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      Individual face- and house-related eye movement patterns distinctively activate FFA and PPA

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          Abstract

          We investigated if the fusiform face area (FFA) and the parahippocampal place area (PPA) contain a representation of fixation sequences that are typically used when looking at faces or houses. Here, we instructed observers to follow a dot presented on a uniform background. The dot’s movements represented gaze paths acquired separately from observers looking at face or house pictures. Even when gaze dispersion differences were controlled, face- and house-associated gaze patterns could be discriminated by fMRI multivariate pattern analysis in FFA and PPA, more so for the current observer’s own gazes than for another observer’s gaze. The discrimination of the observer’s own gaze patterns was not observed in early visual areas (V1 – V4) or superior parietal lobule and frontal eye fields. These findings indicate a link between perception and action—the complex gaze patterns that are used to explore faces and houses—in the FFA and PPA.

          Abstract

          The fusiform face area and parahippocampal place area respond to face and scene stimuli respectively. Here, the authors show using fMRI that these brain areas are also preferentially activated by eye movements associated with looking at faces and scenes even when no images are shown.

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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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            The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception

            Using functional magnetic resonance imaging (fMRI), we found an area in the fusiform gyrus in 12 of the 15 subjects tested that was significantly more active when the subjects viewed faces than when they viewed assorted common objects. This face activation was used to define a specific region of interest individually for each subject, within which several new tests of face specificity were run. In each of five subjects tested, the predefined candidate “face area” also responded significantly more strongly to passive viewing of (1) intact than scrambled two-tone faces, (2) full front-view face photos than front-view photos of houses, and (in a different set of five subjects) (3) three-quarter-view face photos (with hair concealed) than photos of human hands; it also responded more strongly during (4) a consecutive matching task performed on three-quarter-view faces versus hands. Our technique of running multiple tests applied to the same region defined functionally within individual subjects provides a solution to two common problems in functional imaging: (1) the requirement to correct for multiple statistical comparisons and (2) the inevitable ambiguity in the interpretation of any study in which only two or three conditions are compared. Our data allow us to reject alternative accounts of the function of the fusiform face area (area “FF”) that appeal to visual attention, subordinate-level classification, or general processing of any animate or human forms, demonstrating that this region is selectively involved in the perception of faces.
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              Assignment of functional activations to probabilistic cytoarchitectonic areas revisited.

              Probabilistic cytoarchitectonic maps in standard reference space provide a powerful tool for the analysis of structure-function relationships in the human brain. While these microstructurally defined maps have already been successfully used in the analysis of somatosensory, motor or language functions, several conceptual issues in the analysis of structure-function relationships still demand further clarification. In this paper, we demonstrate the principle approaches for anatomical localisation of functional activations based on probabilistic cytoarchitectonic maps by exemplary analysis of an anterior parietal activation evoked by visual presentation of hand gestures. After consideration of the conceptual basis and implementation of volume or local maxima labelling, we comment on some potential interpretational difficulties, limitations and caveats that could be encountered. Extending and supplementing these methods, we then propose a supplementary approach for quantification of structure-function correspondences based on distribution analysis. This approach relates the cytoarchitectonic probabilities observed at a particular functionally defined location to the areal specific null distribution of probabilities across the whole brain (i.e., the full probability map). Importantly, this method avoids the need for a unique classification of voxels to a single cortical area and may increase the comparability between results obtained for different areas. Moreover, as distribution-based labelling quantifies the "central tendency" of an activation with respect to anatomical areas, it will, in combination with the established methods, allow an advanced characterisation of the anatomical substrates of functional activations. Finally, the advantages and disadvantages of the various methods are discussed, focussing on the question of which approach is most appropriate for a particular situation.
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                Author and article information

                Contributors
                stefan.pollmann@ovgu.de
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                4 December 2019
                4 December 2019
                2019
                : 10
                : 5532
                Affiliations
                [1 ]ISNI 0000 0001 1018 4307, GRID grid.5807.a, Department of Experimental Psychology, , Otto-von-Guericke University, ; Magdeburg, Germany
                [2 ]GRID grid.452320.2, Center for Behavioral Brain Sciences, ; Magdeburg, Germany
                [3 ]ISNI 0000 0004 0368 8293, GRID grid.16821.3c, Institute of Psychology and Behavioral Science, , Shanghai Jiao Tong University, ; Shanghai, China
                [4 ]ISNI 0000 0004 0368 8293, GRID grid.16821.3c, Shanghai Key Laboratory of Psychotic Disorders, Shanghai Mental Health Center, Shanghai Jiao Tong University School of Medicine, ; Shanghai, China
                [5 ]ISNI 0000 0001 2297 375X, GRID grid.8385.6, Institute of Neuroscience and Medicine, Brain & Behaviour (INM-7), Research Centre Jülich, ; Jülich, Germany
                [6 ]ISNI 0000 0001 2176 9917, GRID grid.411327.2, Institute of Systems Neuroscience, Medical Faculty, , Heinrich Heine University Düsseldorf, ; Düsseldorf, Germany
                [7 ]ISNI 0000 0004 0368 505X, GRID grid.253663.7, Beijing Key Laboratory of Learning and Cognition and School of Psychology, Capital Normal University, ; Beijing, China
                Author information
                http://orcid.org/0000-0001-5840-5658
                Article
                13541
                10.1038/s41467-019-13541-3
                6892816
                31797874
                729a6e66-3e03-45b4-a01b-8bc2814d7bcf
                © The Author(s) 2019

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 11 February 2019
                : 12 November 2019
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100008530, EC | European Regional Development Fund (Europski Fond za Regionalni Razvoj);
                Award ID: ZS/2016/04/78113
                Award ID: ZS/2016/04/78113
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft (German Research Foundation);
                Award ID: PO 548/14-2
                Award Recipient :
                Categories
                Article
                Custom metadata
                © The Author(s) 2019

                Uncategorized
                attention,perception,sensory processing,human behaviour
                Uncategorized
                attention, perception, sensory processing, human behaviour

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