Temporal organisation of the brain’s intrinsic motor network: the relationship with circadian phenotype and motor performance

Elise Facer-Childs, Brunno Machado de Campos, Benita Middleton, Debra J Skene, Andrew Bagshaw

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Abstract

Background: Functional connectivity (FC) of the motor network (MN) is often used to investigate how intrinsic properties of the brain are associated with motor abilities and performance. In addition, the MN is a key feature in clinical work to map the recovery after stroke and aid the understanding of neurodegenerative disorders. Time of day variation and individual differences in circadian timing, however, have not yet been considered collectively when looking at FC.

Methods: A total of 33 healthy, right handed individuals (13 male, 23.1 ± 4.2 years) took part in the study. Actigraphy, sleep diaries and circadian phase markers (dim light melatonin onset and cortisol awakening response) were used to determine early (ECP, n = 13) and late (LCP, n = 20) circadian phenotype groups. Resting state functional MRI testing sessions were conducted at 14:00 h, 20:00 h and 08:00 h and preceded by a maximum voluntary contraction test for isometric grip strength to measure motor performance.

Results: Significant differences in FC of the MN between ECPs and LCPs were found, as well as significant variations between different times of day. A higher amplitude in diurnal variation of FC and performance was observed in LCPs compared to ECPs, with the morning being most significantly affected. Overall, lower FC was significantly associated with poorer motor performance.

Discussion: Our findings uncover intrinsic differences between times of day and circadian phenotype groups. This suggests that central mechanisms contribute to diurnal variation in motor performance and the functional integrity of the MN at rest influences the ability to perform in a motor task.
Original languageEnglish
Article number117840
Number of pages8
JournalNeuroImage
Volume232
Early online date9 Feb 2021
DOIs
Publication statusPublished - 15 May 2021

Bibliographical note

Funding Information:
This work was supported by funding from the Biotechnology and Biological Sciences Research Council (BBSRC, BB/J014532/1) and the Engineering and Physical Sciences Research Council (EPSRC, EP/J002909/1) as well as the Birmingham University Imaging Centre. B.M.C. was supported by Brazilian Institute of Neuroscience and Neurotechnology (FAPESP 2013/07559?3 and 2017/25795?7). E.R.F-C has been supported by a Wellcome Trust ISSF Accelerator fellowship (Wellcome 204846/Z/16/Z), two Innovation Connections grants (Department of Industry, Innovation and Science, Australia, #ICG000899 and #ICG001546) and is currently supported by a Science Industry Endowment Fund Ross Metcalf STEM+ Business Fellowship administered by the Commonwealth Scientific and Industrial Research Organisation. Author contributions: E.R.F-C. and A.P.B. designed the study with contributions from D.J.S. E.R.F-C collected, processed and analysed the MRI data with contributions from A.P.B. and B.M.C. B.M.C. developed the neuroimaging software used for the analyses and was involved in analysis of the data. RIA analyses was performed by B.M. E.R.F-C wrote the manuscript and created all Figures and Tables with contributions from A.P.B and B.M.C. All other authors edited the manuscript. Competing interests: B.M. and D.J.S. are co-directors of Stockgrand Ltd. E.R.F-C has received research support or consultancy fees from Team Focus Ltd, British Athletics, the Australian National Football League, the Australian National Rugby League, Henley Business School, Collingwood Football Club and St Kilda Football Club which are not related to this paper. The authors declare no other competing financial interests. Data and code availability: De-identified participant data can be made available by contacting the corresponding author upon request. Reuse is only permitted following written agreement from the corresponding author and Primary Institution. B.M.C. developed the neuroimaging software and code used for the analyses. Code can be made available by contacting the co-author B.M.C. upon request. Ethical approval and consent: The study was approved by University of Birmingham Research Ethics Committee and all participants gave written informed consent before involvement.

Keywords

  • Actigraphy
  • Chronotype
  • Circadian phenotype
  • Cortisol
  • Functional connectivity
  • Grip strength
  • Melatonin
  • Motor network
  • Motor performance
  • Resting-state functional magnetic resonance imaging (fMRI)
  • Sleep

ASJC Scopus subject areas

  • Neurology
  • Cognitive Neuroscience

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