Brice A. Kuhl

Neural Reactivation Reveals Mechanisms for Updating Memory

Our ability to remember new information is often compromised by competition from prior learning, leading to many instances of forgetting. One of the challenges in studying why these lapses occur and how they can be prevented is that it is methodologically difficult to “see” competition between memories as it occurs. Here, we used multi-voxel pattern analysis of human fMRI data to measure the neural reactivation of both older (competing) and newer (target) memories during individual attempts to retrieve newer memories. Of central interest was the following: (1) whether older memories were reactivated during retrieval of newer memories; (2) how reactivation of older memories related to retrieval performance; and (3) whether neural mechanisms engaged during the encoding of newer memories were predictive of neural competition experienced during retrieval. Our results indicate that older and newer visual memories were often simultaneously reactivated in ventral temporal cortex—even when target memories were successfully retrieved. Importantly, stronger reactivation of older memories was associated with less accurate retrieval of newer memories, slower mnemonic decisions, and increased activity in anterior cingulate cortex. Finally, greater activity in the inferior frontal gyrus during the encoding of newer memories (memory updating) predicted lower competition in ventral temporal cortex during subsequent retrieval. Together, these results provide novel insight into how older memories compete with newer memories and specify neural mechanisms that allow competition to be overcome and memories to be updated.

Repetition Suppression and Multi-Voxel Pattern Similarity Differentially Track Implicit and Explicit Visual Memory

Repeated exposure to a visual stimulus is associated with corresponding reductions in neural activity, particularly within visual cortical areas. It has been argued that this phenomenon of repetition suppression is related to increases in processing fluency or implicit memory. However, repetition of a visual stimulus can also be considered in terms of the similarity of the pattern of neural activity elicited at each exposure—a measure that has recently been linked to explicit memory. Despite the popularity of each of these measures, direct comparisons between the two have been limited, and the extent to which they differentially (or similarly) relate to behavioral measures of memory has not been clearly established. In the present study, we compared repetition suppression and pattern similarity as predictors of both implicit and explicit memory. Using functional magnetic resonance imaging, we scanned 20 participants while they viewed and categorized repeated presentations of scenes. Repetition priming (facilitated categorization across repetitions) was used as a measure of implicit memory, and subsequent scene recognition was used as a measure of explicit memory. We found that repetition priming was predicted by repetition suppression in prefrontal, parietal, and occipitotemporal regions; however, repetition priming was not predicted by pattern similarity. In contrast, subsequent explicit memory was predicted by pattern similarity (across repetitions) in some of the same occipitotemporal regions that exhibited a relationship between priming and repetition suppression; however, explicit memory was not related to repetition suppression. This striking double dissociation indicates that repetition suppression and pattern similarity differentially track implicit and explicit learning.

Overcoming Suppression in Order to Remember: Contributions from Anterior Cingulate and Ventrolateral Prefrontal Cortex

The ability to remember is often compromised by competition from irrelevant memories. However, acts of selective remembering can alter the competitive relationship between memories; memories that are selected against are weakened, whereas those that are retrieved are strengthened. Whereas the weakening of selectedagainst memories is typically evidenced by subsequently poorer recall of these memories, the present study tested the hypothesis that when previously selected-against memories can subsequently be successfully retrieved, such acts of successful retrieval are associated with engagement of neurobiological mechanisms that serve to detect and overcome competition. Consistent with this hypothesis, fMRI revealed that anterior cingulate cortex and right ventrolateral prefrontal cortex are differentially engaged during successful retrieval of previously selected-against memories, and that their engagement is directly related to the magnitude of weakening that is induced by prior acts of selecting against these memories.

Age-related differences in the neural basis of the subjective vividness of memories: evidence from multivoxel pattern classification.

