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      Human Scalp Electroencephalography Reveals that Repetition Suppression Varies with Expectation

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          Abstract

          Repetitions of a sensory event elicit lower levels of brain activity than its initial presentation (“repetition suppression,” RS). According to one view, RS depends on the biophysics of neuronal discharge, and is thus an automatic consequence of stimulus processing (“fatigue” model). Another account suggests that RS depends on the statistical structure of the environment, and occurs when repeated stimuli are less surprising than novel stimuli (“surprise reduction” model). In support of the latter view, functional magnetic resonance imaging studies have shown that RS is modulated by the local probability of repetition. However, single-cell recordings from macaque inferotemporal area (IT) have failed to replicate this finding. Here, we recorded scalp electroencephalography from human participants viewing pairs of faces that repeated (face 1–face 1) or alternated (face 1–face 2), in contexts in which repetitions were expected or unexpected. As previously described, event-related potentials in the range of 100–400 ms recorded at posterior electrode sites and at the vertex differed between repetitions and alternations. Critically, at central electrodes, we observed that the difference between repeated and alternating stimuli was attenuated when repetitions were unexpected, as predicted by the surprise reduction model. These findings demonstrate that the modulation of RS by repetition probability is observable using direct neural recording methods in human participants, and that it occurs relatively late (>300 ms) post-stimulus. Finally, we found that theta-band (4–8 Hz) spectral power over central electrodes varied with the three-way interaction between of repetition, expectation, and the rate of change of the environment, consistent with recent reports that frontal theta may be a hallmark of learning processes originating in the anterior cingulate and medial prefrontal cortex.

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          The role of the medial frontal cortex in cognitive control.

          Adaptive goal-directed behavior involves monitoring of ongoing actions and performance outcomes, and subsequent adjustments of behavior and learning. We evaluate new findings in cognitive neuroscience concerning cortical interactions that subserve the recruitment and implementation of such cognitive control. A review of primate and human studies, along with a meta-analysis of the human functional neuroimaging literature, suggest that the detection of unfavorable outcomes, response errors, response conflict, and decision uncertainty elicits largely overlapping clusters of activation foci in an extensive part of the posterior medial frontal cortex (pMFC). A direct link is delineated between activity in this area and subsequent adjustments in performance. Emerging evidence points to functional interactions between the pMFC and the lateral prefrontal cortex (LPFC), so that monitoring-related pMFC activity serves as a signal that engages regulatory processes in the LPFC to implement performance adjustments.
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            Repetition and the brain: neural models of stimulus-specific effects.

            One of the most robust experience-related cortical dynamics is reduced neural activity when stimuli are repeated. This reduction has been linked to performance improvements due to repetition and also used to probe functional characteristics of neural populations. However, the underlying neural mechanisms are as yet unknown. Here, we consider three models that have been proposed to account for repetition-related reductions in neural activity, and evaluate them in terms of their ability to account for the main properties of this phenomenon as measured with single-cell recordings and neuroimaging techniques. We also discuss future directions for distinguishing between these models, which will be important for understanding the neural consequences of repetition and for interpreting repetition-related effects in neuroimaging data.
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              The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure.

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                Author and article information

                Journal
                Front Hum Neurosci
                Front. Hum. Neurosci.
                Frontiers in Human Neuroscience
                Frontiers Research Foundation
                1662-5161
                28 July 2011
                2011
                : 5
                Affiliations
                1simpleDepartment of Experimental Psychology, University of Oxford Oxford, UK
                Author notes

                Edited by: Francisco Barcelo, University of Illes Balears, Spain

                Reviewed by: Juliana Yordanova, Bulgarian Academy of Sciences, Bulgaria; Rik Henson, University of Cambridge, UK

                *Correspondence: Christopher Summerfield, Department of Experimental Psychology, University of Oxford, South Parks Road, Oxford, UK. e-mail: christopher.summerfield@ 123456psy.ox.ac.uk
                Article
                10.3389/fnhum.2011.00067
                3147224
                21847378
                Copyright © 2011 Summerfield, Wyart, Johnen and de Gardelle.

                This is an open-access article subject to a non-exclusive license between the authors and Frontiers Media SA, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and other Frontiers conditions are complied with.

                Page count
                Figures: 7, Tables: 0, Equations: 1, References: 76, Pages: 13, Words: 10695
                Categories
                Neuroscience
                Original Research

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