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      Anatomical connectivity patterns predict face-selectivity in the fusiform gyrus

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          Abstract

          A fundamental assumption in neuroscience is that brain structure determines function. Accordingly, functionally distinct regions of cortex should be structurally distinct in their connections to other areas. We tested this hypothesis in relation to face selectivity in the fusiform gyrus. By using only structural connectivity, as measured through diffusion weighted imaging, we are able to predict functional activation to faces in the fusiform gyrus. These predictions outperformed two control models and a standard group-average benchmark. The structure-function relationship discovered from these participants was highly robust in predicting activation in a second group of participants, despite differences in acquisition parameters and stimuli. This approach can thus reliably estimate activation in participants who cannot perform functional imaging tasks, and is an alternative to group-activation maps. Additionally, we identified cortical regions whose connectivity is highly influential in predicting face-selectivity within the fusiform, suggesting a possible mechanistic architecture underlying face processing in humans.

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          Most cited references37

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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 small world of the cerebral cortex.

            While much information is available on the structural connectivity of the cerebral cortex, especially in the primate, the main organizational principles of the connection patterns linking brain areas, columns and individual cells have remained elusive. We attempt to characterize a wide variety of cortical connectivity data sets using a specific set of graph theory methods. We measure global aspects of cortical graphs including the abundance of small structural motifs such as cycles, the degree of local clustering of connections and the average path length. We examine large-scale cortical connection matrices obtained from neuroanatomical data bases, as well as probabilistic connection matrices at the level of small cortical neuronal populations linked by intra-areal and inter-areal connections. All cortical connection matrices examined in this study exhibit "small-world" attributes, characterized by the presence of abundant clustering of connections combined with short average distances between neuronal elements. We discuss the significance of these universal organizational features of cortex in light of functional brain anatomy. Supplementary materials are at www.indiana.edu/~cortex/lab.htm.
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              The fusiform face area: a cortical region specialized for the perception of faces.

              Faces are among the most important visual stimuli we perceive, informing us not only about a person's identity, but also about their mood, sex, age and direction of gaze. The ability to extract this information within a fraction of a second of viewing a face is important for normal social interactions and has probably played a critical role in the survival of our primate ancestors. Considerable evidence from behavioural, neuropsychological and neurophysiological investigations supports the hypothesis that humans have specialized cognitive and neural mechanisms dedicated to the perception of faces (the face-specificity hypothesis). Here, we review the literature on a region of the human brain that appears to play a key role in face perception, known as the fusiform face area (FFA). Section 1 outlines the theoretical background for much of this work. The face-specificity hypothesis falls squarely on one side of a longstanding debate in the fields of cognitive science and cognitive neuroscience concerning the extent to which the mind/brain is composed of: (i) special-purpose ('domain-specific') mechanisms, each dedicated to processing a specific kind of information (e.g. faces, according to the face-specificity hypothesis), versus (ii) general-purpose ('domain-general') mechanisms, each capable of operating on any kind of information. Face perception has long served both as one of the prime candidates of a domain-specific process and as a key target for attack by proponents of domain-general theories of brain and mind. Section 2 briefly reviews the prior literature on face perception from behaviour and neurophysiology. This work supports the face-specificity hypothesis and argues against its domain-general alternatives (the individuation hypothesis, the expertise hypothesis and others). Section 3 outlines the more recent evidence on this debate from brain imaging, focusing particularly on the FFA. We review the evidence that the FFA is selectively engaged in face perception, by addressing (and rebutting) five of the most widely discussed alternatives to this hypothesis. In section 4, we consider recent findings that are beginning to provide clues into the computations conducted in the FFA and the nature of the representations the FFA extracts from faces. We argue that the FFA is engaged both in detecting faces and in extracting the necessary perceptual information to recognize them, and that the properties of the FFA mirror previously identified behavioural signatures of face-specific processing (e.g. the face-inversion effect). Section 5 asks how the computations and representations in the FFA differ from those occurring in other nearby regions of cortex that respond strongly to faces and objects. The evidence indicates clear functional dissociations between these regions, demonstrating that the FFA shows not only functional specificity but also area specificity. We end by speculating in section 6 on some of the broader questions raised by current research on the FFA, including the developmental origins of this region and the question of whether faces are unique versus whether similarly specialized mechanisms also exist for other domains of high-level perception and cognition.
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                Author and article information

                Journal
                9809671
                21092
                Nat Neurosci
                Nat. Neurosci.
                Nature Neuroscience
                1097-6256
                1546-1726
                17 November 2011
                25 December 2011
                01 August 2012
                : 15
                : 2
                : 321-327
                Affiliations
                [1 ]Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, 43 Vassar Street, Cambridge, MA 02139
                [2 ]McGovern Institute for Brain Research, Massachusetts Institute of Technology, 43 Vassar Street, Cambridge, MA 02139
                [3 ]Harvard-MIT Health Sciences and Technology, Massachusetts Institute of Technology, 43 Vassar Street, Cambridge, MA 02139
                Author notes
                Corresponding authors: zsaygin@ 123456mit.edu (Z.M. Saygin), Phone: +1-401-9352405, Fax: +1 617-324-5311, Address: Dept. of Brain and Cognitive Sciences, Massachusetts Institute of Technology, 43 Vassar St., Room 46-4033E, Cambridge, MA 02139, dosher@ 123456mit.edu (D.E. Osher), Phone: +1-617-324-4355, Fax: +1 617-324-5311, Address: Dept. of Brain and Cognitive Sciences, Massachusetts Institute of Technology, 43 Vassar St., Room 46-4033A, Cambridge, MA 02139
                [*]

                Z.M.S and D.E.O contributed equally to this work

                Article
                NIHMS337421
                10.1038/nn.3001
                3267901
                22197830
                8f39c999-8cb4-443e-9969-9fa2b919144f

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                History
                Funding
                Funded by: National Eye Institute : NEI
                Award ID: T32 EY013935-01 || EY
                Funded by: National Institute on Drug Abuse : NIDA
                Award ID: R90 DA023427-01 || DA
                Funded by: National Institute of Mental Health : NIMH
                Award ID: F32 MH084488-01 || MH
                Categories
                Article

                Neurosciences
                dwi,tractography,ffa,fusiform,diffusion imaging,structural connectivity,dti
                Neurosciences
                dwi, tractography, ffa, fusiform, diffusion imaging, structural connectivity, dti

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