Department of Exercise Sciences


Inhibition in human primary motor cortex during synchronised versus syncopated finger movements

Winston D. Byblow & Cathy M. Stinear.
Published in Experimental Brain Research (2006) 168: 287-293

Introduction

Here we advance a novel hypothesis for coordinated movement—syncopation of movement with respect to a regular external beat requires greater excitability of inhibitory networks (sICI) of involved muscle representations, than the more stable synchronisation pattern.

Method

Eight right-handed subjects performed a behavioural experiment making button presses in time with a metronome beginning in syncopation. The metronome tempo was scaled from 0.8 to 2.0 Hz in 0.2 Hz increments every 5 s. The relative phase between the metronome and the finger switch was measured, and the incidence and mean transition frequency (from syncopation to synchronisation) was determined. All subjects exhibited spontaneous transitions from syncopation to synchronisation patterns around 1.70±0.18 Hz. Based on these findings, a frequency of 1 Hz was selected for the TMS experiment with the aim of comparing the two patterns at a comparable level of stability. Using single- and paired pulse TMS we examined MEPs and sICI of first dorsal interosseous (FDI) (Fig 1).

Fig.1
Fig. 1 Schematic of experimental set-up, and relative timing between auditory metronome and stimulus delivery during task performance. M is the auditory metronome; S is the speaker emitting tones when the key is pressed by index finger abduction. Hypothetical traces are overlaid (right inset). Motor-evoked potentials were recorded from the right first dorsal interosseous (FDI) in response to both single pulse (large amplitude response) and paired-pulse transcranial magnetic stimulation (TMS) (small amplitude response). The left inset illustrates schematically the timing of TMS relative to the metronome. Dashed vertical lines indicate onset of auditory metronome beats, and filled inverted triangle indicate magnetic stimuli delivery. The shaded areas represent the time window in which the button press had to be initiated in order for the trial to be included in the analysis. Button presses occurred coincident with the metronome during synchronized trials, and between metronome beats during syncopated trials. Stimuli were delivered during button presses during ON trials, and between presses during OFF trials. Hypothetical EMG traces are shown with indicative bursts identified as dark rectangles. Horizontal calibration bar represents 200 ms.

Results

The presence of the metronome did not modulate MEP amplitude or sICI at rest. Stimulator intensity was adjusted so that NC MEPs were matched between conditions before examining sICI. Inhibition (sICI) at rest was near 50% (55±7%) as intended by the procedure. There was a main effect of pattern with greater sICI during syncopation (68.8±6.7%) than synchronisation (39.4±10%); F2,8=3.7, P<0.05 (Fig. 3).

Fig.3
Fig. 3 a Two overlaid electromyography traces from a single subject recorded while at rest (left), and during the offphase of synchronised (middle) and syncopated (right) movement. Upper traces are from single-pulse timulation; lower traces are from pairedpulse stimulation. The stimulus artefact appears on the left of each trace and the evoked potential occurs 20 ms later; calibration bar 0.6 mV, 20 ms. B Group results of intracortical inhibition (%). Note: MEP amplitude decreases as intracortical inhibition increases, however, greater levels of inhibition are denoted by larger values; *P=0.011. Error bars are SEM

Interpretation

  • In support of our hypothesis, syncopation was associated with increased excitability of networks that mediate motor cortical inhibition. It seems likely that the excitability of intracortical cells that mediate sICI increased during syncopation in order to prevent entrainment to the metronome.
  • Synchronisation was associated with less inhibition, or a potential release of inhibition, relative to syncopation. This finding is consistent with recent neurophysiological evidence from experiments with healthy participants which examined sICI during rhythmic bimanual coordination. These findings may have relevance to other stereotypical motor patterns including the coupling of hand movements and other interlimb coordination patterns.

Acknowledgements

Funding was provided by the Neurological Foundation of New Zealand. The authors are grateful to Stephan Swinnen and Richard Ivry for helpful suggestions and comments on earlier drafts of this work, and to Steve McMillan for assistance with data collection and analysis.