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      Longitudinal Changes in Semantic Concreteness in Semantic Variant Primary Progressive Aphasia (svPPA)

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          Abstract

          This study examines longitudinal changes in the concreteness of nouns produced by human patients with semantic variant primary progressive aphasia (svPPA). Cross-sectional studies show that patients with svPPA demonstrate severe loss of concrete noun knowledge linked to atrophy of the left ventral temporal lobe. It is unknown how disease spread and duration affect the magnitude of the concreteness impairment in svPPA. We evaluate longitudinal spoken production of concrete nouns in svPPA, and relate this to changes in longitudinal MRI measures of gray matter (GM). Noun concreteness in svPPA is compared to that of behavioral variant frontotemporal dementia (bvFTD) patients, who typically demonstrate highly concrete speech. We elicited naturalistic speech samples at two time points (time 1 and time 2) in patients with svPPA ( n = 11) and bvFTD ( n = 15) through descriptions of the Cookie Theft picture and evaluated each spoken noun for concreteness. Compared to bvFTD patients whose noun production remained highly concrete throughout the testing period, mixed-effects models revealed that noun concreteness significantly decreased as disease progressed in svPPA. We also measured longitudinal changes to GM in a subset of svPPA patients ( n = 7), who showed significant decline in the left and right temporal and frontal regions. Regression analyses revealed that longitudinal GM atrophy in the right fusiform and parahippocampal gyri and the left superior temporal gyrus was related to decreasing noun concreteness. These results suggest that progressive atrophy of the ventral temporal lobe in svPPA contributes to declining concrete noun production over time.

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          The Spatial and Temporal Signatures of Word Production Components: A Critical Update

          In the first decade of neurocognitive word production research the predominant approach was brain mapping, i.e., investigating the regional cerebral brain activation patterns correlated with word production tasks, such as picture naming and word generation. Indefrey and Levelt (2004) conducted a comprehensive meta-analysis of word production studies that used this approach and combined the resulting spatial information on neural correlates of component processes of word production with information on the time course of word production provided by behavioral and electromagnetic studies. In recent years, neurocognitive word production research has seen a major change toward a hypothesis-testing approach. This approach is characterized by the design of experimental variables modulating single component processes of word production and testing for predicted effects on spatial or temporal neurocognitive signatures of these components. This change was accompanied by the development of a broader spectrum of measurement and analysis techniques. The article reviews the findings of recent studies using the new approach. The time course assumptions of Indefrey and Levelt (2004) have largely been confirmed requiring only minor adaptations. Adaptations of the brain structure/function relationships proposed by Indefrey and Levelt (2004) include the precise role of subregions of the left inferior frontal gyrus as well as a probable, yet to date unclear role of the inferior parietal cortex in word production.
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            What the left and right anterior fusiform gyri tell us about semantic memory.

            The study of patients with semantic dementia, a variant of frontotemporal lobar degeneration, has emerged over the last two decades as an important lesion model for studying human semantic memory. Although it is well-known that semantic dementia is associated with temporal lobe degeneration, controversy remains over whether the semantic deficit is due to diffuse temporal lobe damage, damage to only a sub-region of the temporal lobe or even less severe damage elsewhere in the brain. The manner in which the right and left temporal lobes contribute to semantic knowledge is also not fully elucidated. In this study we used unbiased imaging analyses to correlate resting cerebral glucose metabolism and behavioural scores in tests of verbal and non-verbal semantic memory. In addition, a region of interest analysis was performed to evaluate the role of severely hypometabolic areas. The best, indeed the only, strong predictor of semantic scores across a set of 21 patients with frontotemporal lobar degeneration with semantic impairment was degree of hypometabolism in the anterior fusiform region subjacent to the head and body of the hippocampus. As hypometabolism in the patients' rostral fusiform was even more extreme than the abnormality in other regions with putative semantic relevance, such as the temporal poles, the significant fusiform correlations cannot be attributed to floor-level function in these other regions. More detailed analysis demonstrated more selective correlations: left anterior fusiform function predicted performance on two expressive verbal tasks, whereas right anterior fusiform metabolism predicted performance on a non-verbal test of associative semantic knowledge. This pattern was further supported by an additional behavioural study performed on a wider cohort of patients with semantic dementia, in which the patients with more extensive right-temporal atrophy (when matched on degree of naming deficit to a set of cases with more extensive left temporal atrophy) were significantly more impaired on the test of non-verbal semantics. Our preferred interpretation of this laterality effect involves differential strength of connectivity between different regions of a widespread semantic network in the human brain.
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              Object-specific semantic coding in human perirhinal cortex.

