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      When Learning and Remembering Compete: A Functional MRI Study

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          Abstract

          Recent functional neuroimaging evidence suggests a bottleneck between learning new information and remembering old information. In two behavioral experiments and one functional MRI (fMRI) experiment, we tested the hypothesis that learning and remembering compete when both processes happen within a brief period of time. In the first behavioral experiment, participants intentionally remembered old words displayed in the foreground, while incidentally learning new scenes displayed in the background. In line with a memory competition, we found that remembering old information was associated with impaired learning of new information. We replicated this finding in a subsequent fMRI experiment, which showed that this behavioral effect was coupled with a suppression of learning-related activity in visual and medial temporal areas. Moreover, the fMRI experiment provided evidence that left mid-ventrolateral prefrontal cortex is involved in resolving the memory competition, possibly by facilitating rapid switching between learning and remembering. Critically, a follow-up behavioral experiment in which the background scenes were replaced with a visual target detection task provided indications that the competition between learning and remembering was not merely due to attention. This study not only provides novel insight into our capacity to learn and remember, but also clarifies the neural mechanisms underlying flexible behavior.

          Author Summary

          This study provides clear evidence for a bottleneck in our memory system between learning new and remembering old information. The ability to continuously learn and remember is usually taken for granted. Virtually all interactive situations we encounter require concurrent learning and remembering. For example, normal social communication requires that we process the new information that another person is providing. While listening, we are usually already retrieving information in preparation of an appropriate reply. Other examples include driving through an unfamiliar city while interpreting familiar traffic signs, or encountering novel products during shopping while remembering what we need. Although these examples clearly illustrate the importance of the simultaneous occurrence of learning and remembering, this study shows that remembering and learning compete for resources when both processes happen within a brief period. The study also examined the neural consequences of the competition between learning and remembering using functional MRI (fMRI). In line with the behavioral competition, the neuroimaging results showed a clear suppression of learning-related brain activity as a result of concurrent remembering. Finally, the study provides evidence that a specific region in the prefrontal cortex can resolve the bottleneck, possibly by allowing rapid switching between learning and remembering

          Abstract

          When we try to learn and remember at the same time, a bottleneck occurs within our memory system with both behavioral and neural costs.

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          Most cited references21

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          The medial temporal lobe.

          The medial temporal lobe includes a system of anatomically related structures that are essential for declarative memory (conscious memory for facts and events). The system consists of the hippocampal region (CA fields, dentate gyrus, and subicular complex) and the adjacent perirhinal, entorhinal, and parahippocampal cortices. Here, we review findings from humans, monkeys, and rodents that illuminate the function of these structures. Our analysis draws on studies of human memory impairment and animal models of memory impairment, as well as neurophysiological and neuroimaging data, to show that this system (a) is principally concerned with memory, (b) operates with neocortex to establish and maintain long-term memory, and (c) ultimately, through a process of consolidation, becomes independent of long-term memory, though questions remain about the role of perirhinal and parahippocampal cortices in this process and about spatial memory in rodents. Data from neurophysiology, neuroimaging, and neuroanatomy point to a division of labor within the medial temporal lobe. However, the available data do not support simple dichotomies between the functions of the hippocampus and the adjacent medial temporal cortex, such as associative versus nonassociative memory, episodic versus semantic memory, and recollection versus familiarity.
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            Parietal lobe contributions to episodic memory retrieval.

            Although the parietal lobe is not traditionally thought to support declarative memory, recent event-related fMRI studies of episodic retrieval have consistently revealed a range of memory-related influences on activation in lateral posterior parietal cortex (PPC) and precuneus extending into posterior cingulate and retrosplenial cortex. This article surveys the fMRI literature on PPC activation during remembering, a literature that complements earlier electroencephalography data. We consider these recent memory-related fMRI responses within the context of classical ideas about parietal function that emphasize space-based attention and motor intention. We conclude by proposing three hypotheses concerning how parietal cortex might contribute to memory.
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              Left ventrolateral prefrontal cortex and the cognitive 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 goals and actions. In this review, we consider the contribution of left ventrolateral prefrontal cortex (VLPFC) to the cognitive control of memory. Reviewed evidence supports a two-process model of mnemonic control, supported by a double dissociation among rostral regions of left VLPFC. Specifically, anterior VLPFC (approximately BA 47; inferior frontal gyrus pars orbitalis) supports controlled access to stored conceptual representations, whereas mid-VLPFC (approximately BA 45; inferior frontal gyrus pars triangularis) supports a domain-general selection process that operates post-retrieval to resolve competition among active representations. We discuss the contribution of these control mechanisms across a range of mnemonic domains, including semantic retrieval, recollection of contextual details about past events, resolution of proactive interference in working memory, and task switching. Finally, we consider open directions for future research into left VLPFC function and the cognitive control of memory.
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                Author and article information

                Contributors
                Role: Academic Editor
                Journal
                PLoS Biol
                pbio
                plbi
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, USA )
                1544-9173
                1545-7885
                January 2009
                13 January 2009
                : 7
                : 1
                : e1000011
                Affiliations
                [1 ] Center for Neuroscience, Swammerdam Institute for Life Sciences, Faculty of Science, University of Amsterdam, Amsterdam, The Netherlands
                [2 ] Center for Cognitive Neuroscience, Duke University, Durham, North Carolina, United States of America
                [3 ] Department of Psychology and Neuroscience, Duke University, Durham, North Carolina, United States of America
                University of California, Irvine, United States of America
                Author notes
                * To whom correspondence should be addressed. E-mail: s.m.daselaar@ 123456uva.nl
                Article
                08-PLBI-RA-2100R4 plbi-07-01-05
                10.1371/journal.pbio.1000011
                2621268
                19143473
                f77eb469-5487-4257-abe6-2e726dbb41ff
                Copyright: © 2009 Huijbers et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                : 27 May 2008
                : 26 November 2008
                Page count
                Pages: 8
                Categories
                Research Article
                Neuroscience
                Custom metadata
                Huijbers W, Pennartz CM, Cabeza R, Daselaar SM (2009) When learning and remembering compete: A functional MRI study. PLoS Biol 7(1): e1000011. doi: 10.1371/journal.pbio.1000011

                Life sciences
                Life sciences

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