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      Theta- and Gamma-Band Activity Discriminates Face, Body and Object Perception

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          Abstract

          Face and body perception is mediated by configural mechanisms, which allow the perception of these stimuli as a whole, rather than the sum of individual parts. Indirect measures of configural processing in visual cognition are the face and body inversion effects (FIE and BIE), which refer to the drop in performance when these stimuli are perceived upside-down. Albeit FIE and BIE have been well characterized at the behavioral level, much still needs to be understood in terms of the neurophysiological correlates of these effects. Thus, in the current study, the brain’s electrical activity has been recorded by a 128 channel electroencephalogram (EEG) in 24 healthy participants while perceiving (upright and inverted) faces, bodies and houses. EEG data were analyzed in both the time domain (i.e., event-related potentials—ERPs) and the frequency domain [i.e., induced theta (5–7 Hz) and gamma (28–45 Hz) oscillations]. ERPs amplitude results showed increased N170 amplitude for inverted faces and bodies (compared to the same stimuli presented in canonical position) but not for houses. ERPs latency results showed delayed N170 components for inverted (vs. upright) faces, houses, but not bodies. Spectral analysis of induced oscillations indicated physiological FIE and BIE; that is decreased gamma-band synchronization over right occipito-temporal electrodes for inverted (vs. upright) faces, and increased bilateral frontoparietal theta-band synchronization for inverted (vs. upright) faces. Furthermore, increased left occipito-temporal and right frontal theta-band synchronization for upright (vs. inverted) bodies was found. Our findings, thus, demonstrate clear differences in the neurophysiological correlates of face and body perception. The neurophysiological FIE suggests disruption of feature binding processes (decrease in occipital gamma oscillations for inverted faces), together with enhanced feature-based attention (increase in frontoparietal theta oscillations for inverted faces). In contrast, the BIE may suggest that structural encoding for bodies is mediated by the first stages of configural processing (decrease in occipital theta oscillations for inverted bodies).

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          Most cited references74

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          EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis.

          Evidence is presented that EEG oscillations in the alpha and theta band reflect cognitive and memory performance in particular. Good performance is related to two types of EEG phenomena (i) a tonic increase in alpha but a decrease in theta power, and (ii) a large phasic (event-related) decrease in alpha but increase in theta, depending on the type of memory demands. Because alpha frequency shows large interindividual differences which are related to age and memory performance, this double dissociation between alpha vs. theta and tonic vs. phasic changes can be observed only if fixed frequency bands are abandoned. It is suggested to adjust the frequency windows of alpha and theta for each subject by using individual alpha frequency as an anchor point. Based on this procedure, a consistent interpretation of a variety of findings is made possible. As an example, in a similar way as brain volume does, upper alpha power increases (but theta power decreases) from early childhood to adulthood, whereas the opposite holds true for the late part of the lifespan. Alpha power is lowered and theta power enhanced in subjects with a variety of different neurological disorders. Furthermore, after sustained wakefulness and during the transition from waking to sleeping when the ability to respond to external stimuli ceases, upper alpha power decreases, whereas theta increases. Event-related changes indicate that the extent of upper alpha desynchronization is positively correlated with (semantic) long-term memory performance, whereas theta synchronization is positively correlated with the ability to encode new information. The reviewed findings are interpreted on the basis of brain oscillations. It is suggested that the encoding of new information is reflected by theta oscillations in hippocampo-cortical feedback loops, whereas search and retrieval processes in (semantic) long-term memory are reflected by upper alpha oscillations in thalamo-cortical feedback loops. Copyright 1999 Elsevier Science B.V.
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            Abnormal neural oscillations and synchrony in schizophrenia.

            Converging evidence from electrophysiological, physiological and anatomical studies suggests that abnormalities in the synchronized oscillatory activity of neurons may have a central role in the pathophysiology of schizophrenia. Neural oscillations are a fundamental mechanism for the establishment of precise temporal relationships between neuronal responses that are in turn relevant for memory, perception and consciousness. In patients with schizophrenia, the synchronization of beta- and gamma-band activity is abnormal, suggesting a crucial role for dysfunctional oscillations in the generation of the cognitive deficits and other symptoms of the disorder. Dysfunctional oscillations may arise owing to anomalies in the brain's rhythm-generating networks of GABA (gamma-aminobutyric acid) interneurons and in cortico-cortical connections.
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              The many faces of configural processing.

              Adults' expertise in recognizing faces has been attributed to configural processing. We distinguish three types of configural processing: detecting the first-order relations that define faces (i.e. two eyes above a nose and mouth), holistic processing (glueing the features together into a gestalt), and processing second-order relations (i.e. the spacing among features). We provide evidence for their separability based on behavioral marker tasks, their sensitivity to experimental manipulations, and their patterns of development. We note that inversion affects each type of configural processing, not just sensitivity to second-order relations, and we review evidence on whether configural processing is unique to faces.
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                Author and article information

                Contributors
                Journal
                Front Hum Neurosci
                Front Hum Neurosci
                Front. Hum. Neurosci.
                Frontiers in Human Neuroscience
                Frontiers Media S.A.
                1662-5161
                12 March 2020
                2020
                : 14
                : 74
                Affiliations
                [1] 1Department of Psychology, University of Milan—Bicocca , Milan, Italy
                [2] 2School of Psychology, University of East London (UEL) , London, United Kingdom
                [3] 3Institute of Psychiatry, Psychology, and Neuroscience (IoPPN), King’s College London , London, United Kingdom
                [4] 4School of Architecture, Computing and Engineering, University of East London (UEL) , London, United Kingdom
                [5] 5NeuroMI: Milan Center for Neuroscience , Milan, Italy
                [6] 6Department of Education, Psychology, and Communication, University of Bari Aldo Moro , Bari, Italy
                Author notes

                Edited by: Vasil Kolev, Institute of Neurobiology (BAS), Bulgaria

                Reviewed by: Kiyoshi Nakahara, Kochi University of Technology, Japan; Márk Molnár, Institute of Cognitive Neuroscience and Psychology (MTA), Hungary

                *Correspondence: Francesco Bossi francesco.bossi@ 123456imtlucca.it

                Present address: Francesco Bossi, IMT School for Advanced Studies, Lucca, Italy

                Specialty section: This article was submitted to Cognitive Neuroscience, a section of the journal Frontiers in Human Neuroscience

                Article
                10.3389/fnhum.2020.00074
                7080986
                32226369
                97f3766c-ab27-4586-9ca4-8a273cf20e81
                Copyright © 2020 Bossi, Premoli, Pizzamiglio, Balaban, Ricciardelli and Rivolta.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 14 November 2019
                : 20 February 2020
                Page count
                Figures: 5, Tables: 0, Equations: 0, References: 89, Pages: 12, Words: 9085
                Categories
                Human Neuroscience
                Original Research

                Neurosciences
                neural oscillations,face-inversion effect,body-inversion effect,gamma activity,theta activity,configural processing

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