Joel L. Voss

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.

Strengthening Individual Memories by Reactivating Them During Sleep

During sleep, memories can be influenced in a specific and systematic manner. While asleep, people heard sounds that had earlier been associated with objects at specific spatial locations. Upon waking, they recalled these locations more accurately than other locations for which no reminder cues were provided. Consolidation thus operates during sleep with high specificity and is subject to systematic influences through simple auditory stimulation.

Targeted enhancement of cortical-hippocampal brain networks and associative memory

Brain stimulation to improve human memory The hippocampus is a crucial brain area for certain types of memory. Working with humans, Wang et al. found that a specific type of non-invasive brain stimulation improved memory tests and enhanced information flow between the hippocampus and a number of other brain regions. This increased connectivity was highly specific for the individual target areas selected for each participant. Science, this issue p. 1054 Noninvasive stimulation of the brain can improve memories for episodes by boosting the connectivity between cortical regions. The influential notion that the hippocampus supports associative memory by interacting with functionally distinct and distributed brain regions has not been directly tested in humans. We therefore used targeted noninvasive electromagnetic stimulation to modulate human cortical-hippocampal networks and tested effects of this manipulation on memory. Multiple-session stimulation increased functional connectivity among distributed cortical-hippocampal network regions and concomitantly improved associative memory performance. These alterations involved localized long-term plasticity because increases were highly selective to the targeted brain regions, and enhancements of connectivity and associative memory persisted for ~24 hours after stimulation. Targeted cortical-hippocampal networks can thus be enhanced noninvasively, demonstrating their role in associative memory.

Fluent Conceptual Processing and Explicit Memory for Faces Are Electrophysiologically Distinct

Implicit memory and explicit memory are fundamentally different manifestations of memory storage in the brain. Yet, conceptual fluency driven by previous experience could theoretically be responsible for both conceptual implicit memory and aspects of explicit memory. For example, contemplating the meaning of a word might serve to speed subsequent processing of that word and also make it seem familiar. We examined electrophysiological correlates of conceptual priming with 180 celebrity faces to determine whether or not they resemble electrophysiological correlates of explicit memory. Celebrity faces are ideal for this purpose because they carry with them preexisting conceptual information (i.e., biographical facts) that can selectively be brought to mind such that conceptual processing can be manipulated systematically. In our experiment, exposure to biographical information associated with only one-half of the celebrities yielded conceptual priming for those faces, whereas all faces were perceptually primed. Conceptual priming was indexed by positive brain potentials over frontal regions from ∼250 to 500 ms. Explicit memory retrieval was associated with later brain potentials over posterior regions that were strikingly similar to potentials previously associated with pure familiarity for faces (when a face seems familiar in the absence of retrieval of any specific information about previous occurrence). Furthermore, the magnitude of conceptual priming was correlated across subjects with the amplitude of frontal but not posterior potentials, whereas the opposite was true for explicit memory. Distinct brain processes were thus associated with conceptual priming and conscious recognition of faces, thus providing a sharper focus on the border between implicit and explicit memory.

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

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.

Hippocampal brain-network coordination during volitional exploratory behavior enhances learning

Exploratory behaviors during learning determine what is studied and when, helping to optimize subsequent memory performance. To elucidate the cognitive and neural determinants of exploratory behaviors, we manipulated the control that human subjects had over the position of a moving window through which they studied objects and their locations. Our behavioral, neuropsychological and neuroimaging data indicate that volitional control benefits memory performance and is linked to a brain network that is centered on the hippocampus. Increases in correlated activity between the hippocampus and other areas were associated with specific aspects of memory, which suggests that volitional control optimizes interactions among specialized neural systems through the hippocampus. Memory is therefore an active process that is intrinsically linked to behavior. Furthermore, brain structures that are typically seen as passive participants in memory encoding (for example, the hippocampus) are actually part of an active network that controls behavior dynamically as it unfolds.

Finding meaning in novel geometric shapes influences electrophysiological correlates of repetition and dissociates perceptual and conceptual priming

Repeatedly viewing an object can engender fluency-related implicit memory for perceptual and conceptual attributes, as indexed in tests of perceptual and conceptual priming, respectively. Stimuli with minimal pre-experimental meaning allow direct comparisons between these two types of priming and explorations of whether corresponding neural mechanisms differ. We therefore examined electrophysiological correlates of perceptual and conceptual priming for minimalist geometric shapes (squiggles). Response time measures of conceptual priming were evident for squiggles rated by individual subjects as most meaningful, but not for those rated least meaningful. Conceptual-priming magnitude was proportional across individuals to the amplitude of FN400 brain potentials, but only for meaningful squiggles. Perceptual priming was evident for squiggles irrespective of meaningfulness, and perceptual-priming magnitude was proportional to the amplitude of frontal P170 potentials. These findings therefore show that a single exposure to a novel stimulus can lead to neural processing accompanying conceptual priming that is distinct from that accompanying perceptual priming (FN400 potentials vs. P170 potentials, respectively). Overall, this evidence is also relevant to the current debate over the neural correlates of familiarity-based recognition, and runs counter to the prominent supposition that familiarity can be generically indexed by FN400 potentials.

