Distinct Effects of Brain Activation Using tDCS and Observational Practice: Implications for Motor Rehabilitation

Abstract

Complex motor skills can be acquired while observing a model without physical practice. Transcranial direct-current stimulation (tDCS) applied to the primary motor cortex (M1) also facilitates motor learning. However, the effectiveness of observational practice for bimanual coordination skills is debated. We compared the behavioural and brain causal connectivity patterns following three interventions: primary motor cortex stimulation (M1-tDCS), action-observation (AO) and a combined group (AO+M1-tDCS) when acquiring a bimanual, two-ball juggling skill. Thirty healthy young adults with no juggling experience were randomly assigned to either video observation of a skilled juggler, anodal M1-tDCS or video observation combined with M1-tDCS. Thirty trials of juggling were performed and scored after the intervention. Resting-state EEG data were collected before and after the intervention. Information flow rate was applied to EEG source data to measure causal connectivity. The two observation groups were more accurate than the tDCS alone group. In the AO condition, there was strong information exchange from (L) parietal to (R) parietal regions, strong bidirectional information exchange between (R) parietal and (R) occipital regions and an extensive network of activity that was (L) lateralized. The M1-tDCS condition was characterized by bilateral long-range connections with the strongest information exchange from the (R) occipital region to the (R) temporal and (L) occipital regions. AO+M1-tDCS induced strong bidirectional information exchange in occipital and temporal regions in both hemispheres. Uniquely, it was the only condition that was characterized by information exchange between the (R) frontal and central regions. This study provides new results about the distinct network dynamics of stimulating the brain for skill acquisition, providing insights for motor rehabilitation.

Keywords: action observation; effective connectivity; electroencephalogram; motor skill acquisition; observational learning; transcranial direct-current stimulation.

Figure 1

Experimental procedure. All participants performed a 2-trial juggle followed by 3 min eyes open resting-state EEG (rsEEG). Participants were randomized to one of three interventions: action observation (AO), tDCS stimulation (M1-tDCS), or action observation and tDCS stimulation (AO+M1-tDCS). Individuals in the AO group watched a video of a skilled juggler for 15 min. Individuals in the tDCS group received 15 min of weak direct current (2 mA) of anodal stimulation over the primary motor cortex (M1). Individuals in the AO+M1-tDCS group watched the skilled juggler video while simultaneously receiving 15 min of 2 mA anodal stimulation over M1.

Figure 2

Mean total juggling form scores (and between-participant SEs) for each of the three groups across a 2-trial pre-test and six, 5-trial blocks of post-intervention practice.

Figure 3

Causal connectivity analysis of EEG source data. Schematics (I–IV) display from top to bottom: all participants pre-intervention (N = 27), AO post-intervention (n = 10), M1-tDCS post-intervention (n = 8), and AO+M1-tDCS post-intervention (n = 9). Labels are listed in Table 1. (a) Maps of mean of absolute normalized information flow rate |τi→j|. Transmitting regions listed on the y-axis and receiving regions listed on the x-axis. (b) Maps of the top 10 mean |τi→j| values. (c) Qualitative summary illustration of the spatial distribution of the directional connections for all groups pre-intervention and each group post-intervention. The Illustration displays the top 10 connections based on the average value of |τi→j|. The five most important connections are shown in red. The next five top connections (i.e., 6–10) are shown in blue.

Figure 4

Probability density histograms of the |τi→j| values for the M1-tDCS (blue), the AO (rose) group and the AO+MI-tDCS group (green).