Kinaesthetic illusion shapes the cortical plasticity evoked by action observation

Ambra Bisio, Monica Biggio, Laura Avanzino, Piero Ruggeri, Marco Bove

Research output: Contribution to journalArticle

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.

Original languageEnglish
JournalJournal of Physiology
DOIs
Publication statusPublished - Jan 1 2019

Fingerprint

Observation
Touch
Motor Cortex
Peripheral Nerves
Muscle Spindles
Proprioception
Transcranial Magnetic Stimulation
Vibration
Immobilization
Tendons
Cognition
Muscles

Keywords

  • action observation
  • movement illusion
  • primary motor cortex
  • proprioception
  • transcranial magnetic stimulation

ASJC Scopus subject areas

  • Physiology

Cite this

Kinaesthetic illusion shapes the cortical plasticity evoked by action observation. / Bisio, Ambra; Biggio, Monica; Avanzino, Laura; Ruggeri, Piero; Bove, Marco.

In: Journal of Physiology, 01.01.2019.

Research output: Contribution to journalArticle

@article{95ce59c841054c1da016b6af5edbaba6,
title = "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.",
keywords = "action observation, movement illusion, primary motor cortex, proprioception, transcranial magnetic stimulation",
author = "Ambra Bisio and Monica Biggio and Laura Avanzino and Piero Ruggeri and Marco Bove",
year = "2019",
month = "1",
day = "1",
doi = "10.1113/JP277799",
language = "English",
journal = "Journal of Physiology",
issn = "0022-3751",
publisher = "Wiley-Blackwell",

}

TY - JOUR

T1 - Kinaesthetic illusion shapes the cortical plasticity evoked by action observation

AU - Bisio, Ambra

AU - Biggio, Monica

AU - Avanzino, Laura

AU - Ruggeri, Piero

AU - Bove, Marco

PY - 2019/1/1

Y1 - 2019/1/1

N2 - 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.

AB - 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.

KW - action observation

KW - movement illusion

KW - primary motor cortex

KW - proprioception

KW - transcranial magnetic stimulation

UR - http://www.scopus.com/inward/record.url?scp=85066147862&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85066147862&partnerID=8YFLogxK

U2 - 10.1113/JP277799

DO - 10.1113/JP277799

M3 - Article

C2 - 31074046

AN - SCOPUS:85066147862

JO - Journal of Physiology

JF - Journal of Physiology

SN - 0022-3751

ER -