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      Scene content is predominantly conveyed by high spatial frequencies in scene-selective visual cortex

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          Abstract

          In complex real-world scenes, image content is conveyed by a large collection of intertwined visual features. The visual system disentangles these features in order to extract information about image content. Here, we investigate the role of one integral component: the content of spatial frequencies in an image. Specifically, we measure the amount of image content carried by low versus high spatial frequencies for the representation of real-world scenes in scene-selective regions of human visual cortex. To this end, we attempted to decode scene categories from the brain activity patterns of participants viewing scene images that contained the full spatial frequency spectrum, only low spatial frequencies, or only high spatial frequencies, all carefully controlled for contrast and luminance. Contrary to the findings from numerous behavioral studies and computational models that have highlighted how low spatial frequencies preferentially encode image content, decoding of scene categories from the scene-selective brain regions, including the parahippocampal place area (PPA), was significantly more accurate for high than low spatial frequency images. In fact, decoding accuracy was just as high for high spatial frequency images as for images containing the full spatial frequency spectrum in scene-selective areas PPA, RSC, OPA and object selective area LOC. We also found an interesting dissociation between the posterior and anterior subdivisions of PPA: categories were decodable from both high and low spatial frequency scenes in posterior PPA but only from high spatial frequency scenes in anterior PPA; and spatial frequency was explicitly decodable from posterior but not anterior PPA. Our results are consistent with recent findings that line drawings, which consist almost entirely of high spatial frequencies, elicit a neural representation of scene categories that is equivalent to that of full-spectrum color photographs. Collectively, these findings demonstrate the importance of high spatial frequencies for conveying the content of complex real-world scenes.

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          Most cited references39

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          A cortical representation of the local visual environment.

          Medial temporal brain regions such as the hippocampal formation and parahippocampal cortex have been generally implicated in navigation and visual memory. However, the specific function of each of these regions is not yet clear. Here we present evidence that a particular area within human parahippocampal cortex is involved in a critical component of navigation: perceiving the local visual environment. This region, which we name the 'parahippocampal place area' (PPA), responds selectively and automatically in functional magnetic resonance imaging (fMRI) to passively viewed scenes, but only weakly to single objects and not at all to faces. The critical factor for this activation appears to be the presence in the stimulus of information about the layout of local space. The response in the PPA to scenes with spatial layout but no discrete objects (empty rooms) is as strong as the response to complex meaningful scenes containing multiple objects (the same rooms furnished) and over twice as strong as the response to arrays of multiple objects without three-dimensional spatial context (the furniture from these rooms on a blank background). This response is reduced if the surfaces in the scene are rearranged so that they no longer define a coherent space. We propose that the PPA represents places by encoding the geometry of the local environment.
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            Visual objects in context.

            Moshe Bar (2004)
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              Parahippocampal and retrosplenial contributions to human spatial navigation.

              Spatial navigation is a core cognitive ability in humans and animals. Neuroimaging studies have identified two functionally defined brain regions that activate during navigational tasks and also during passive viewing of navigationally relevant stimuli such as environmental scenes: the parahippocampal place area (PPA) and the retrosplenial complex (RSC). Recent findings indicate that the PPA and RSC have distinct and complementary roles in spatial navigation, with the PPA more concerned with representation of the local visual scene and RSC more concerned with situating the scene within the broader spatial environment. These findings are a first step towards understanding the separate components of the cortical network that mediates spatial navigation in humans.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: SoftwareRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: ResourcesRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: ConceptualizationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                22 December 2017
                2017
                : 12
                : 12
                : e0189828
                Affiliations
                [1 ] Department of Psychology, The Ohio State University, Columbus, Ohio, United States of America
                [2 ] Department of Psychology, University of Toronto, Toronto, Ontario, Canada
                University of Muenster, GERMANY
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0001-8585-9858
                Article
                PONE-D-17-29847
                10.1371/journal.pone.0189828
                5741213
                29272283
                06ae6f71-03f7-4cb7-aa34-95f2a8560ea8
                © 2017 Berman 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
                : 11 August 2017
                : 1 December 2017
                Page count
                Figures: 3, Tables: 0, Pages: 16
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100000038, Natural Sciences and Engineering Research Council of Canada;
                Award ID: RGPIN-2015-06696
                Award Recipient :
                Funded by: Canadian Foundation for Innovation
                Award ID: 32896
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100007224, Connaught Fund;
                Award ID: New Researcher Award
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000071, National Institute of Child Health and Human Development;
                Award ID: HD078545-A1
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100000155, Social Sciences and Humanities Research Council of Canada;
                Award ID: 430-2017-01189
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100004359, Sony Electronics;
                Award ID: Sony Faculty Research Award
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000053, National Eye Institute;
                Award ID: R01-EY025648
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/100000879, Alfred P. Sloan Foundation;
                Award ID: BR-2014-098
                Award Recipient :
                This work was supported by: Natural Sciences and Engineering Research Council of Canada, RGPIN-2015-06696, to DBW; Canadian Foundation for Innovation, 32896, to DBW; Connaught Fund, New Researcher Award, to DBW; National Eye Institute, R01-EY025648, to JDG; Alfred P. Sloan Foundation, BR-2014-098, to JDG. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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