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Research Articles, Systems/Circuits

Structure of Population Activity in Primary Motor Cortex for Single Finger Flexion and Extension

Spencer A. Arbuckle, Jeff Weiler, Eric A. Kirk, Charles L. Rice, Marc Schieber, J. Andrew Pruszynski, Naveed Ejaz and Jörn Diedrichsen
Journal of Neuroscience 25 November 2020, 40 (48) 9210-9223; DOI: https://doi.org/10.1523/JNEUROSCI.0999-20.2020
Spencer A. Arbuckle
1Brain and Mind Institute, Western University, London, Ontario N6A3K7, Canada
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Jeff Weiler
1Brain and Mind Institute, Western University, London, Ontario N6A3K7, Canada
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Eric A. Kirk
2School of Kinesiology, Faculty of Health Sciences, Western University, London, Ontario N6A3K7, Canada
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Charles L. Rice
2School of Kinesiology, Faculty of Health Sciences, Western University, London, Ontario N6A3K7, Canada
3Department of Anatomy & Cell Biology, Schulich School of Medicine & Dentistry, Western University, London, Ontario N6A 3K7, Canada
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Marc Schieber
4Departments of Neurology, Neuroscience, Biomedical Engineering, and Center for Visual Science, University of Rochester, Rochester, New York 14642
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J. Andrew Pruszynski
1Brain and Mind Institute, Western University, London, Ontario N6A3K7, Canada
5Departments of Physiology and Pharmacology, Psychology, Western University, London, Ontario N6A3K7, Canada
6Robarts Research Institute, Western University, London, Ontario N6A3K7, Canada
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Naveed Ejaz
1Brain and Mind Institute, Western University, London, Ontario N6A3K7, Canada
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Jörn Diedrichsen
1Brain and Mind Institute, Western University, London, Ontario N6A3K7, Canada
7Departments of Statistical and Actuarial Sciences, and Computer Science, Western University, London, Ontario N6A3K7, Canada
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Abstract

How is the primary motor cortex (M1) organized to control fine finger movements? We investigated the population activity in M1 for single finger flexion and extension, using 7T functional magnetic resonance imaging (fMRI) in female and male human participants and compared these results to the neural spiking patterns recorded in two male monkeys performing the identical task. fMRI activity patterns were distinct for movements of different fingers, but were quite similar for flexion and extension of the same finger. In contrast, spiking patterns in monkeys were quite distinct for both fingers and directions, which is similar to what was found for muscular activity patterns. The discrepancy between fMRI and electrophysiological measurements can be explained by two (non-mutually exclusive) characteristics of the organization of finger flexion and extension movements. Given that fMRI reflects predominantly input and recurrent activity, the results can be explained by an architecture in which neural populations that control flexion or extension of the same finger produce distinct outputs, but interact tightly with each other and receive similar inputs. Additionally, neurons tuned to different movement directions for the same finger (or combination of fingers) may cluster closely together, while neurons that control different finger combinations may be more spatially separated. When measuring this organization with fMRI at a coarse spatial scale, the activity patterns for flexion and extension of the same finger would appear very similar. Overall, we suggest that the discrepancy between fMRI and electrophysiological measurements provides new insights into the general organization of fine finger movements in M1.

SIGNIFICANCE STATEMENT The primary motor cortex (M1) is important for producing individuated finger movements. Recent evidence shows that movements that commonly co-occur are associated with more similar activity patterns in M1. Flexion and extension of the same finger, which never co-occur, should therefore be associated with distinct representations. However, using carefully controlled experiments and multivariate analyses, we demonstrate that human fMRI activity patterns for flexion or extension of the same finger are highly similar. In contrast, spiking patterns measured in monkey M1 are clearly distinct. This suggests that populations controlling opposite movements of the same finger, while producing distinct outputs, may cluster together and share inputs and local processing. These results provide testable hypotheses about the organization of hand control in M1.

  • electrophysiology
  • fingers
  • fMRI
  • hand control
  • humans
  • monkeys
  • primary motor cortex

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The Journal of Neuroscience: 40 (48)
Journal of Neuroscience
Vol. 40, Issue 48
25 Nov 2020
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Structure of Population Activity in Primary Motor Cortex for Single Finger Flexion and Extension
Spencer A. Arbuckle, Jeff Weiler, Eric A. Kirk, Charles L. Rice, Marc Schieber, J. Andrew Pruszynski, Naveed Ejaz, Jörn Diedrichsen
Journal of Neuroscience 25 November 2020, 40 (48) 9210-9223; DOI: 10.1523/JNEUROSCI.0999-20.2020

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Structure of Population Activity in Primary Motor Cortex for Single Finger Flexion and Extension
Spencer A. Arbuckle, Jeff Weiler, Eric A. Kirk, Charles L. Rice, Marc Schieber, J. Andrew Pruszynski, Naveed Ejaz, Jörn Diedrichsen
Journal of Neuroscience 25 November 2020, 40 (48) 9210-9223; DOI: 10.1523/JNEUROSCI.0999-20.2020
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Keywords

  • electrophysiology
  • fingers
  • fMRI
  • hand control
  • humans
  • monkeys
  • primary motor cortex

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