White matter basis for the hub-and-spoke semantic representation: evidence from semantic dementia. 2020

Yan Chen, and Lin Huang, and Keliang Chen, and Junhua Ding, and Yumei Zhang, and Qing Yang, and Yingru Lv, and Zaizhu Han, and Qihao Guo
State Key Laboratory of Cognitive Neuroscience and Learning and IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing 100875, China.

The hub-and-spoke semantic representation theory posits that semantic knowledge is processed in a neural network, which contains an amodal hub, the sensorimotor modality-specific regions, and the connections between them. The exact neural basis of the hub, regions and connectivity remains unclear. Semantic dementia could be an ideal lesion model to construct the semantic network as this disease presents both amodal and modality-specific semantic processing (e.g. colour) deficits. The goal of the present study was to identify, using an unbiased data-driven approach, the semantic hub and its general and modality-specific semantic white matter connections by investigating the relationship between the lesion degree of the network and the severity of semantic deficits in 33 patients with semantic dementia. Data of diffusion-weighted imaging and behavioural performance in processing knowledge of general semantic and six sensorimotor modalities (i.e. object form, colour, motion, sound, manipulation and function) were collected from each subject. Specifically, to identify the semantic hub, we mapped the white matter nodal degree value (a graph theoretical index) of the 90 regions in the automated anatomical labelling atlas with the general semantic abilities of the patients. Of the regions, only the left fusiform gyrus was identified as the hub because its structural connectivity strength (i.e. nodal degree value) could significantly predict the general semantic processing of the patients. To identify the general and modality-specific semantic connections of the semantic hub, we separately correlated the white matter integrity values of each tract connected with the left fusiform gyrus, with the performance for general semantic processing and each of six semantic modality processing. The results showed that the hub region worked in concert with nine other regions in the semantic memory network for general semantic processing. Moreover, the connection between the hub and the left calcarine was associated with colour-specific semantic processing. The observed effects could not be accounted for by potential confounding variables (e.g. total grey matter volume, regional grey matter volume and performance on non-semantic control tasks). Our findings refine the neuroanatomical structure of the semantic network and underline the critical role of the left fusiform gyrus and its connectivity in the network.

UI MeSH Term Description Entries
D008297 Male Males
D008568 Memory Complex mental function having four distinct phases: (1) memorizing or learning, (2) retention, (3) recall, and (4) recognition. Clinically, it is usually subdivided into immediate, recent, and remote memory.
D008875 Middle Aged An adult aged 45 - 64 years. Middle Age
D009415 Nerve Net A meshlike structure composed of interconnecting nerve cells that are separated at the synaptic junction or joined to one another by cytoplasmic processes. In invertebrates, for example, the nerve net allows nerve impulses to spread over a wide area of the net because synapses can pass information in any direction. Neural Networks (Anatomic),Nerve Nets,Net, Nerve,Nets, Nerve,Network, Neural (Anatomic),Networks, Neural (Anatomic),Neural Network (Anatomic)
D001921 Brain The part of CENTRAL NERVOUS SYSTEM that is contained within the skull (CRANIUM). Arising from the NEURAL TUBE, the embryonic brain is comprised of three major parts including PROSENCEPHALON (the forebrain); MESENCEPHALON (the midbrain); and RHOMBENCEPHALON (the hindbrain). The developed brain consists of CEREBRUM; CEREBELLUM; and other structures in the BRAIN STEM. Encephalon
D005260 Female Females
D006801 Humans Members of the species Homo sapiens. Homo sapiens,Man (Taxonomy),Human,Man, Modern,Modern Man
D000368 Aged A person 65 years of age or older. For a person older than 79 years, AGED, 80 AND OVER is available. Elderly
D012660 Semantics The relationships between symbols and their meanings. Semantic
D057180 Frontotemporal Dementia The most common clinical form of FRONTOTEMPORAL LOBAR DEGENERATION, this dementia presents with personality and behavioral changes often associated with disinhibition, apathy, and lack of insight. DDPAC,Dementia, Frontotemporal,Dementia, Frontotemporal, with Parkinsonism,Dementia, Hereditary Dysphasic Disinhibition,Disinhibition-Dementia-Parkinsonism-Amyotrophy Complex,Disinhibition-Dementia-Parkinsonism-Amytrophy Complex,FTD-GRN,FTD-PGRN,FTDP-17,FTLD with TDP-43 Pathology,FTLD-17 GRN,FTLD-TDP,Familial Pick's Disease,Frontotemporal Dementia with Parkinsonism,Frontotemporal Dementia with Parkinsonism-17,Frontotemporal Dementia, Ubiquitin-Positive,Frontotemporal Lobar Degeneration With Ubiquitin-Positive Inclusions,Frontotemporal Lobe Dementia,Frontotemporal Lobe Dementia (FLDEM),GRN-Related Frontotemporal Dementia,HDDD1,HDDD2,Hereditary Dysphasic Disinhibition Dementia,Multiple System Tauopathy with Presenile Dementia,Semantic Dementia,Wilhelmsen-Lynch Disease,Complex, Disinhibition-Dementia-Parkinsonism-Amyotrophy,Complex, Disinhibition-Dementia-Parkinsonism-Amytrophy,Complices, Disinhibition-Dementia-Parkinsonism-Amyotrophy,Complices, Disinhibition-Dementia-Parkinsonism-Amytrophy,Dementia, Frontotemporal Lobe,Dementia, Frontotemporal Lobe (FLDEM),Dementia, GRN-Related Frontotemporal,Dementia, Semantic,Dementia, Ubiquitin-Positive Frontotemporal,Dementias, Frontotemporal,Dementias, Frontotemporal Lobe,Dementias, Frontotemporal Lobe (FLDEM),Dementias, GRN-Related Frontotemporal,Dementias, Semantic,Dementias, Ubiquitin-Positive Frontotemporal,Disease, Familial Pick's,Disease, Wilhelmsen-Lynch,Diseases, Familial Pick's,Diseases, Wilhelmsen-Lynch,Disinhibition Dementia Parkinsonism Amyotrophy Complex,Disinhibition Dementia Parkinsonism Amytrophy Complex,Disinhibition-Dementia-Parkinsonism-Amyotrophy Complices,Disinhibition-Dementia-Parkinsonism-Amytrophy Complices,FTLD with TDP 43 Pathology,Familial Pick Disease,Familial Pick's Diseases,Familial Picks Disease,Frontotemporal Dementia with Parkinsonism 17,Frontotemporal Dementia, GRN-Related,Frontotemporal Dementia, Ubiquitin Positive,Frontotemporal Dementias,Frontotemporal Dementias, GRN-Related,Frontotemporal Dementias, Ubiquitin-Positive,Frontotemporal Lobar Degeneration With Ubiquitin Positive Inclusions,Frontotemporal Lobe Dementias,Frontotemporal Lobe Dementias (FLDEM),GRN Related Frontotemporal Dementia,GRN-Related Frontotemporal Dementias,Lobe Dementia, Frontotemporal,Lobe Dementias, Frontotemporal,Pick's Disease, Familial,Pick's Diseases, Familial,Semantic Dementias,Ubiquitin-Positive Frontotemporal Dementia,Ubiquitin-Positive Frontotemporal Dementias,Wilhelmsen Lynch Disease,Wilhelmsen-Lynch Diseases

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