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Callosal anatomical and effective connectivity between primary motor cortices predicts visually cued bimanual temporal coordination performance

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Abstract

Default in-phase coupling of hand movements needs to be suppressed when temporal coordination is required for out-of-phase bimanual movements. There is lack of knowledge on how the brain overrides these default in-phase movements to enable a required interval of activity between hands. We used a visually cued bimanual temporal coordination (vc-BTC) paradigm with a constant rhythmical time base of 1 s, to test the accuracy of in-phase and out-of-phase (0.1, 0.2,…,0.9) finger tapping. We hypothesized that (1) stronger anatomical and effective interhemispheric connectivity between the hand areas of the primary motor cortex (M1HAND) predict higher temporal offsets between hands in the out-of-phase conditions of the vc-BTC; (2) patients with relapsing-remitting multiple sclerosis (RRMS) and clinically isolated syndrome (CIS) have reduced interhemispheric connectivity and altered between-hand coupling. Anatomical connectivity was determined by fractional anisotropy of callosal hand motor fibers (FA-hCMF). Effective connectivity was probed by short interval interhemispheric inhibition (S-IHI) using paired-coil transcranial magnetic stimulation (TMS). In healthy subjects, higher FA-hCMF and S-IHI correlated with higher temporal offsets between hands in the out-of-phase conditions of the tapping test. FA-hCMF was reduced in patients with RRMS but not in CIS, while S-IHI was reduced in both patient groups. These abnormalities were associated with smaller temporal offsets between hands leading to less deviation from the required phasing in the out-of-phase tapping conditions. Findings provide multiple levels of evidence that callosal anatomical and effective connectivity between the hand areas of the motor cortices play important roles in visually cued bimanual temporal coordination performance.

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Abbreviations

CC:

Corpus callosum

CMF:

Callosal motor fibers

CIS:

Clinically isolated syndrome

DTI:

Diffusion tensor imaging

EDSS:

Expanded disability status scale

FA:

Fractional anisotropy

FA-hCMF:

Fractional anisotropy of hand callosal motor fibers

FDI:

First dorsal interosseous

hCMF:

Hand callosal motor fibers

M1HAND :

Primary motor cortex hand area

MEP:

Motor evoked potential

9-HPT:

Nine-hole peg test

NAWM:

Normal appearing with matter

RMT:

Resting motor threshold

RRMS:

Relapsing-remitting multiple sclerosis

S-IHI:

Short interval interhemispheric inhibition

TMS:

Transcranial magnetic stimulation

vc-BTC:

Visually cued bimanual temporal coordination

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  1. Annemarie Hübers

    Present address: Department of Neurology, University Clinic, Ulm, Germany

Authors and Affiliations

  1. Department of Neurology, Goethe University, Frankfurt, Germany

    Mathias Wahl, Birgit Lauterbach-Soon, Annemarie Hübers & Ulf Ziemann

  2. Department of Neurology and Stroke, and Hertie Institute for Clinical Brain Research, Eberhard-Karls University, Hoppe-Seyler-Str. 3, 72076, Tübingen, Germany

    Ulf Ziemann

  3. Institute of Neuroradiology, Goethe University, Frankfurt, Germany

    Elke Hattingen

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Correspondence to Ulf Ziemann.

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This study was supported by a grant from TEVA Pharma GmbH.

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Wahl, M., Lauterbach-Soon, B., Hattingen, E. et al. Callosal anatomical and effective connectivity between primary motor cortices predicts visually cued bimanual temporal coordination performance. Brain Struct Funct 221, 3427–3443 (2016). https://doi.org/10.1007/s00429-015-1110-z

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