Benjamin J. Levy

Inhibitory processes and the control of memory retrieval

People are often confronted with reminders of things they would prefer not to think about. When this happens, they often attempt to put the unwanted memories out of awareness. Recent research shows that the capacity to suppress distracting traces is mediated by executive-control processes that are analogous to those involved in overriding prepotent motor responses, and it is these processes that cause persisting memory failures for the suppressed items. There is evidence that memory retrieval and motor tasks that are likely to demand executive control recruit overlapping neural mechanisms, suggesting that a common process mediates control in these domains. Together, these findings indicate that memory failures often arise from the mechanisms that lie at the heart of our capacity to influence the focus of thought.

Inhibiting Your Native Language: The Role of Retrieval-Induced Forgetting During Second-Language Acquisition

After immersion in a foreign language, speakers often have difficulty retrieving native-language words—a phenomenon known as first-language attrition. We propose that first-language attrition arises in part from the suppression of native-language phonology during second-language use, and thus is a case of phonological retrieval-induced forgetting. In two experiments, we investigated this hypothesis by having native English speakers name visual objects in a language they were learning (Spanish). Repeatedly naming the objects in Spanish reduced the accessibility of the corresponding English words, as measured by an independent-probe test of inhibition. The results establish that the phonology of the words was inhibited, as access to the concepts underlying the presented objects was facilitated, not impaired. More asymmetry between English and Spanish fluency was associated with more inhibition for native-language words. This result supports the idea that inhibition plays a functional role in overcoming interference during the early stages of second-language acquisition.

Individual differences in the suppression of unwanted memories: The executive deficit hypothesis

When confronted with reminders to an unpleasant memory, people often try to prevent the unwanted memory from coming to mind. In this article, we review behavioral and neurocognitive evidence concerning the consequences of exerting such control over memory retrieval. This work indicates that suppressing retrieval is accomplished by control mechanisms that inhibit the unwanted memories, making them harder to recall later, even when desired. This process engages executive control mechanisms mediated by the lateral prefrontal cortex to terminate recollection-related activity in the hippocampus. Together, these findings specify a neurocognitive model of how memory control operates, suggesting that executive control may be an important means of down-regulating intrusive memories over time. We conclude by proposing that individual differences in the regulation of intrusive memories in the aftermath of trauma may be mediated by pre-existing differences in executive control ability. In support of this executive deficit hypothesis, we review the recent work indicating links between executive control ability and memory suppression.

A progress report on the inhibitory account of retrieval-induced forgetting

Remembering and forgetting reflect fundamentally interdependent processes in human memory (Bjork, 2011). This interdependency is particularly apparent in research on retrieval-induced forgetting, which has shown that retrieving a subset of information can cause the forgetting of other information (Anderson et al. Journal of Experimental Psychology: Learning, Memory, & Cognition 20:1063-1087, 1994). According to one prominent theoretical account, retrieval-induced forgetting is caused by an inhibitory process that acts to resolve competition during retrieval. Specifically, when cues activate competing, contextually inappropriate responses, those responses are claimed to be inhibited in order to facilitate the retrieval of target responses (Anderson Journal of Memory and Language 49: 415–445, 2003; Levy & Anderson Trends in Cognitive Sciences 6: 299–305, 2002; Storm, 2011b). Interest in retrieval-induced forgetting has grown steadily over the past two decades. In fact, a search of the abstracts at the 5th International Conference on Memory (ICOM, York University, 2011) revealed 40 presentations specifically mentioning “retrieval-induced forgetting,” and nearly twice that number referring to the concept of inhibition. Clearly, researchers are interested in the empirical phenomenon of retrieval-induced forgetting, and inhibition is gaining increasing attention as a mechanism involved in memory. The goal of the present progress report is to critically review the inhibitory account of retrieval-induced forgetting and to provide direction so that future research can have a more meaningful impact on our understanding of human memory.

