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Research Articles, Development/Plasticity/Repair

Cerebellar GABA Change during Visuomotor Adaptation Relates to Adaptation Performance and Cerebellar Network Connectivity: A Magnetic Resonance Spectroscopic Imaging Study

Caroline Nettekoven, Leah Mitchell, William T. Clarke, Uzay Emir, Jon Campbell, Heidi Johansen-Berg, Ned Jenkinson and Charlotte J. Stagg
Journal of Neuroscience 12 October 2022, 42 (41) 7721-7732; DOI: https://doi.org/10.1523/JNEUROSCI.0096-22.2022
Caroline Nettekoven
1Wellcome Centre for Integrative Neuroimaging, Functional MRI of the Brain, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU UK
2Oxford Centre for Human Brain Activity, Wellcome Centre for Integrative Neuroimaging, Department of Psychiatry, University of Oxford, Oxford OX3 7JX, UK
3Medical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX1 3TH UK
4Department of Psychiatry, University of Oxford, Oxford OX3 7JX UK
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Leah Mitchell
1Wellcome Centre for Integrative Neuroimaging, Functional MRI of the Brain, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU UK
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William T. Clarke
1Wellcome Centre for Integrative Neuroimaging, Functional MRI of the Brain, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU UK
3Medical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX1 3TH UK
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Uzay Emir
5School of Health Sciences, Purdue University, Purdue, Indiana 47907
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Jon Campbell
1Wellcome Centre for Integrative Neuroimaging, Functional MRI of the Brain, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU UK
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Heidi Johansen-Berg
1Wellcome Centre for Integrative Neuroimaging, Functional MRI of the Brain, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU UK
2Oxford Centre for Human Brain Activity, Wellcome Centre for Integrative Neuroimaging, Department of Psychiatry, University of Oxford, Oxford OX3 7JX, UK
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Ned Jenkinson
6School of Sport, Exercise and Rehabilitation Sciences, University of Birmingham, Birmingham B15 2TT UK
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Charlotte J. Stagg
1Wellcome Centre for Integrative Neuroimaging, Functional MRI of the Brain, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford OX3 9DU UK
2Oxford Centre for Human Brain Activity, Wellcome Centre for Integrative Neuroimaging, Department of Psychiatry, University of Oxford, Oxford OX3 7JX, UK
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Abstract

Motor adaptation is crucial for performing accurate movements in a changing environment and relies on the cerebellum. Although cerebellar involvement has been well characterized, the neurochemical changes in the cerebellum underpinning human motor adaptation remain unknown. We used a novel magnetic resonance spectroscopic imaging (MRSI) technique to measure changes in the inhibitory neurotransmitter GABA in the human cerebellum during visuomotor adaptation. Participants (n = 17, six female) used their right hand to adapt to a rotated cursor in the scanner, compared with a control task requiring no adaptation. We spatially resolved adaptation-driven GABA changes at the cerebellar nuclei and cerebellar cortex in the left and the right cerebellar hemisphere independently and found that simple right-hand movements increase GABA in the right cerebellar nuclei and decreases GABA in the left. When isolating adaptation-driven GABA changes, we found that GABA in the left cerebellar nuclei and the right cerebellar nuclei diverged, although GABA change from baseline at the right cerebellar nuclei was not different from zero at the group level. Early adaptation-driven GABA fluctuations in the right cerebellar nuclei correlated with adaptation performance. Participants showing greater GABA decrease adapted better, suggesting early GABA change is behaviorally relevant. Early GABA change also correlated with functional connectivity change in a cerebellar network. Participants showing greater decreases in GABA showed greater strength increases in cerebellar network connectivity. Results were specific to GABA, to adaptation, and to the cerebellar network. This study provides first evidence for plastic changes in cerebellar neurochemistry during motor adaptation. Characterizing these naturally occurring neurochemical changes may provide a basis for developing therapeutic interventions to facilitate human motor adaptation.

SIGNIFICANCE STATEMENT Despite motor adaptation being fundamental to maintaining accurate movements, its neurochemical basis remains poorly understood, perhaps because measuring neurochemicals in the human cerebellum is technically challenging. Using a novel magnetic resonance spectroscopic imaging method, this study provides evidence for GABA changes in the left compared with the right cerebellar nuclei driven by both simple movement and motor adaptation. Although right cerebellar GABA changes were not significantly different from zero at the group level, the adaptation-driven GABA fluctuations in the right cerebellar nuclei correlated with adaptation performance and with functional connectivity change in a cerebellar network. These results show the first evidence for plastic changes in cerebellar neurochemistry during a cerebellar learning task. This provides the basis for developing therapeutic interventions that facilitate these naturally occurring changes to amplify cerebellar-dependent learning.

  • cerebellum
  • functional connectivity
  • GABA
  • neuroimaging
  • spectroscopy
  • visuomotor adaptation

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The Journal of Neuroscience: 42 (41)
Journal of Neuroscience
Vol. 42, Issue 41
12 Oct 2022
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Cerebellar GABA Change during Visuomotor Adaptation Relates to Adaptation Performance and Cerebellar Network Connectivity: A Magnetic Resonance Spectroscopic Imaging Study
Caroline Nettekoven, Leah Mitchell, William T. Clarke, Uzay Emir, Jon Campbell, Heidi Johansen-Berg, Ned Jenkinson, Charlotte J. Stagg
Journal of Neuroscience 12 October 2022, 42 (41) 7721-7732; DOI: 10.1523/JNEUROSCI.0096-22.2022

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Cerebellar GABA Change during Visuomotor Adaptation Relates to Adaptation Performance and Cerebellar Network Connectivity: A Magnetic Resonance Spectroscopic Imaging Study
Caroline Nettekoven, Leah Mitchell, William T. Clarke, Uzay Emir, Jon Campbell, Heidi Johansen-Berg, Ned Jenkinson, Charlotte J. Stagg
Journal of Neuroscience 12 October 2022, 42 (41) 7721-7732; DOI: 10.1523/JNEUROSCI.0096-22.2022
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Keywords

  • cerebellum
  • functional connectivity
  • GABA
  • neuroimaging
  • spectroscopy
  • visuomotor adaptation

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