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      Integrative and distinctive coding of visual and conceptual object features in the ventral visual stream

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          Abstract

          A significant body of research in cognitive neuroscience is aimed at understanding how object concepts are represented in the human brain. However, it remains unknown whether and where the visual and abstract conceptual features that define an object concept are integrated. We addressed this issue by comparing the neural pattern similarities among object-evoked fMRI responses with behavior-based models that independently captured the visual and conceptual similarities among these stimuli. Our results revealed evidence for distinctive coding of visual features in lateral occipital cortex, and conceptual features in the temporal pole and parahippocampal cortex. By contrast, we found evidence for integrative coding of visual and conceptual object features in perirhinal cortex. The neuroanatomical specificity of this effect was highlighted by results from a searchlight analysis. Taken together, our findings suggest that perirhinal cortex uniquely supports the representation of fully specified object concepts through the integration of their visual and conceptual features.

          eLife digest

          Our ability to interact with the world depends in large part on our understanding of objects. But objects that look similar, such as a hairdryer and a gun, may do different things, while objects that look different, such as tape and glue, may have similar roles. The fact that we can effortlessly distinguish between such objects suggests that the brain combines information about an object’s visual and abstract properties.

          Nevertheless, brain imaging experiments show that thinking about what an object looks like activates different brain regions to thinking about abstract knowledge. For example, thinking about an object’s appearance activates areas that support vision, whereas thinking about how to use that object activates regions that control movement. So how does the brain combine these different kinds of information?

          Martin et al. asked healthy volunteers to answer questions about objects while lying inside a brain scanner. Questions about appearance (such as “is a hairdryer angular?”) activated different regions of the brain to questions about abstract knowledge (“is a hairdryer manmade?”). But both types of question also activated a region of the brain called the perirhinal cortex. When volunteers responded to either type of question, the activity in their perirhinal cortex signaled both the physical appearance of the object as well as its abstract properties, even though both types of information were not necessary for the task. This suggests that information in the perirhinal cortex reflects combinations of multiple features of objects.

          These findings provide insights into a neurodegenerative disorder called semantic dementia. Patients with semantic dementia lose their general knowledge about the world. This leads to difficulties interacting with everyday objects. Patients may try to use a fork to comb their hair, for example. Notably, the perirhinal cortex is a brain region that is usually damaged in semantic dementia. Loss of combined information about the visual and abstract properties of objects may lie at the core of the observed impairments.

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          Most cited references80

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          Information-based functional brain mapping.

          The development of high-resolution neuroimaging and multielectrode electrophysiological recording provides neuroscientists with huge amounts of multivariate data. The complexity of the data creates a need for statistical summary, but the local averaging standardly applied to this end may obscure the effects of greatest neuroscientific interest. In neuroimaging, for example, brain mapping analysis has focused on the discovery of activation, i.e., of extended brain regions whose average activity changes across experimental conditions. Here we propose to ask a more general question of the data: Where in the brain does the activity pattern contain information about the experimental condition? To address this question, we propose scanning the imaged volume with a "searchlight," whose contents are analyzed multivariately at each location in the brain.
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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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                Author and article information

                Contributors
                Role: Reviewing Editor
                Journal
                eLife
                Elife
                eLife
                eLife
                eLife Sciences Publications, Ltd
                2050-084X
                02 February 2018
                2018
                : 7
                : e31873
                Affiliations
                [1 ]deptDepartment of Psychology University of Toronto TorontoCanada
                [2 ]deptDepartment of Psychology Mount Allison University SackvilleCanada
                [3 ]deptRotman Research Institute Baycrest TorontoCanada
                [4 ]deptDepartment of Psychology Queen's University KingstonCanada
                [5]University of Pennsylvania United States
                [6]University of Pennsylvania United States
                Author information
                http://orcid.org/0000-0002-7014-4371
                Article
                31873
                10.7554/eLife.31873
                5832413
                29393853
                5e121436-53bf-4d79-bae9-d8cff84132c1
                © 2018, Martin et al

                This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

                History
                : 10 September 2017
                : 01 February 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100000038, Natural Sciences and Engineering Research Council of Canada;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000913, James S. McDonnell Foundation;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001804, Canada Research Chairs;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000192, Ontario Ministry of Economic Development and Innovation;
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100000038, Natural Sciences and Engineering Research Council of Canada;
                Award ID: PDF - 502437 - 2017
                Award Recipient :
                The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
                Categories
                Research Article
                Neuroscience
                Custom metadata
                Perirhinal cortex, a brain structure located in the medial temporal lobe, uniquely supports the integration of visual and conceptual object information.

                Life sciences
                semantic memory,visual cognition,integration,fmri,perirhinal cortex,ventral visual stream,human

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