Accurate forced-choice recognition without awareness of memory retrieval

Recognition confidence and the explicit awareness of memory retrieval commonly accompany accurate responding in recognition tests. Memory performance in recognition tests is widely assumed to measure explicit memory, but the generality of this assumption is questionable. Indeed, whether recognition in nonhumans is always supported by explicit memory is highly controversial. Here we identified circumstances wherein highly accurate recognition was unaccompanied by hallmark features of explicit memory. When memory for kaleidoscopes was tested using a two-alternative forced-choice recognition test with similar foils, recognition was enhanced by an attentional manipulation at encoding known to degrade explicit memory. Moreover, explicit recognition was most accurate when the awareness of retrieval was absent. These dissociations between accuracy and phenomenological features of explicit memory are consistent with the notion that correct responding resulted from experience-dependent enhancements of perceptual fluency with specific stimuli--the putative mechanism for perceptual priming effects in implicit memory tests. This mechanism may contribute to recognition performance in a variety of frequently-employed testing circumstances. Our results thus argue for a novel view of recognition, in that analyses of its neurocognitive foundations must take into account the potential for both (1) recognition mechanisms allied with implicit memory and (2) recognition mechanisms allied with explicit memory.

More than a feeling: Pervasive influences of memory without awareness of retrieval

The subjective experiences of recollection and familiarity have featured prominently in the search for neurocognitive mechanisms of memory. However, these two explicit expressions of memory, which involve conscious awareness of memory retrieval, are distinct from an entire category of implicit expressions of memory that do not entail such awareness. This review summarizes recent evidence showing that neurocognitive processing related to implicit memory can powerfully influence the behavioral and neural measures typically associated with explicit memory. Although there are striking distinctions between the neurocognitive processing responsible for implicit versus explicit memory, tests designed to measure only explicit memory nonetheless often capture implicit memory processing as well. In particular, the evidence described here suggests that investigations of familiarity memory are prone to the accidental capture of implicit memory processing. These findings have considerable implications for neurocognitive accounts of memory, as they suggest that many neural and behavioral measures often accepted as signals of explicit memory instead reflect the distinct operation of implicit memory mechanisms that are only sometimes related to explicit memory expressions. Proper identification of the explicit and implicit mechanisms for memory is vital to understanding the normal operation of memory, in addition to the disrupted memory capabilities associated with many neurological disorders and mental illnesses. We suggest that future progress requires utilizing neural, behavioral, and subjective evidence to dissociate implicit and explicit memory processing so as to better understand their distinct mechanisms as well as their potential relationships. When searching for the neurocognitive mechanisms of memory, it is important to keep in mind that memory involves more than a feeling.

Conceptual priming and familiarity: Different expressions of memory during recognition testing with distinct neurophysiological correlates

Familiarity and recollection are qualitatively different explicit-memory phenomena evident during recognition testing. Investigations of the neurocognitive substrates of familiarity and recollection, however, have typically disregarded implicit-memory processes likely to be engaged during recognition tests. We reasoned that differential neural responses to old and new items in a recognition test may reflect either explicit or implicit memory. Putative neural correlates of familiarity in prior experiments, for example, may actually reflect contamination by implicit memory. In two experiments, we used obscure words that subjects could not formally define to tease apart electrophysiological correlates of familiarity and one form of implicit memory, conceptual priming. In Experiment 1, conceptual priming was observed for words only if they elicited meaningful associations. In Experiment 2, two distinct neural signals were observed in conjunction with familiarity-based recognition: late posterior potentials for words that both did and did not elicit meaningful associations and FN400 potentials only for the former. Given that symbolic meaning is a prerequisite for conceptual priming, the combined results specifically link late posterior potentials and FN400 potentials with familiarity and conceptual priming, respectively. These findings contradict previous interpretations of FN400 potentials as generic signals of familiarity and show that repeated stimuli in recognition tests can engender facilitated processing of conceptual information in addition to retrieval processing that leads to the awareness of memory retrieval. The different characteristics of the electrical markers of these two types of process further underscore the biological validity of the distinction between implicit memory and explicit memory.