Dataset Information

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

ABSTRACT: 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.

SUBMITTER: Chen Y

PROVIDER: S-EPMC7191302 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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

Chen Yan Y Huang Lin L Chen Keliang K Ding Junhua J Zhang Yumei Y Yang Qing Q Lv Yingru Y Han Zaizhu Z Guo Qihao Q

Brain : a journal of neurology 20200401 4

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 ...[more]

PMID: 32155237

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Project description:Built upon a wealth of neuroimaging, neurostimulation, and neuropsychology data, a recent proposal set forth a framework termed controlled semantic cognition (CSC) to account for how the brain underpins the ability to flexibly use semantic knowledge (Lambon Ralph et al., 2017; Nature Reviews Neuroscience). In CSC, the 'semantic control' system, underpinned predominantly by the prefrontal cortex, dynamically monitors and modulates the 'semantic representation' system that consists of a 'hub' (anterior temporal lobe, ATL) and multiple 'spokes' (modality-specific areas). CSC predicts that unfamiliar and exacting semantic tasks should intensify communication between the 'control' and 'representation' systems, relative to familiar and less taxing tasks. In the present study, we used functional magnetic resonance imaging (fMRI) to test this hypothesis. Participants paired unrelated concepts by canonical colours (a less accustomed task - e.g., pairing ketchup with fire-extinguishers due to both being red) or paired well-related concepts by semantic relationship (a typical task - e.g., ketchup is related to mustard). We found the 'control' system was more engaged by atypical than typical pairing. While both tasks activated the ATL 'hub', colour pairing additionally involved occipitotemporal 'spoke' regions abutting areas of hue perception. Furthermore, we uncovered a gradient along the ventral temporal cortex, transitioning from the caudal 'spoke' zones preferring canonical colour processing to the rostral 'hub' zones preferring semantic relationship. Functional connectivity also differed between the tasks: Compared with semantic pairing, colour pairing relied more upon the inferior frontal gyrus, a key node of the control system, driving enhanced connectivity with occipitotemporal 'spoke'. Together, our findings characterise the interaction within the neural architecture of semantic cognition - the control system dynamically heightens its connectivity with relevant components of the representation system, in response to different semantic contents and difficulty levels.

Project description:In the present study, we aimed to test the association between the correct function of the left ventral white matter pathways and semantic processing (dual stream models for language processing, Hickok & Poeppel, 2004), using a new set of language tasks during intraoperative electrical stimulation at white matter level. Additionally, we evaluated brain regions needed for correct performance on the different semantic tasks using lesion-symptom analyses (voxel lesion-symptom mapping and track-wise lesion analysis) in a sample of 62 candidates for the awake brain surgery. We found that electrical stimulation in the vicinity of the inferior longitudinal and inferior fronto-occipital fasciculi disturbed performance on semantic processing tasks. Individuals presented with significantly more semantic paraphasias during brain tumor resection than during the electrical stimulation at the cortex level. Track-wise analyses confirmed the role of these left ventral pathways in semantic processing: a significant relationship was observed between the probability of inferior fronto-occipital fasciculus disconnection/damage and the semantic matching tasks, as well as the number of semantic paraphasias in naming. Importantly, the same analyses for the total score of the Boston Naming Test confirmed significant relationships between this test score and the integrity of the inferior fronto-occipital, inferior longitudinal and uncinate fasciculi. This was further supported by the results of VLSM analyses showing a significant relationship between BNT and the presence of lesion within left middle and inferior temporal gyri. The present findings provide new intraoperative evidence for the role of the white-matter ventral pathways in semantic processing, while at the same time emphasizing the need to include a broader assessment of semantic-conceptual aspects during the awake neurosurgical intervention. This approach will ensure better preservation of functional tissue in the tumoral vicinity and therefore substantially diminish post-surgical language impairments.

Project description:The neural architecture of semantic knowledge comprises two key structures: (i) A set of widely dispersed regions, located adjacent to the sensorimotor cortices, serve as spokes that represent various modality-specific and context-dependent contents. (ii) The anterior-temporal lobe (ATL) serves as a hub that computes the nonlinear mappings required to transform modality-specific information into pan-modality, multifaceted concepts. Little is understood regarding whether neural dynamics between the hub and spokes might flexibly alter depending on the nature of a concept and how it impinges upon behaviour. Using fMRI, we demonstrate for the first time that the ATL serves as a 'pivot' which dynamically forms flexible long-range networks with cortical modules specialised for different domains (in the present case, the knowledge about actions and places). In two experiments, we manipulated semantic congruity and asked participants to recognise visually presented items. In Experiment 1 (dual-object displays), the ATL increased its functional coupling with the bilateral frontoparietal action-sensitive system when the objects formed a pair that permitted semantically meaningful action. In Experiment 2 (objects embedded in a scene), the ATL augmented its coupling with the retrosplenial cortex of the place-sensitive system when the objects and scene formed a semantically coherent ensemble. Causative connectivity revealed that, while communication between the hub and spokes was bidirectional, the hub's directional impact on spokes dwarfed the strength of the inverse spoke-to-hub connectivity. Furthermore, the size of behavioural congruity effects co-varied with the strength of neural coupling between the ATL hub and action- / place-related spokes, evident both at the within-individual level (the behavioural fluctuation across scanning runs) and between-individual level (the behavioural variation of between participants). Together, these findings have important implications for understanding the machinery that links neural dynamics with semantic cognition.

Dataset Information

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

Publications

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

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