Does sonification of action simulation training impact corticospinal excitability and audiomotor plasticity?

Fabio Castro,Giovanni Di Pino,Daniel Bishop,Aleksandra Vuckovic,Alexander Nowicky,Ladan Osman

doi:10.1007/s00221-021-06069-w

Fabio Castro, Giovanni Di Pino + Show 4 more

Open Access

https://doi.org/10.1007/s00221-021-06069-w

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Abstract

Sonification is a sensory augmentation strategy whereby a sound is associated with, and modulated by, movement. Evidence suggests that sonification could be a viable strategy to maximize learning and rehabilitation. Recent studies investigated sonification of action observation, reporting beneficial effects, especially in Parkinson’s disease. However, research on simulation training—a training regime based on action observation and motor imagery, in which actions are internally simulated, without physical execution—suggest that action observation alone is suboptimal, compared to the combined use of action observation and motor imagery. In this study, we explored the effects of sonified action observation and motor imagery on corticospinal excitability, as well as to evaluate the extent of practice-dependent plasticity induced by this training. Nineteen participants were recruited to complete a practice session based on combined and congruent action observation and motor imagery (AOMI) and physical imitation of the same action. Prior to the beginning, participants were randomly assigned to one of two groups, one group (nine participants) completed the practice block with sonified AOMI, while the other group (ten participants) completed the practice without extrinsic auditory information and served as control group. To investigate practice-induced plasticity, participants completed two auditory paired associative stimulation (aPAS) protocols, one completed after the practice block, and another one completed alone, without additional interventions, at least 7 days before the practice. After the practice block, both groups significantly increased their corticospinal excitability, but sonification did not exert additional benefits, compared to non-sonified conditions. In addition, aPAS significantly increased corticospinal excitability when completed alone, but when it was primed by a practice block, no modulatory effects on corticospinal excitability were found. It is possible that sonification of combined action observation and motor imagery may not be a useful strategy to improve corticospinal, but further studies are needed to explore its relationship with performance improvements. We also confirm the neuromodulatory effect of aPAS, but its interaction with audiomotor practice remain unclear.

Highlights

Motor skill learning is a fundamental aspect of everyday life and injury recovery
Evidence shows that AOMI may enhance learning and performance compared with AO or MI alone, in sport contexts (Aoyama et al 2020; Romano-Smith et al 2018), rehabilitation, such as stroke (Sun et al 2016) and Developmental Coordination Disorder (DCD; Marshall et al 2020; Scott et al 2019)
To measure changes in corticospinal excitability as a result of the intervention and auditory paired associative stimulation (aPAS), we investigated changes in peak-to-peak amplitude motor-evoked potentials (MEPs) of the right first dorsal interosseous (FDI) muscle, a muscle that was involved in the action

Summary

Introduction

Recent evidence exploring strategies to maximize learning suggest that action simulation training. Experimental Brain Research (2021) 239:1489–1505 based on action observation (AO) and motor imagery (MI) could be an effective addition to the learning process (Ruffino et al 2017; Ste-Marie et al 2012), and rehabilitation (for a review see Abbruzzese et al 2015; Mulder 2007). Recent investigations explored the combined effects of performing MI during AO, suggesting that combined action observation and motor imagery (AOMI) engages the brain in a more extended way, compared to the two activities alone. Neuroimaging studies report that, AOMI engages largely overlapping networks involved in AO and MI alone, it exhibits distinctive neural signatures (Taube et al 2015). To account for this, in recent years, a ‘dual simulation hypothesis’ has been proposed, which suggests that sensorimotor representations evoked by AO and MI may be computed simultaneously and, according to their content and perspective, could either complement or compete for neural substrates underlying sensorimotor computation

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