yellow colors indicate positive difference potentials in A and negative difference potentials in B. ERP waveforms recorded from the midline frontal scalp location referenced to averaged mastoids are shown in C for the three conditions (including only trials with reaction times faster than the median reaction time for each subject and each condition, so as to accentuate effects associated with perceptual priming). (Figure adapted from Paller et al., 2003.)

Figure 2. ERP correlates of conceptual implicit memory and explicit memory (Voss & Paller, 2006)

ERPs in A were recorded during a conceptual priming test. ERPs to famous faces that had also been presented with corresponding conceptual information in an earlier phase of the experiment (conceptual priming) differed from ERPs to famous faces previously presented without corresponding information (no conceptual priming), in the amplitude of FN400 potentials and LPC potentials, as indicated. In both cases ERPs were relatively more positive with conceptual priming. These ERP differences computed over two intervals are shown topographically in B (same format as in Fig. 1). The electrode locations for ERPs in A are marked with stars on the topographic maps. The magnitude of the FN400 difference was correlated across-subjects with the magnitude of conceptual priming indexed behaviorally, as shown in C (left), but it did not correlate significantly with the difference in explicit memory ratings between the two conditions. Conversely, the magnitude of the LPC difference between repeated faces with versus without conceptual priming was correlated with the corresponding difference in explicit memory ratings, as shown in C (right), and was not correlated with the magnitude of conceptual priming.

Figure 3. Disentangling ERP correlates of conceptual implicit memory and familiarity during a recognition test (Voss & Paller, 2007)

Behavioral measures of conceptual priming were exhibited for squiggles that were meaningful, but not those that were meaningless (sample squiggles shown in A; meaningful and meaningless conditions defined based on subjective ratings made by each subject). To identify ERP correlates of conceptual priming during recognition testing, contrasts were made between meaningful and meaningless squiggles that were equated in explicit memory strength. ERPs for both conditions appear in B for the frontal midline electrode indicated by a star on the topographic plot. The FN400 difference between meaningful and meaningless items attributed to conceptual priming is shown topographically in B. In contrast, the magnitude of LPC potentials correlated across-subjects with the accuracy of familiarity-based recognition (d' for “know” responses), as shown in C. These correlations were significant for both meaningful and meaningless items. Thus, FN400 potentials varied as a function of meaningfulness ratings and corresponding ability to support conceptual priming, whereas LPC potentials were associated with familiarity-based recognition irrespective of meaningfulness.