Kinaesthetic illusion shapes the cortical plasticity evoked by action observation

Abstract

Key points The combination of action observation (AO) and a peripheral nerve stimulation has been shown to induce plasticity in the primary motor cortex (M1). However, using peripheral nerve stimulation little is known about the specificity of the sensory inputs. The current study, using muscle tendon vibration to stimulate muscle spindles and transcranial magnetic stimulation to assess M1 excitability, investigated whether a proprioceptive stimulation leading to a kinaesthetic illusion of movement (KI) was able to evoke M1 plasticity when combined with AO. M1 excitability increased immediately and up to 60 min after AO‐KI stimulation as a function of the vividness of the perceived illusion, and only when the movement directions of AO and KI were congruent. Tactile stimulation coupled with AO and KI alone were not sufficient to induce M1 plasticity. This methodology might be proposed to subjects during a period of immobilization to promote M1 activity without requiring any voluntary movement. Abstract Physical practice is crucial to evoke cortical plasticity, but motor cognition techniques, such as action observation (AO), have shown their potentiality in promoting it when associated with peripheral afferent inputs, without the need of performing a movement. Here we investigated whether the combination of AO and a proprioceptive stimulation, able to evoke a kinaesthetic illusion of movement (KI), induced plasticity in the primary motor cortex (M1). In the main experiment, the role of congruency between the observed action and the illusory movement was explored together with the importance of the specificity of the sensory input modality (proprioceptive vs. tactile stimulation) to induce plasticity in M1. Further, a control experiment was carried out to assess the role of the mere kinaesthetic illusion on M1 excitability. Results showed that the combination of AO and KI evoked plasticity in M1, with an increase of the excitability immediately and up to 60 min after the conditioning protocol (P always <0.05). Notably, a significant increase in M1 excitability occurred only when the directions of the observed and illusory movements were congruent. Further, a significant positive linear relationship was found between the amount of M1 excitability increase and the vividness of the perceived illusion (P = 0.03). Finally, the tactile stimulation coupled with AO was not sufficient to induce changes in M1 excitability as well as the KI alone. All these findings indicate the importance of combining different sensory input signals to induce plasticity in M1, and that proprioception is the most suitable sensory modality to allow it.

Primary motor cortex excitability as a marker of plasticity in a stimulation protocol combining action observation and kinesthetic illusion of movement

“…The results of the Main experiment showed that M1 excitability significantly increased during AO‐KI with respect to a rest condition. We confirmed our previous finding concerning the efficacy of AO‐KI to evoke a long‐lasing increase in M1 excitability (Bisio et al., 2019). Furthermore, a significant positive relationship was found between MEP amplitude changes during AO‐KI with respect to rest and the long‐term changes in the motor cortical activity obtained after AO‐KI administration.…”

“…In a previous study (Bisio et al, 2019), we investigated longlasting changes in M1 activity following AO-KI, and we observed an increase in M1 excitability, lasting up to 1 hr after AO-KI was administered when AO and KI went in congruent directions. Here, we confirm that M1 excitability is significantly enhanced after participants' exposure to AO-KI.…”

“…The sample size was estimated using G*Power software, based on a desired power of 0.80, alpha of 0.05, and a medium effect size of 0.32. The effect size was assessed on the basis of our group's previous neurophysiological and behavioral studies (Bisio et al, 2017(Bisio et al, , 2019Bisio, Avanzino, Gueugneau, et al, 2015;Bisio, Avanzino, Lagravinese, et al, 2015) that combined AO with peripheral stimulations. The results of this power analysis indicated 15 participants as an appropriate sample size.…”

“…The latter was obtained as follows: RC slope values in POST epochs were normalized to their baseline values (PRE), and the percent changes with respect to PRE were calculated as (Slope POST /Slope PRE )*100 for each subject, at each evaluation time epoch. These values were averaged across evaluation time epochs, and the mean percent change in RC slope values was computed for each subject (Bisio et al, 2019).…”

“…Scientific literature on cortical plasticity has produced several stimulation protocols that can induce long-term changes in the motor cortical areas (Cirillo et al, 2017;Huang et al, 2017;Ziemann et al, 2008). Some of these protocols have combined multiple stimuli to evoke plastic changes in the motor cortex exploiting the mechanisms of associative plasticity (Bisio et al, 2017(Bisio et al, , 2018(Bisio et al, , 2019Bisio, Avanzino, Gueugneau, et al, 2015;Bonassi et al, 2017;Kaneko et al, 2014;Rizzo et al, 2009;Stefan et al, 2000). Examples come from studies that associate cognitive techniques and peripheral signals.…”