              Category-specificity has been demonstrated in the human posterior ventral temporal cortex for a variety of object categories. Although object representations within the ventral visual pathway must be sufficiently rich and complex to support the recognition of individual objects, little is known about how specific objects are represented. Here, we used representational similarity analysis to determine what different kinds of object information are reflected in fMRI activation patterns and uncover the relationship between categorical and object-specific semantic representations. Our results show a gradient of informational specificity along the ventral stream from representations of image-based visual properties in early visual cortex, to categorical representations in the posterior ventral stream. A key finding showed that object-specific semantic information is uniquely represented in the perirhinal cortex, which was also increasingly engaged for objects that are more semantically confusable. These findings suggest a key role for the perirhinal cortex in representing and processing object-specific semantic information that is more critical for highly confusable objects. Our findings extend current distributed models by showing coarse dissociations between objects in posterior ventral cortex, and fine-grained distinctions between objects supported by the anterior medial temporal lobes, including the perirhinal cortex, which serve to integrate complex object information.
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                Author and article information

                Journal
                eNeuro
                eNeuro
                eneuro
                eneuro
                eNeuro
                eNeuro
                Society for Neuroscience
                2373-2822
                26 December 2018
                10 January 2018
                Nov-Dec 2018
                : 5
                : 6
                : ENEURO.0197-18.2018
                Affiliations
                [1 ]Department of Neurology and Penn Frontotemporal Degeneration Center
                [2 ]Department of Radiology and Penn Image Computing and Science Laboratory, University of Pennsylvania , Philadelphia, PA 19104-4283
                Author notes

                The authors declare no competing financial interests.

                Author contributions: K.A.Q.C., S.A., and M.G. designed research; S.A. performed research; K.A.Q.C. and C.A.O. analyzed data; K.A.Q.C. and M.G. wrote the paper.

                This work was supported in part by National Institutes of Health Grants AG017586, AG052943, and DC013063.

                Correspondence should be addressed to either Katheryn A. Q. Cousins or Murray Grossman, Department of Neurology, 3 West Gates, Hospital of the University of Pennsylvania, 3400 Spruce Street, Philadelphia, PA 19104-4283, E-mail: kcous@ 123456pennmedicine.upenn.edu or rossma@ 123456pennmedicine.upenn.edu .
                Author information
                https://orcid.org/0000-0002-7447-6218
                Article
                eN-NWR-0197-18
                10.1523/ENEURO.0197-18.2018
                6377408
                feae3316-a22a-4b12-9b65-e2ae96b0f0e3
                Copyright © 2018 Cousins et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 18 May 2018
                : 26 October 2018
                : 22 November 2018
                Page count
                Figures: 3, Tables: 5, Equations: 0, References: 59, Pages: 10, Words: 8196
                Funding
                Funded by: http://doi.org/10.13039/100000049HHS | NIH | National Institute on Aging (NIA)
                Award ID: AG017586
                Award ID: AG052943
                Funded by: http://doi.org/10.13039/100000055HHS | NIH | National Institute on Deafness and Other Communication Disorders (NIDCD)
                Award ID: DC013063
                Categories
                1
                1.1
                New Research
                Cognition and Behavior
                Custom metadata
                November/December 2018

                concreteness,frontotemporal dementia,longitudinal,semantic memory,semantic variant primary progressive aphasia,ventral temporal lobe

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