Transcranial magnetic stimulation and action observation: exploring methodological issues

This thesis explored a number of methodological issues present in motor cognition research using transcranial magnetic stimulation (TMS). The facilitatory effect of the corticospinal pathway during observation of simple hand actions was also investigated. TMS was applied to the motor cortex during action observation and the resulting MEP peak-to-peak amplitudes were analysed. A series of four studies were conducted to test whether a motor facilitation effect specific to the muscles involved in the observed actions were obtained, while simultaneously investigating five prominent methodological concerns in TMS research. In Study 1 the issue of choosing the optimal control condition was investigated. The MEP facilitation obtained during action observation (ball pinch) was compared to two commonly used control conditions (fixation cross and static image). Consistent with published literature, the action condition resulted in larger MEP amplitudes than the controls. There was no statistical difference in MEP amplitude between the two resting conditions. It was argued, however, that the static image allows for more accurate comparison with the action condition by providing meaningful visual cues without the associated action. In Study 2, the effect of short-term physical execution on the relationship between observed actions and neural activity was explored. The motor facilitation effect was present during action observation. This was not enhanced following execution of the observed action which is in contrast with the literature that shows the observation-execution matching system tuned to familiarity with an action. In TMS studies, different stimulation timings are included in order to reduce anticipatory effects of the TMS pulse. While the different timings are usually analysed together, in Studies 1 and 2, the two stimulation timings were analysed separately. As a consequence, a motor facilitation effect was only evident for the earlier stimulation timing of 6250ms in Study 1. When participants executed the action prior to observing it in Study 2, there was no effect of stimulation timing, leading to speculation that the prior execution may have had some effect on the attentional demands during the subsequent observation. Studies 3 and 4 explored two general methods concerns regarding the motor hotspot and stimulation intensity. In Study 3, the muscle- vi specificity notion was explored via observation of index finger and little finger movements versus observation of a static hand, with the corresponding muscles tested at their individual hotspots. This was a novel approach as one hotspot is typically used for all muscles under investigation. The choice of motor hotspot, however, did not significantly affect the muscle-specific findings, providing further support for the muscle-specific motor facilitation findings reported in the literature. Finally, Study 4 investigated the concept of stimulation intensity. TMS action observation studies differ in the stimulation intensities used, typically ranging from 110% to 130% of resting motor threshold. Since the motor response obtained through TMS may be affected depending on the stimulation intensity used, two stimulation intensities were employed (high vs. low) during observation of finger movements. A motor facilitation effect was reported in the low intensity stimulation, which was expected given that near threshold intensities are more representative of the ongoing level of cortical excitability. No motor facilitation effect was shown in the high intensity stimulation, possibly due to the nature of high stimulation intensities on the corticospinal pathway, or simply because the low intensity stimulations were always delivered before the high intensity stimulations. In light of the stimulation timing findings of Study 1, this may have resulted in participants getting distracted or fatigued, focussing their attention elsewhere (and therefore lowering MEP amplitudes) during the latter high stimulations. From the results presented in these studies, it is clear that there is a muscle specific motor facilitation during action observation and its characteristics are influenced by many procedural, technical and cognitive and attentional factors. This thesis provides a much needed critical analysis into the methods and methodologies commonly adopted in this area of research. It is essential to continue to explore the methods employed in TMS motor cognition studies, making them accepted universally and scientifically rigorous

Differences in cortical activity related to motor planning between experienced guitarists and non-musicians during guitar playing.

The influence of motor skill learning on movement-related brain activity was investigated using electroencephalography. Previous research has indicated that experienced performers display movement-related cortical potentials (MRCPs) of smaller amplitude and later onset compared to novices participants. Unfortunately, previous studies have lacked ecological validity with experimenters recording the MRCP prior to simple motor tasks and applying the results to more complex motor skills. This study replicated previous research using an ecologically valid motor skill; recording the MRCP from a group of experienced guitarists and a control group of non-musicians while they played a simple scale on the guitar. Results indicated no difference between groups in early motor planning. In contrast, the later, negative slope and motor potential components were of smaller amplitude and the negative slope began later in the experienced guitarists. The data may indicate that, for experienced guitarists, a reduced level of effort is required during the motor preparation phase of the task. These findings have implications for musical instrument learning as well as motor skill acquisition in general

Reflecting on mirror mechanisms:motor resonance effects during action observation only present with low-intensity transcranial magnetic stimulation

