Elsevier

Brain Research

Volume 1410, 2 September 2011, Pages 101-111
Brain Research

Research Report
Continuous theta burst stimulation over the left pre-motor cortex affects sensorimotor timing accuracy and supraliminal error correction

https://doi.org/10.1016/j.brainres.2011.06.062Get rights and content

Abstract

Adjustments to movement in response to changes in our surroundings are common in everyday behavior. Previous research has suggested that the left pre-motor cortex (PMC) is specialized for the temporal control of movement and may play a role in temporal error correction. The aim of this study was to determine the role of the left PMC in sensorimotor timing and error correction using theta burst transcranial magnetic stimulation (TBS). In Experiment 1, subjects performed a sensorimotor synchronization task (SMS) with the left and the right hand before and after either continuous or intermittent TBS (cTBS or iTBS). Timing accuracy was assessed during synchronized finger tapping with a regular auditory pacing stimulus. Responses following perceivable local timing shifts in the pacing stimulus (phase shifts) were used to measure error correction. Suppression of the left PMC using cTBS decreased timing accuracy because subjects tapped further away from the pacing tones and tapping variability increased. In addition, error correction responses returned to baseline tap–tone asynchrony levels faster following negative shifts and no overcorrection occurred following positive shifts after cTBS. However, facilitation of the left PMC using iTBS did not affect timing accuracy or error correction performance. Experiment 2 revealed that error correction performance may change with practice, independent of TBS. These findings provide evidence for a role of the left PMC in both sensorimotor timing and error correction in both hands. We propose that the left PMC may be involved in voluntarily controlled phase correction responses to perceivable timing shifts.

Highlights

► We study the role of the left premotor cortex (PMC) in timing and error correction. ► Continuous theta burst stimulation over the left PMC decreased timing accuracy. ► Continuous theta burst stimulation over the left PMC affected error correction. ► The effects on timing and error correction were equal in the left and right hands. ► We conclude that the left PMC controls timing and error correction in both hands.

Introduction

Motor timing requires rhythmic coordination of perception and movement, and can be studied in a laboratory environment with the use of a sensorimotor synchronization (SMS) task. In SMS, subjects tap their finger in synchrony with a regular pacing stimulus such as an auditory tone train (Repp, 2005). SMS requires the ability to produce motor output based on anticipation of the regular stimulus. In SMS, tapping responses on average precede the pacing tone by 20 to 80 ms (termed negative mean asynchrony, Aschersleben, 2002). Several lines of research have suggested that the left pre-motor cortex (PMC) is specialized in the temporal control of movement for both hands during SMS. Functional imaging studies have consistently reported activation of the left PMC during SMS (Jäncke et al., 2000, Lutz et al., 2000, Thaut et al., 2009). Magnetoencephalography (MEG) studies have shown that the left PMC plays a modulatory role during an auditory paced SMS task, irrespective of the hand used (Pollok et al., 2006a, Pollok et al., 2008a). Furthermore, transient suppression of the left PMC using repetitive transcranial magnetic stimulation (rTMS) caused subjects to tap further away from the pacing stimuli (i.e. increased negative tap–tone asynchrony) and led to an increased variability of inter-tap intervals (Pollok et al., 2008b). These findings provide evidence that the left PMC plays an important role in motor timing.

Due to inherent variability in the motor response, error correction is required during SMS to sustain a consistent tap–tone relationship even when the pacing stimulus is regular (Repp, 2005). Error correction mechanisms can be studied using a regular SMS pacing sequence that contains occasional phase shifts (i.e. local changes in the otherwise regular inter-stimulus interval). Following these perturbations, subjects show a rapid behavioral adjustment and return to their baseline negative mean asynchrony levels within several taps (Repp, 2002a). The response to local perturbations is controlled by a phase correction mechanism. Phase correction responses to subliminal perturbations that fall below the perceptual threshold are thought to be fully automatic (Repp, 2002b). However, there is evidence that both automatic and voluntarily controlled mechanisms contribute to phase correction responses following supraliminal, perceivable timing shifts (Repp, 2002b). Additionally, a previous Positron Emission Tomography (PET) study showed that the bilateral pre-motor cortices were activated during the correction of timing shifts (Stephan et al., 2002). The findings suggested that pre-motor activity was specifically associated with shifts that were consciously perceived. Therefore, the PMC (especially the left PMC) may play a role in voluntarily controlled phase correction in response to supraliminal phase shifts, in line with earlier research (Halsband et al., 1993). In contrast, suppression by rTMS over the left PMC did not significantly change error correction in a study by Doumas et al. (2005). Hence, the exact role of the left PMC in supraliminal error correction during SMS remains unclear.

Theta burst stimulation (TBS) is a form of repetitive TMS that uses gamma frequency pulses (50 Hz) nested within a theta cycle of 5 Hz. The pattern of TBS stimulation is based on the physiological neural firing rhythm found in the animal hippocampus (Kandel and Spencer, 1961). TBS can be applied continuously (cTBS) to achieve a long-term depression-like effect, or intermittently (iTBS) by applying 2 s of TBS every 10 s to induce a long-term potentiation-like effect (Huang et al., 2005, Huang et al., 2011). The advantage of TBS over conventional repetitive TMS is that it can produce longer-lasting effects with a shorter stimulation period (Huang et al., 2005).

Here, we aimed to determine the specific role of the left PMC in sensorimotor synchronization and supraliminal error correction. To this end, we used both suppression and facilitation theta burst stimulation (TBS) protocols over the left PMC. The effect of TBS on sensorimotor timing and supraliminal error correction was measured during performance with either the left or the right hand.

Section snippets

Experiment 1: effects of TBS over the left PMC on SMS performance

The aim of Experiment 1 was to examine the effects of suppression or facilitation TBS over the left PMC on motor timing during regular SMS and on error correction following supraliminal phase shifts. We hypothesized that cTBS over the left PMC would lead to an increase in tap–tone asynchrony and variability during regular SMS. We furthermore hypothesized that cTBS over the left PMC would impair error correction performance. Lastly, we hypothesized that facilitatory iTBS over the left PMC may

Discussion

The aim of this study was to determine the role of the left PMC in sensorimotor timing and error correction. The first main finding was that continuous TBS over the left PMC affected both sensorimotor timing and supraliminal error correction. Timing performance during sensorimotor synchronization was negatively affected by continuous TBS over the left PMC such that subjects tapped further away from the tones and tapping variability increased after TBS. Error correction responses following

Subjects

A total of 16 subjects (8 males, mean age 23.3 ± 3.9) took part, all of whom were students at the University of Sheffield. All subjects were right handed (mean Edinburgh Handedness Inventory score of 73.1 ± 19.1). Twelve subjects responded positively when asked whether they had had any previous musical training. The level of musical training ranged from self-taught play to the highest level (grade 8) as defined by the Associated Board of the Royal Schools of Music, UK. None of them was a

Acknowledgments

This work was funded by the Sheffield Undergraduate Research Experience (SURE) scheme. Janine Bijsterbosch is supported by a Medical Research Council PhD studentship.

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