Dataset Information

The Left Fusiform Gyrus is a Critical Region Contributing to the Core Behavioral Profile of Semantic Dementia.

ABSTRACT: Given that extensive cerebral regions are co-atrophic in semantic dementia (SD), it is not yet known which critical regions (SD-semantic-critical regions) are really responsible for the semantic deficits of SD. To identify the SD-semantic-critical regions, we explored the relationship between the degree of cerebral atrophy in the whole brain and the severity of semantic deficits in 19 individuals with SD. We found that the gray matter volumes (GMVs) of two regions [left fusiform gyrus (lFFG) and left parahippocampal gyrus (lPHG)] significantly correlated with the semantic scores of patients with SD. Importantly, the effects of the lFFG remained significant after controlling for the GMVs of the lPHG. Moreover, the effects of the region could not be accounted for by the total GMV, general cognitive ability, laterality of brain atrophy, or control task performance. We further observed that each atrophic portion of the lFFG along the anterior-posterior axis might dedicate to the loss of semantic functions in SD. These results reveal that the lFFG could be a critical region contributing to the semantic deficits of SD.

SUBMITTER: Ding J

PROVIDER: S-EPMC4871861 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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The Left Fusiform Gyrus is a Critical Region Contributing to the Core Behavioral Profile of Semantic Dementia.

Ding Junhua J Chen Keliang K Chen Yan Y Fang Yuxing Y Yang Qing Q Lv Yingru Y Lin Nan N Bi Yanchao Y Guo Qihao Q Han Zaizhu Z

Frontiers in human neuroscience 20160519

Given that extensive cerebral regions are co-atrophic in semantic dementia (SD), it is not yet known which critical regions (SD-semantic-critical regions) are really responsible for the semantic deficits of SD. To identify the SD-semantic-critical regions, we explored the relationship between the degree of cerebral atrophy in the whole brain and the severity of semantic deficits in 19 individuals with SD. We found that the gray matter volumes (GMVs) of two regions [left fusiform gyrus (lFFG) and ...[more]

PMID: 27242479

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Project description:Semantic memory underpins our understanding of objects, people, places, and ideas. Anomia, a disruption of semantic memory access, is the most common residual language disturbance and is seen in dementia and following injury to temporal cortex. While such anomia has been well characterized by lesion symptom mapping studies, its pathophysiology is not well understood. We hypothesize that inputs to the semantic memory system engage a specific heteromodal network hub that integrates lexical retrieval with the appropriate semantic content. Such a network hub has been proposed by others, but has thus far eluded precise spatiotemporal delineation. This limitation in our understanding of semantic memory has impeded progress in the treatment of anomia. We evaluated the cortical structure and dynamics of the lexical semantic network in driving speech production in a large cohort of patients with epilepsy using electrocorticography (n = 64), functional MRI (n = 36), and direct cortical stimulation (n = 30) during two generative language processes that rely on semantic knowledge: visual picture naming and auditory naming to definition. Each task also featured a non-semantic control condition: scrambled pictures and reversed speech, respectively. These large-scale data of the left, language-dominant hemisphere uniquely enable convergent, high-resolution analyses of neural mechanisms characterized by rapid, transient dynamics with strong interactions between distributed cortical substrates. We observed three stages of activity during both visual picture naming and auditory naming to definition that were serially organized: sensory processing, lexical semantic processing, and articulation. Critically, the second stage was absent in both the visual and auditory control conditions. Group activity maps from both electrocorticography and functional MRI identified heteromodal responses in middle fusiform gyrus, intraparietal sulcus, and inferior frontal gyrus; furthermore, the spectrotemporal profiles of these three regions revealed coincident activity preceding articulation. Only in the middle fusiform gyrus did direct cortical stimulation disrupt both naming tasks while still preserving the ability to repeat sentences. These convergent data strongly support a model in which a distinct neuroanatomical substrate in middle fusiform gyrus provides access to object semantic information. This under-appreciated locus of semantic processing is at risk in resections for temporal lobe epilepsy as well as in trauma and strokes that affect the inferior temporal cortex-it may explain the range of anomic states seen in these conditions. Further characterization of brain network behaviour engaging this region in both healthy and diseased states will expand our understanding of semantic memory and further development of therapies directed at anomia.

Project description:Background Semantic dementia (SD) is a subtype of frontotemporal dementia (FTD) characterized by language deficits due to severe temporal lobe degeneration. The consistent neuropathological diagnosis is FTD-TDP subtype C, with characteristic round TDP-43 protein inclusions in the dentate gyrus. Despite this striking clinicopathological concordance, the pathogenic mechanisms are largely unexplained forestalling the development of targeted therapeutics. Methods We carried out laser capture microdissection of the dentate gyrus of 15 SD patients and 17 non-demented controls, and assessed relative protein abundance changes by label-free quantitative mass spectrometry. To identify SD specific proteins, we compared our results to eight other FTD and Alzheimer’s disease (AD) proteomic datasets of cortical brain tissue, parallel with functional enrichment analyses and protein-protein interactions (PPI). Results Of the total 5,354 quantified proteins, 151 showed differential abundance (FDR<1%) in SD patients. Seventy-two proteins were previously found altered with the same directional change in at least one FTD/AD proteomic study, while 79 proteins were considered as showing potentially SD specific dysregulation. Functional enrichment indicated an overrepresentation of pathways related to the immune response, metabolic processes, and cell-junction assembly. PPI analysis highlighted a cluster of interacting proteins associated with adherens junction and cadherin binding– the cadherin-catenin complex. Multiple proteins in this complex showed strong and apparent specific upregulation in SD, including β-catenin (CTNNB1), γ-catenin (JUP), and N-cadherin (CDH2). Conclusions We discovered an increase of cell adhesion proteins in SD specifically constituting the cadherin-catenin complex at the synaptic membrane, essential for synaptic signaling. Although further validation is warranted, we anticipate that these findings will help unravel the disease processes underlying SD.

Dataset Information

The Left Fusiform Gyrus is a Critical Region Contributing to the Core Behavioral Profile of Semantic Dementia.

Publications

The Left Fusiform Gyrus is a Critical Region Contributing to the Core Behavioral Profile of Semantic Dementia.

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