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      Holistic Face Categorization in Higher Order Visual Areas of the Normal and Prosopagnosic Brain: Toward a Non-Hierarchical View of Face Perception

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          Abstract

          How a visual stimulus is initially categorized as a face in a network of human brain areas remains largely unclear. Hierarchical neuro-computational models of face perception assume that the visual stimulus is first decomposed in local parts in lower order visual areas. These parts would then be combined into a global representation in higher order face-sensitive areas of the occipito-temporal cortex. Here we tested this view in fMRI with visual stimuli that are categorized as faces based on their global configuration rather than their local parts (two-tones Mooney figures and Arcimboldo's facelike paintings). Compared to the same inverted visual stimuli that are not categorized as faces, these stimuli activated the right middle fusiform gyrus (“Fusiform face area”) and superior temporal sulcus (pSTS), with no significant activation in the posteriorly located inferior occipital gyrus (i.e., no “occipital face area”). This observation is strengthened by behavioral and neural evidence for normal face categorization of these stimuli in a brain-damaged prosopagnosic patient whose intact right middle fusiform gyrus and superior temporal sulcus are devoid of any potential face-sensitive inputs from the lesioned right inferior occipital cortex. Together, these observations indicate that face-preferential activation may emerge in higher order visual areas of the right hemisphere without any face-preferential inputs from lower order visual areas, supporting a non-hierarchical view of face perception in the visual cortex.

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          Most cited references102

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          Distributed and overlapping representations of faces and objects in ventral temporal cortex.

          The functional architecture of the object vision pathway in the human brain was investigated using functional magnetic resonance imaging to measure patterns of response in ventral temporal cortex while subjects viewed faces, cats, five categories of man-made objects, and nonsense pictures. A distinct pattern of response was found for each stimulus category. The distinctiveness of the response to a given category was not due simply to the regions that responded maximally to that category, because the category being viewed also could be identified on the basis of the pattern of response when those regions were excluded from the analysis. Patterns of response that discriminated among all categories were found even within cortical regions that responded maximally to only one category. These results indicate that the representations of faces and objects in ventral temporal cortex are widely distributed and overlapping.
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            The distinct modes of vision offered by feedforward and recurrent processing.

            An analysis of response latencies shows that when an image is presented to the visual system, neuronal activity is rapidly routed to a large number of visual areas. However, the activity of cortical neurons is not determined by this feedforward sweep alone. Horizontal connections within areas, and higher areas providing feedback, result in dynamic changes in tuning. The differences between feedforward and recurrent processing could prove pivotal in understanding the distinctions between attentive and pre-attentive vision as well as between conscious and unconscious vision. The feedforward sweep rapidly groups feature constellations that are hardwired in the visual brain, yet is probably incapable of yielding visual awareness; in many cases, recurrent processing is necessary before the features of an object are attentively grouped and the stimulus can enter consciousness.
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              Perception's shadow: long-distance synchronization of human brain activity.

              Transient periods of synchronization of oscillating neuronal discharges in the frequency range 30-80 Hz (gamma oscillations) have been proposed to act as an integrative mechanism that may bring a widely distributed set of neurons together into a coherent ensemble that underlies a cognitive act. Results of several experiments in animals provide support for this idea. In humans, gamma oscillations have been described both on the scalp (measured by electroencephalography and magnetoencephalography) and in intracortical recordings, but no direct participation of synchrony in a cognitive task has been demonstrated so far. Here we record electrical brain activity from subjects who are viewing ambiguous visual stimuli (perceived either as faces or as meaningless shapes). We show for the first time, to our knowledge, that only face perception induces a long-distance pattern of synchronization, corresponding to the moment of perception itself and to the ensuing motor response. A period of strong desynchronization marks the transition between the moment of perception and the motor response. We suggest that this desynchronization reflects a process of active uncoupling of the underlying neural ensembles that is necessary to proceed from one cognitive state to another.
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                Author and article information

                Journal
                Front Hum Neurosci
                Front. Hum. Neurosci.
                Frontiers in Human Neuroscience
                Frontiers Research Foundation
                1662-5161
                10 January 2011
                2010
                : 4
                : 225
                Affiliations
                [1] 1simpleInstitute of Research in Psychology, University of Louvain Louvain-la-Neuve, Belgium
                [2] 2simpleInstitute of Neuroscience, University of Louvain Louvain-la-Neuve, Belgium
                [3] 3simpleMaastricht University and Brain Imaging Center, University of Maastricht Maastricht, Netherlands
                Author notes

                Edited by: Leon Y. Deouell, The Hebrew University of Jerusalem, Israel

                Reviewed by: Leon Y. Deouell, The Hebrew University of Jerusalem, Israel; Galit Yovel, Tel Aviv University, Israel

                *Correspondence: Bruno Rossion, Institute of Psychology and Neuroscience, Université de Louvain, 10, Place Cardinal Mercier, 1348 Louvain-la-Neuve, Belgium. e-mail: bruno.rossion@ 123456uclouvain.be
                Article
                10.3389/fnhum.2010.00225
                3025660
                21267432
                f1e70040-1277-461f-bfab-c45ce4ec8536
                Copyright © 2011 Rossion, Dricot, Goebel and Busigny.

                This is an open-access article subject to an exclusive license agreement between the authors and the Frontiers Research Foundation, which permits unrestricted use, distribution, and reproduction in any medium, provided the original authors and source are credited.

                History
                : 14 March 2010
                : 21 November 2010
                Page count
                Figures: 18, Tables: 2, Equations: 0, References: 146, Pages: 30, Words: 17342
                Categories
                Neuroscience
                Original Research

                Neurosciences
                visual cortex,ffa,face perception,fusiform gyrus,prosopagnosia,mooney
                Neurosciences
                visual cortex, ffa, face perception, fusiform gyrus, prosopagnosia, mooney

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