Sub-millimeter fMRI reveals multiple topographical digit representations that form action maps in human motor cortex

Huber, L. et al. (2020) Sub-millimeter fMRI reveals multiple topographical digit representations that form action maps in human motor cortex. NeuroImage, 208, 116463. (doi: 10.1016/j.neuroimage.2019.116463) (PMID:31862526)

Abstract

The human brain coordinates a wide variety of motor activities. On a large scale, the cortical motor system is topographically organized such that neighboring body parts are represented by neighboring brain areas. This homunculus-like somatotopic organization along the central sulcus has been observed using neuroimaging for large body parts such as the face, hands and feet. However, on a finer scale, invasive electrical stimulation studies show deviations from this somatotopic organization that suggest an organizing principle based on motor actions rather than body part moved. It has not been clear how the action-map organization principle of the motor cortex in the mesoscopic (sub-millimeter) regime integrates into a body map organization principle on a macroscopic scale (cm). Here we developed and applied advanced mesoscopic (sub-millimeter) fMRI and analysis methodology to non-invasively investigate the functional organization topography across columnar and laminar structures in humans. Compared to previous methods, in this study, we could capture locally specific blood volume changes across entire brain regions along the cortical curvature. We find that individual fingers have multiple mirrored representations in the primary motor cortex depending on the movements they are involved in. We find that individual digits have cortical representations up to 3 ​mm apart from each other arranged in a column-like fashion. These representations are differentially engaged depending on whether the digits’ muscles are used for different motor actions such as flexion movements, like grasping a ball or retraction movements like releasing a ball. This research provides a starting point for non-invasive investigation of mesoscale topography across layers and columns of the human cortex and bridges the gap between invasive electrophysiological investigations and large coverage non-invasive neuroimaging.

• Item Type: Articles
• Additional Information: The research was supported by the NIMH Intramural Research Program (ZIA-MH002783). We thank Kenny Chung and Harry Hall for radiographic assistance. The study was approved under NIH Combined Neuroscience Institutional Review Board protocol 93-M-0170 (ClinicalTrials.gov identifier: NCT00001360). Laurentius Huber was funded form the NWO VENI project 016.Veni.198.032 for part of the study. Portions of this study used the high-performance computational capabilities of the Biowulf Linux cluster at the National Institutes of Health, Bethesda, MD (biowulf.nih.gov). We thank Mark Hallett for comments on the manuscript. Benedikt ​Poser ​is funded by NWO VIDI 016.Vidi.178.052 and NIH ​MH111444 NIMH (PI Feinberg). ​Sriranga Kashyap is funded by NIH MH111444 NIMH (PI Feinberg). Natalia Petridou received funding from the Netherlands Organization for Scientific Research VIDI (NWO) grant 13339 and the National Institute of Mental Health award number R01MH111417. We thank James Kolasinsky for discussions about intermediate results of this study and task design.
• Status: Published
• Refereed: Yes
• Glasgow Author(s) Enlighten ID: Goense, Dr Jozien
• Authors: Huber, L., Finn, E. S., Handwerker, D. A., Bönstrup, M., Glen, D. R., Kashyap, S., Ivanov, D., Petridou, N., Marrett, S., Goense, J., Poser, B. A., and Bandettini, P. A.
• College/School: College of Science and Engineering > School of Psychology
• Journal Name: NeuroImage
• Publisher: Elsevier
• ISSN: 1053-8119
• ISSN (Online): 1095-9572
• Published Online: 17 December 2019
• Copyright Holders: Copyright © 2020 The Authors
• First Published: First published in NeuroImage 208:116463
• Publisher Policy: Reproduced under a Creative Commons license