Heather D. Lucas

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.

Why Some Faces won't be Remembered: Brain Potentials Illuminate Successful Versus Unsuccessful Encoding for Same-Race and Other-Race Faces

Memory is often less accurate for faces from another racial group than for faces from ones own racial group. The mechanisms underlying this phenomenon are a topic of active debate. Contemporary theories invoke factors such as inferior expertise with faces from other racial groups and an encoding emphasis on race-specifying information. We investigated neural mechanisms of this memory bias by recording event-related potentials while participants attempted to memorize same-race (SR) and other-race (OR) faces. Brain potentials at encoding were compared as a function of successful versus unsuccessful recognition on a subsequent-memory test. Late positive amplitudes predicted subsequent memory for SR faces and, to a lesser extent, for OR faces. By contrast, the amplitudes of earlier frontocentral N200 potentials and occipito-temporal P2 potentials were larger for later-remembered relative to later-forgotten OR faces. Furthermore, N200 and P2 amplitudes were larger for OR faces with features considered atypical of that race relative to faces that were race-stereotypical (according to a consensus from a large group of other participants). In keeping with previous reports, we infer that these earlier potentials index the processing of unique or individuating facial information, which is key to remembering a face. Individuation may tend to be uniformly high for SR faces but lower and less reliable for OR faces. Individuation may also be more readily applied for OR faces that appear less stereotypical. These electrophysiological measures thus provide novel evidence that poorer memory for OR faces stems from encoding that is inadequate because it fails to emphasize individuating information.

Myelomeningocele and Waardenburg syndrome (type 3) in patients with interstitial deletions of 2q35 and the PAX3 gene: Possible digenic inheritance of a neural tube defect

From a spina bifida clinic we have identified two patients with a syndrome of myelomeningocele and Waardenburg syndrome type 3 (WS3). The patients each possess a single, de novo, interstitial deletion of chromosome 2 (2q35-36.2), including the PAX3 gene. Deletion of PAX3 was confirmed by fluorescence in situ hybridization (FISH). Analysis with PAX3 and flanking microsatellites shows that the deleted interval of chromosome 2 is of paternal origin and is at least 2 and 6 cM in the two patients. Interstitial deletions in this region result in the Waardenburg syndrome (WS1), but have not been associated with neural tube defects (NTDs). Although other etiologies have not been formally excluded, these patients raise the possibility of a digenic etiology of their NTDs via a genetic interaction of the deleted PAX3 gene with a second unidentified locus.

Assuming too much from ‘familiar’ brain potentials

Familiarity is sometimes associated with midfrontal old/new (FN400) signals, but investigators assume too much by inferring familiarity whenever they identify these signals. We describe how Rosburg and colleagues (2011) made this assumption, yielding potentially faulty conclusions about the recognition heuristic. We provide an alternative interpretation emphasizing implicit processing that can underlie decision-making.

Familiarity or conceptual priming? good question! comment on stenberg, hellman, johansson, and rosén (2009)

Stenberg et al. argued that FN400 brain potentials index familiarity rather than conceptual priming. Their data from a test of name recognition showed that both familiarity and FN400s were influenced by frequency but not fame, whereas separate behavioral measures of priming were influenced by fame but not frequency. However, this apparent dissociation was gravely weakened by confounds in task demands and inadequate behavioral measures of priming. Although Stenberg et al. failed to provide evidence suitable for disentangling neural correlates of familiarity from those of conceptual priming, an analysis of their report can be used to highlight difficulties that remain to be surmounted to understand recognition and the neural events that signal distinct memory functions engaged during recognition.

Relational memory and self-efficacy measures reveal distinct profiles of subjective memory concerns in older adults.