Transcranial magnetic stimulation (TMS) studies indicate that the observation of other people's actions influences the excitability of the observer's motor system. Motor evoked potential (MEP) amplitudes typically increase in muscles which would be active during the execution of the observed action. This 'motor resonance' effect is thought to result from activity in mirror neuron regions, which enhance the excitability of the primary motor cortex (M1) via cortico-cortical pathways. The importance of TMS intensity has not yet been recognised in this area of research. Low-intensity TMS predominately activates corticospinal neurons indirectly, whereas high-intensity TMS can directly activate corticospinal axons. This indicates that motor resonance effects should be more prominent when using low-intensity TMS. A related issue is that TMS is typically applied over a single optimal scalp position (OSP) to simultaneously elicit MEPs from several muscles. Whether this confounds results, due to differences in the manner that TMS activates spatially separate cortical representations, has not yet been explored. In the current study, MEP amplitudes, resulting from single-pulse TMS applied over M1, were recorded from the first dorsal interosseous (FDI) and abductor digiti minimi (ADM) muscles during the observation of simple finger abductions. We tested if the TMS intensity (110% vs. 130% resting motor threshold) or stimulating position (FDI-OSP vs. ADM-OSP) influenced the magnitude of the motor resonance effects. Results showed that the MEP facilitation recorded in the FDI muscle during the observation of index-finger abductions was only detected using low-intensity TMS. In contrast, changes in the OSP had a negligible effect on the presence of motor resonance effects in either the FDI or ADM muscles. These findings support the hypothesis that MN activity enhances M1 excitability via cortico-cortical pathways and highlight a methodological framework by which the neural underpinnings of action observation can be further explored. © 2013 Loporto et al

Reduced motor cortex activity during movement preparation following a period of motor skill practice

Experts in a skill produce movement-related cortical potentials (MRCPs) of smaller amplitude and later onset than novices. This may indicate that, following long-term training, experts require less effort to plan motor skill performance. However, no longitudinal evidence exists to support this claim. To address this, EEG was used to study the effect of motor skill training on cortical activity related to motor planning. Ten non-musicians took part in a 5-week training study learning to play guitar. At week 1, the MRCP was recorded from motor areas whilst participants played the G Major scale. Following a period of practice of the scale, the MRCP was recorded again at week 5. Results showed that the amplitude of the later pre-movement components were smaller at week 5 compared to week 1. This may indicate that, following training, less activity at motor cortex sites is involved in motor skill preparation. This supports claims for a more efficient motor preparation following motor skill training

Prior action execution has no effect on corticospinal facilitation during action observation

Transcranial magnetic stimulation (TMS) has been used widely in research investigating corticospinal (CS) excitability during action observation. Generally, this work has shown that observation of an action performed by others, in the absence of overt movement, modulates the excitability of the CS pathway in humans. Despite the extent of the literature exploring action observation effects, however, there has been little research to date that has compared observation with the combination of observation and execution directly. Here, we report a single-pulse TMS study that investigated whether CS excitability during action observation was modulated by actions performed by the observers prior to viewing a ball pinching action. The results showed that CS excitability during action observation increased when compared to observation of a static hand, but that there was no additional motor facilitation when participants performed the same action prior to observing it. Our findings highlight the importance of action observation and its consequences on the CS system, whilst also illustrating the limited effect of prior action execution on the CS pathway for a simple action task

The mean MEP amplitudes recorded from the right FDI muscle during observation of index and static videos at high and low stimulation intensity in experiment 1.

<p>The MEP amplitudes are presented as <i>z</i>-scores (mean ± SE). Significant differences are indicated by asterisks (*<i>p</i> = 0.001).</p

Three different videos used in this study.

<p>Experiment 1 consisted of: (i) static hand and; (ii) index-finger movements. Experiment 2 consisted of: (i) static hand; (ii) index-finger movements and; (iii) little finger movements. One TMS pulse was delivered per video at either 2500 or 3500 ms after video onset.</p

Individual participant's values for OSP and resting motor threshold percentage.

<p>The most common OSPs were 4 cm lateral and 1.5 cm anterior for FDI-OSP, and 4 cm lateral for ADM-OSP (all relative to Cz). The mean threshold value was 47% for FDI-OSP and 50% for ADM-OSP.</p

MEP amplitudes obtained in experiment 2. Values are in µV (mean ± S.D.).

<p>MEP amplitudes obtained in experiment 2. Values are in µV (mean ± S.D.).</p

The mean MEP amplitudes recorded from the participants' right FDI (left panel) and right ADM (right panel) muscles during observation of index, little, and static videos recorded from the FDI-OSP (white) and ADM-OSP (black) in experiment 2.

<p>The MEP amplitudes are presented as <i>z</i>-scores (mean ± SE). Significant differences are indicated by asterisks (*<i>p</i> = 0.05).</p