Although older adults often show reduced episodic memory accuracy, their ratings of the subjective vividness of their memories often equal or even exceed those of young adults. Such findings suggest that young and older adults may differentially access and/or weight different kinds of information in making vividness judgments. We examined this idea using multivoxel pattern classification of fMRI data to measure category representations while participants saw and remembered pictures of objects and scenes. Consistent with our hypothesis, there were age-related differences in how category representations related to the subjective sense of vividness. During remembering, older adults’ vividness ratings were more related, relative to young adults’, to category representations in prefrontal cortex. In contrast, young adults’ vividness ratings were more related, relative to older adults, to category representations in parietal cortex. In addition, category representations were more correlated among posterior regions in young than in older adults, whereas correlations between PFC and posterior regions did not differ between the 2 groups. Together, these results are consistent with the idea that young and older adults differentially weight different types of information in assessing subjective vividness of their memories.

The functional neuroimaging of forgetting

Forgetting is a common, often troubling, experience. Failing to remember where we left our keys, the name of a colleague, the meaning of a word we once knew, or an errand that needed to be done on the way home, can be embarrassing and, at times, quite costly. Not all instances of forgetting are unpleasant, however. More often than we realize our goal is actually to forget, rather than remember. For example, forgetting is adaptive when we move and must unlearn information that is no longer relevant, such as our old phone number and address. Similarly, workers who must repeat similar activities throughout a workday, such as a waiter who takes many similar orders in a shift, would likely be better off if they could forget the orders from earlier in the day. Thus, while many of us desire to have a perfect memory, in many ways we would be disadvantaged if we were to remember every experience. Why do we forget? This question was once one of the most prominent topics of research on memory, with much of the original work inspired by Ebbinghaus (1885/1913), who carefully documented the rate at which he forgot nonsense syllables. Early accounts pitted the idea that memories passively decay over time against the notion that subsequent learning interferes with our prior experiences, either by disrupting the consolidation of those traces into durable memories or by interfering with our ability to retrieve them. Over time, each of these theories has experienced difficulty explaining some aspects of forgetting and, thus, none has been able to provide a unified account of forgetting. Regrettably, this has meant that the field has never settled on a cohesive theory of forgetting, with modern overviews tending to focus on describing a set of experimental results without a clear theoretical account of why forgetting occurs. Given the ubiquity of forgetting in everyday life, however, a comprehensive understanding of its causes is of prime importance to theories of memory. Perhaps the primary failing of these earlier theories was the implicit assumption that forgetting is produced by a single mechanism. Instead, forgetting may arise from a disruption to any of the events that promote successful memory. Here we propose five distinct mechanisms that produce forgetting, none of which alone is sufficient to account for all types of forgetting. In the following sections, we describe the behavioral and neuroimaging evidence supporting the existence of each ofWhy do we sleep? Even after decades of investigation, this simple question remains an open issue. Indeed, there is no single answer, and complementary functional hypotheses have been suggested. For instance, it has been proposed that we sleep in order to preserve energy (Berger & Phillips, 1995), to keep cerebral thermoregulation constant (McGinty & Szymusiak, 1990), to detoxify neural cells (Inoue, Honda, & Komoda, 1995), to restore tissues (Adam & Oswald, 1977), and to preserve genetically programmed behavioural patterns (Jouvet, 1991). An additional hypothesis of interest is that sleep aids the long-term storage of memories recently acquired during wakefulness, and thus that it helps to prevent forgetting. Quintilien raised a similar idea in the 1st century AD (see Dudai, 2004). However, it was not until the beginning of the 20th century that this hypothesis was tested empirically. The first known experimental study on this matter was performed by Jenkins and Dallenbach in 1924. They showed that the classical Ebbinghaus forgetting curve for nonsense syllables was markedly dampened if the time between learning and recall was spent asleep, as opposed to time spent in the waking state. However, according to these authors and their immediate successors (e.g., Newman, 1939; Van Ormer, 1933), sleep merely had a passive role in the prevention of oblivion, by protecting novel memories from the intrusion of interfering information arising during wakefulness. A more active role for sleep was advocated 50 years later by the Nobel Prize recipient Francis Crick, who proposed with Mitchison (1983) that sleep allows us to forget undesirable memories. In their view, which is rooted in the connectionism framework, memories are specific configurations of synaptic strengths within neuronal network assemblies, and learning can be defined as the ongoing modification of these synaptic strengths. According to Crick and

