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      Direct Exploration of the Role of the Ventral Anterior Temporal Lobe in Semantic Memory: Cortical Stimulation and Local Field Potential Evidence From Subdural Grid Electrodes

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          Abstract

          Semantic memory is a crucial higher cortical function that codes the meaning of objects and words, and when impaired after neurological damage, patients are left with significant disability. Investigations of semantic dementia have implicated the anterior temporal lobe (ATL) region, in general, as crucial for multimodal semantic memory. The potentially crucial role of the ventral ATL subregion has been emphasized by recent functional neuroimaging studies, but the necessity of this precise area has not been selectively tested. The implantation of subdural electrode grids over this subregion, for the presurgical assessment of patients with partial epilepsy or brain tumor, offers the dual yet rare opportunities to record cortical local field potentials while participants complete semantic tasks and to stimulate the functionally identified regions in the same participants to evaluate the necessity of these areas in semantic processing. Across 6 patients, and utilizing a variety of semantic assessments, we evaluated and confirmed that the anterior fusiform/inferior temporal gyrus is crucial in multimodal, receptive, and expressive, semantic processing.

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          Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation.

          A number of neuroimaging findings have been interpreted as evidence that the left inferior frontal gyrus (IFG) subserves retrieval of semantic knowledge. We provide a fundamentally different interpretation, that it is not retrieval of semantic knowledge per se that is associated with left IFG activity but rather selection of information among competing alternatives from semantic memory. Selection demands were varied across three semantic tasks in a single group of subjects. Functional magnetic resonance imaging signal in overlapping regions of left IFG was dependent on selection demands in all three tasks. In addition, the degree of semantic processing was varied independently of selection demands in one of the tasks. The absence of left IFG activity for this comparison counters the argument that the effects of selection can be attributed solely to variations in degree of semantic retrieval. Our findings suggest that it is selection, not retrieval, of semantic knowledge that drives activity in the left IFG.
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            The ventral visual pathway: an expanded neural framework for the processing of object quality.

            Since the original characterization of the ventral visual pathway, our knowledge of its neuroanatomy, functional properties, and extrinsic targets has grown considerably. Here we synthesize this recent evidence and propose that the ventral pathway is best understood as a recurrent occipitotemporal network containing neural representations of object quality both utilized and constrained by at least six distinct cortical and subcortical systems. Each system serves its own specialized behavioral, cognitive, or affective function, collectively providing the raison d'être for the ventral visual pathway. This expanded framework contrasts with the depiction of the ventral visual pathway as a largely serial staged hierarchy culminating in singular object representations and more parsimoniously incorporates attentional, contextual, and feedback effects. Published by Elsevier Ltd.
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              Functional anatomy of a common semantic system for words and pictures.

              The relationship between the semantic processing of words and of pictures is a matter of debate among cognitive scientists. We studied the functional anatomy of such processing by using positron-emission tomography (PET). We contrasted activity during two semantic tasks (probing knowledge of associations between concepts, and knowledge of the visual attributes of these concepts) and a baseline task (discrimination of physical stimulus size), performed either with words or with pictures. Modality-specific activations unrelated to semantic processing occurred in the left inferior parietal lobule for words, and the right middle occipital gyrus for pictures. A semantic network common to both words and pictures extended from the left superior occipital gyrus through the middle and inferior temporal cortex to the inferior frontal gyrus. A picture-specific activation related to semantic tasks occurred in the left posterior inferior temporal sulcus, and word-specific activations related to semantic tasks were localized to the left superior temporal sulcus, left anterior middle temporal gyrus, and left inferior frontal sulcus. Thus semantic tasks activate a distributed semantic processing system shared by both words and pictures, with a few specific areas differentially active for either words or pictures.
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                Author and article information

                Journal
                Cereb Cortex
                Cereb. Cortex
                cercor
                cercor
                Cerebral Cortex (New York, NY)
                Oxford University Press
                1047-3211
                1460-2199
                October 2015
                09 December 2014
                09 December 2014
                : 25
                : 10
                : 3802-3817
                Affiliations
                [1 ]Department of Neurology
                [2 ]Department of Epilepsy, Movement Disorders and Physiology
                [3 ]Department of Neurosurgery
                [4 ]Human Brain Research Center, Kyoto University Graduate School of Medicine , Kyoto, Japan
                [5 ]Neuroscience and Aphasia Research Unit (NARU), School of Psychological Sciences , University of Manchester , Manchester, UK
                [6 ]Department of Cognitive Psychology in Education, Graduate School of Education, Kyoto University , Kyoto, Japan
                Author notes
                Address correspondence to Riki Matsumoto, MD, PhD, Department of Epilepsy, Movement Disorders and Physiology, Kyoto University Graduate School of Medicine, 54 Kawaharacho, Shogoin, Sakyo-ku, Kyoto 606-8507, Japan. Email: matsumot@ 123456kuhp.kyoto-u.ac.jp ; Prof. Matthew A. Lambon Ralph, Neuroscience and Aphasia Research Unit (NARU), School of Psychological Sciences (Zochonis Building), Brunswick Street, Manchester M13 9PL, UK. Email: matt.lambon-ralph@ 123456manchester.ac.uk

                Akio Ikeda and Matthew A. Lambon Ralph contributed equally to this work and thus are joint senior authors.

                Article
                bhu262
                10.1093/cercor/bhu262
                4585516
                25491206
                989b7a89-60a2-4095-9e79-fb432a94cbf5
                © The Author 2014. Published by Oxford University Press

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

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                Categories
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                Neurology
                anterior fusiform,basal temporal language area,semantic memory,subdural electrodes,ventral anterior temporal lobe

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