Suppressing Unwanted Memories

When reminded of something we would prefer not to think about, we often try to exclude the unwanted memory from awareness. Recent research indicates that people control unwanted memories by stopping memory retrieval, using mechanisms similar to those used to stop reflexive motor responses. Controlling unwanted memories is implemented by the lateral prefrontal cortex, which acts to reduce activity in the hippocampus, thereby impairing retention of those memories. Individual differences in the efficacy of these systems may underlie variation in how well people control intrusive memories and adapt in the aftermath of trauma. This research supports the existence of an active forgetting process and establishes a neurocognitive model for inquiry into motivated forgetting.

Purging of Memories from Conscious Awareness Tracked in the Human Brain

Understanding the neural basis of conscious experience and its regulation are fundamental goals of science. While recent research has made substantial progress in identifying the neural correlates of conscious experiences, it remains unclear how individuals exert control over the contents of awareness. In particular, can a memory that has entered the aware state be purged from consciousness if it is not currently desired? Here we tracked the correlates of consciousness in humans using functional magnetic resonance imaging and demonstrated the involvement of a downregulation mechanism that purges contents from conscious awareness. When individuals tried to prevent the retrieval of a memory in response to reminders, hippocampal activity was reduced, as previously established. Crucially, using trial-by-trial reports of phenomenal awareness, we found that this reduction of hippocampal activation was specifically associated with moments when a memory involuntarily intruded into conscious awareness and needed to be purged. This downregulation of activity during memory intrusions appears to disrupt momentary awareness of unwanted contents and, importantly, predicts impaired recall of the memory on later tests. These results tie the voluntary control of phenomenal awareness to observable changes in neural activity linked to awareness, and so provide a neurobiological model for guiding inquiry into the physical foundations of control over consciousness.

Measuring Memory Reactivation With Functional MRI: Implications for Psychological Theory

Environmental cues often remind us of earlier experiences by triggering the reactivation of memories of events past. Recent evidence suggests that memory reactivation can be observed using functional MRI and that distributed pattern analyses can even provide evidence of reactivation on individual trials. The ability to measure memory reactivation offers unique and powerful leverage on theoretical issues of long-standing interest in cognitive psychology, providing a means to address questions that have proven difficult to answer with behavioral data alone. In this article, we consider three instances. First, reactivation measures can indicate whether memory-based inferences (i.e., generalization) arise through the encoding of integrated cross-event representations or through the flexible expression of separable event memories. Second, online measures of memory reactivation may inform theories of forgetting by providing information about when competing memories are reactivated during competitive retrieval situations. Finally, neural reactivation may provide a window onto the role of replay in memory consolidation. The ability to track memory reactivation, including at the individual trial level, provides unique leverage that is not afforded by behavioral measures and thus promises to shed light on such varied topics as generalization, integration, forgetting, and consolidation.

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

Cognitive and neural consequences of memory suppression in major depressive disorder

Negative biases in cognition have been documented consistently in major depressive disorder (MDD), including difficulties in the ability to control the processing of negative material. Although negative information-processing biases have been studied using both behavioral and neuroimaging paradigms, relatively little research has been conducted examining the difficulties of depressed persons with inhibiting the retrieval of negative information from long-term memory. In this study, we used the think/no-think paradigm and functional magnetic resonance imaging to assess the cognitive and neural consequences of memory suppression in individuals diagnosed with depression and in healthy controls. The participants showed typical behavioral forgetting effects, but contrary to our hypotheses, there were no differences between the depressed and nondepressed participants or between neutral and negative memories. Relative to controls, depressed individuals exhibited greater activity in right middle frontal gyrus during memory suppression, regardless of the valence of the suppressed stimuli, and differential activity in the amygdala and hippocampus during memory suppression involving negatively valenced stimuli. These findings indicate that depressed individuals are characterized by neural anomalies during the suppression of long-term memories, increasing our understanding of the brain bases of negative cognitive biases in MDD.