Lower Parietal Encoding Activation Is Associated with Sharper Information and Better Memory

Abstract Mean fMRI activation in ventral posterior parietal cortex (vPPC) during memory encoding often negatively predicts successful remembering. A popular interpretation of this phenomenon is that vPPC reflects “off‐task” processing. However, recent fMRI studies considering distributed patterns of activity suggest that vPPC actively represents encoded material. Here, we assessed the relationships between pattern‐based content representations in vPPC, mean activation in vPPC, and subsequent remembering. We analyzed data from two fMRI experiments where subjects studied then recalled word‐face or word‐scene associations. For each encoding trial, we measured 1) mean univariate activation within vPPC and 2) the strength of face/scene information as indexed by pattern analysis. Mean activation in vPPC negatively predicted subsequent remembering, but the strength of pattern‐based information in the same vPPC voxels positively predicted later memory. Indeed, univariate amplitude averaged across vPPC voxels negatively correlated with pattern‐based information strength. This dissociation reflected a tendency for univariate reductions to maximally occur in voxels that were not strongly tuned for the category of encoded stimuli. These results indicate that vPPC activity patterns reflect the content and quality of memory encoding and constitute a striking example of lower univariate activity corresponding to stronger pattern‐based information.

Strategic Control of Memory

Cognitive control mechanisms permit memory to be accessed strategically and so aid in bringing knowledge to mind that is relevant to current decisions and actions. A fundamental component of the strategic control of memory is the resolution of interference from competing, irrelevant representations. This article considers how the ventrolateral prefrontal cortex (VLPFC) regulates mnemonic competition in multiple memory systems. We initially discuss how damage to lateral prefrontal cortex impacts mnemonic function and then consider recent neuroimaging and focal lesion findings that highlight the distinct roles that subregions of the VLPFC play in the control of memory.

Stimulating memory consolidation

A study in this issue of Nature Neuroscience reports that administering caffeine to humans immediately after memory encoding enhances consolidation, as reflected by improved performance in a memory test a day later.

Reconstructing perceived and retrieved face images from activity patterns in posterior parietal cortex

Recent findings suggest that posterior parietal cortex (PPC) represents information retrieved from long-term and short-term memory. However, the nature and quality of parietal memory representations remain largely unknown. Here, we tested whether exemplar-level details of perceived and remembered stimuli are represented in PPC, using a recently developed method that allows for individual face images to be reconstructed from fMRI activity patterns (Cowen, Chun, & Kuhl, 2014). The experiment consisted of two phases: perception and working memory. During the perception phase, participants viewed hundreds of faces while performing a continuous recognition task, where they judged whether each image was repeated within a block or not. For the working memory phase, we employed a retro-cue paradigm (Harrison & Tong, 2009) in which two faces were presented in rapid succession followed by a cue to maintain one of the two faces. We first tested whether individual faces can be reconstructed from PPC activity patterns elicited during perception. We estimated a regression model that mapped face components to multi-voxel activity patterns using a set of training faces. Reconstructions were then generated for a distinct set of test faces by taking linear combinations of the predicted component weights. Reconstructions created from PPC were more similar to the actually viewed face than other test faces, indicating that PPC distinguishes individual face images. We further explored whether we could reconstruct faces retrieved from working memory. We trained the model on the perception phase data and applied it to the patterns obtained during the working memory delay period. Reconstructions generated from the delay period activity in PPC exhibited above-chance similarity to the original face, suggesting that the contents of memory can be reconstructed from PPC activity patterns. Together, these findings indicate that PPC activity patterns reflect exemplar-level details of visual stimuli during perception and retrieval from memory. Meeting abstract presented at VSS 2015.