OBJECTIVE Subjective memory concerns (SMCs) in healthy older adults are associated with future decline and can indicate preclinical dementia. However, SMCs may be multiply determined, and often correlate with affective or psychosocial variables rather than with performance on memory tests. Our objective was to identify sensitive and selective methods to disentangle the underlying causes of SMCs. METHOD Because preclinical dementia pathology targets the hippocampus, we hypothesized that performance on hippocampally dependent relational memory tests would correlate with SMCs. We thus administered a series of memory tasks with varying dependence on relational memory processing to 91 older adults, along with questionnaires assessing depression, anxiety, and memory self-efficacy. We used correlational, regression, and mediation analyses to compare the variance in SMCs accounted for by these measures. RESULTS Performance on the task most dependent on relational memory processing showed a stronger negative association with SMCs than did other memory performance metrics. SMCs were also negatively associated with memory self-efficacy. These 2 measures, along with age and education, accounted for 40% of the variance in SMCs. Self-efficacy and relational memory were uncorrelated and independent predictors of SMCs. Moreover, self-efficacy statistically mediated the relationship between SMCs and depression and anxiety, which can be detrimental to cognitive aging. CONCLUSIONS These data identify multiple mechanisms that can contribute to SMCs, and suggest that SMCs can both cause and be caused by age-related cognitive decline. Relational memory measures may be effective assays of objective memory difficulties, while assessing self-efficacy could identify detrimental affective responses to cognitive aging. (PsycINFO Database Record

Dynamic Hippocampal and Prefrontal Contributions to Memory Processes and Representations Blur the Boundaries of Traditional Cognitive Domains

The hippocampus has long been known to be a critical component of the memory system involved in the formation and use of long-term declarative memory. However, recent findings have revealed that the reach of hippocampal contributions extends to a variety of domains and tasks that require the flexible use of cognitive and social behavior, including domains traditionally linked to prefrontal cortex (PFC), such as decision-making. In addition, the prefrontal cortex (PFC) has gained traction as a necessary part of the memory system. These findings challenge the conventional characterizations of hippocampus and PFC as being circumscribed to traditional cognitive domains. Here, we emphasize that the ability to parsimoniously account for the breadth of hippocampal and PFC contributions to behavior, in terms of memory function and beyond, requires theoretical advances in our understanding of their characteristic processing features and mental representations. Notably, several literatures exist that touch upon this issue, but have remained disjointed because of methodological differences that necessarily limit the scope of inquiry, as well as the somewhat artificial boundaries that have been historically imposed between domains of cognition. In particular, this article focuses on the contribution of relational memory theory as an example of a framework that describes both the representations and processes supported by the hippocampus, and further elucidates the role of the hippocampal–PFC network to a variety of behaviors.

Retrieval intention modulates the effects of directed forgetting instructions on recollection.

The neurocognitive basis of memory retrieval is often examined by investigating brain potential old/new effects, which are differences in brain activity between successfully remembered repeated stimuli and correctly rejected new stimuli in a recognition test. In this study, we combined analyses of old/new effects for words with an item-method directed-forgetting manipulation in order to isolate differences between the retrieval processes elicited by words that participants were initially instructed to commit to memory and those that participants were initially instructed to forget. We compared old/new effects elicited by to-be-forgotten (TBF) words with those elicited by to-be-remembered (TBR) words in both an explicit-memory test (a recognition test) and an implicit-memory test (a lexical-decision test). Behavioral results showed clear directed forgetting effects in the recognition test, but not in the lexical decision test. Mirroring the behavioral findings, analyses of brain potentials showed evidence of directed forgetting only in the recognition test. In this test, potentials from 450–650 ms (P600 old/new effects) were more positive for TBR relative to TBF words. By contrast, P600 effects evident during the lexical-decision test did not differ in magnitude between TBR and TBF items. When taken in the context of prior studies that have linked similar parietal old/new effects to the recollection of episodic information, these data suggest that directed-forgetting effects manifest primarily in greater episodic retrieval by TBR than TBF items, and that retrieval intention may be important for these directed-forgetting effects to occur.

On the pervasive influences of implicit memory.

In Voss, Lucas, and Paller (2012) we reviewed evidence that behavioral, neural and subjective phenomena often considered to be hallmarks of explicit memory can be powerfully influenced by processing related to implicit memory. We argued that, as a result, behavioral and neuroimaging experiments designed to measure explicit memory are sometimes prone to capture aspects of implicit memory instead. The nine commentaries published in response to our target article largely resonated with these conclusions. Here we highlight the numerous additional insights offered by these commentaries regarding the circumstances and precise mechanisms that may characterize relationships between implicit and explicit memory, and we describe similarities and differences with our interpretations.