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      A common neural substrate for processing scenes and egomotion-compatible visual motion

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          Abstract

          Neuroimaging studies have revealed two separate classes of category-selective regions specialized in optic flow (egomotion-compatible) processing and in scene/place perception. Despite the importance of both optic flow and scene/place recognition to estimate changes in position and orientation within the environment during self-motion, the possible functional link between egomotion- and scene-selective regions has not yet been established. Here we reanalyzed functional magnetic resonance images from a large sample of participants performing two well-known “localizer” fMRI experiments, consisting in passive viewing of navigationally relevant stimuli such as buildings and places (scene/place stimulus) and coherently moving fields of dots simulating the visual stimulation during self-motion (flow fields). After interrogating the egomotion-selective areas with respect to the scene/place stimulus and the scene-selective areas with respect to flow fields, we found that the egomotion-selective areas V6+ and pIPS/V3A responded bilaterally more to scenes/places compared to faces, and all the scene-selective areas (parahippocampal place area or PPA, retrosplenial complex or RSC, and occipital place area or OPA) responded more to egomotion-compatible optic flow compared to random motion. The conjunction analysis between scene/place and flow field stimuli revealed that the most important focus of common activation was found in the dorsolateral parieto-occipital cortex, spanning the scene-selective OPA and the egomotion-selective pIPS/V3A. Individual inspection of the relative locations of these two regions revealed a partial overlap and a similar response profile to an independent low-level visual motion stimulus, suggesting that OPA and pIPS/V3A may be part of a unique motion-selective complex specialized in encoding both egomotion- and scene-relevant information, likely for the control of navigation in a structured environment.

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          The online version of this article (10.1007/s00429-020-02112-8) contains supplementary material, which is available to authorized users.

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          Separate visual pathways for perception and action.

          Accumulating neuropsychological, electrophysiological and behavioural evidence suggests that the neural substrates of visual perception may be quite distinct from those underlying the visual control of actions. In other words, the set of object descriptions that permit identification and recognition may be computed independently of the set of descriptions that allow an observer to shape the hand appropriately to pick up an object. We propose that the ventral stream of projections from the striate cortex to the inferotemporal cortex plays the major role in the perceptual identification of objects, while the dorsal stream projecting from the striate cortex to the posterior parietal region mediates the required sensorimotor transformations for visually guided actions directed at such objects.
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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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              A new neural framework for visuospatial processing.

              The division of cortical visual processing into distinct dorsal and ventral streams is a key framework that has guided visual neuroscience. The characterization of the ventral stream as a 'What' pathway is relatively uncontroversial, but the nature of dorsal stream processing is less clear. Originally proposed as mediating spatial perception ('Where'), more recent accounts suggest it primarily serves non-conscious visually guided action ('How'). Here, we identify three pathways emerging from the dorsal stream that consist of projections to the prefrontal and premotor cortices, and a major projection to the medial temporal lobe that courses both directly and indirectly through the posterior cingulate and retrosplenial cortices. These three pathways support both conscious and non-conscious visuospatial processing, including spatial working memory, visually guided action and navigation, respectively.
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                Author and article information

                Contributors
                valentinasulpizio@gmail.com
                Journal
                Brain Struct Funct
                Brain Struct Funct
                Brain Structure & Function
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                1863-2653
                1863-2661
                9 July 2020
                9 July 2020
                2020
                : 225
                : 7
                : 2091-2110
                Affiliations
                [1 ]GRID grid.6292.f, ISNI 0000 0004 1757 1758, Department of Biomedical and Neuromotor Sciences-DIBINEM, , University of Bologna, ; Piazza di Porta San Donato 2, 40126 Bologna, Italy
                [2 ]GRID grid.417778.a, ISNI 0000 0001 0692 3437, Department of Cognitive and Motor Rehabilitation and Neuroimaging, , Santa Lucia Foundation (IRCCS Fondazione Santa Lucia), ; Rome, Italy
                [3 ]GRID grid.7841.a, Brain Imaging Laboratory, Department of Psychology, , Sapienza University, ; Rome, Italy
                [4 ]GRID grid.412756.3, ISNI 0000 0000 8580 6601, Department of Movement, Human and Health Sciences, , University of Rome ‘‘Foro Italico’’, ; Rome, Italy
                Author information
                http://orcid.org/0000-0001-7000-550X
                http://orcid.org/0000-0002-0640-4247
                http://orcid.org/0000-0002-0079-3755
                http://orcid.org/0000-0001-8927-3408
                http://orcid.org/0000-0002-4445-0391
                Article
                2112
                10.1007/s00429-020-02112-8
                7473967
                32647918
                b2d4e375-f044-4b81-bc90-d2b933e797a6
                © The Author(s) 2020

                Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 5 February 2020
                : 2 July 2020
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100012998, Foro Italico University of Rome;
                Award ID: FFABR
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003407, Ministero dell’Istruzione, dell’Università e della Ricerca;
                Award ID: PRIN 2015AWSW2Y
                Award Recipient :
                Categories
                Original Article
                Custom metadata
                © Springer-Verlag GmbH Germany, part of Springer Nature 2020

                Neurology
                optic flow,scene perception,functional magnetic resonance,brain mapping,opa,v3a
                Neurology
                optic flow, scene perception, functional magnetic resonance, brain mapping, opa, v3a

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