Physical distance to sensory-motor landmarks predicts language function

Author:

Wang Xiuyi123ORCID,Krieger-Redwood Katya3,Zhang Meichao3,Cui Zaixu4,Wang Xiaokang5,Karapanagiotidis Theodoros3,Du Yi6478ORCID,Leech Robert9,Bernhardt Boris C10,Margulies Daniel S1112,Smallwood Jonathan13,Jefferies Elizabeth3

Affiliation:

1. CAS Key Laboratory of Behavioral Science, Institute of Psychology , , Beijing, 100101 , China

2. Chinese Academy of Sciences , , Beijing, 100101 , China

3. Department of Psychology, University of York , Heslington, York YO10 5DD , UK

4. Chinese Institute for Brain Research , Beijing 102206 , China

5. Department of Biomedical Engineering, University of California , Davis, CA 95616 , USA

6. CAS Key Laboratory of Behavioral Science, Institute of Psychology, Chinese Academy of Sciences , Beijing, 100101 , China

7. CAS Center for Excellence in Brain Science and Intelligence Technology , Shanghai 200031 , China

8. Department of Psychology, University of Chinese Academy of Sciences , Beijing 100049 , China

9. Centre for Neuroimaging Science, Kings College London , London , UK

10. McConnell Brain Imaging Centre, McGill University , Montreal, Quebec , Canada

11. Integrative Neuroscience and Cognition Center (UMR 8002), Centre National de la Recherche Scientifique (CNRS) and Université de Paris , Paris , France

12. Wellcome Centre for Integrative Neuroimaging, Nuffield Department of Clinical Neurosciences, University of Oxford , Oxford , UK

13. Department of Psychology, Queen’s University , Kingston, Ontario , Canada

Abstract

Abstract Auditory language comprehension recruits cortical regions that are both close to sensory-motor landmarks (supporting auditory and motor features) and far from these landmarks (supporting word meaning). We investigated whether the responsiveness of these regions in task-based functional MRI is related to individual differences in their physical distance to primary sensorimotor landmarks. Parcels in the auditory network, that were equally responsive across story and math tasks, showed stronger activation in individuals who had less distance between these parcels and transverse temporal sulcus, in line with the predictions of the “tethering hypothesis,” which suggests that greater proximity to input regions might increase the fidelity of sensory processing. Conversely, language and default mode parcels, which were more active for the story task, showed positive correlations between individual differences in activation and sensory-motor distance from primary sensory-motor landmarks, consistent with the view that physical separation from sensory-motor inputs supports aspects of cognition that draw on semantic memory. These results demonstrate that distance from sensorimotor regions provides an organizing principle of functional differentiation within the cortex. The relationship between activation and geodesic distance to sensory-motor landmarks is in opposite directions for cortical regions that are proximal to the heteromodal (DMN and language network) and unimodal ends of the principal gradient of intrinsic connectivity.

Funder

Scientific Foundation of Institute of Psychology, Chinese Academy of Sciences

Strategic Priority Research Program of Chinese Academy of Sciences

National Natural Science Foundation of China

National Key Research and Development Program of China

Shandong Social Science Planning Fund Program

Scientific Foundation of Institute of Psychology, Chinese Academy of Sciences Grant

European Research Council Consolidator grant

Publisher

Oxford University Press (OUP)

Subject

Cellular and Molecular Neuroscience,Cognitive Neuroscience

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