Boosting and consolidating the proprioceptive cortical aftereffect by combining tendon vibration and repetitive TMS over primary motor cortex

Perasso, Luisa; Avanzino, Laura; Lagravinese, Giovanna; Giannini, Alessandro; Faelli, Emanuela; Bisio, Ambra; Quartarone, Angelo; Rizzo, Vincenzo; Ruggeri, Piero; Bove, Marco

doi:10.1007/s10072-018-3606-9

Cited by 5 publications

(6 citation statements)

References 23 publications

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“…The discharge follows one-to-one the vibration cycles within a wide range and lasts as long as vibration continues (Burke et al 1976;Roll et al 1989). Neurophysiological and neuroimaging investigations demonstrated that muscle tendon vibration increased motor cortical activity in the area corresponding to the muscle antagonist to the vibrated muscle both during (Naito et al 1999;Siggelkow et al 1999;Mancheva et al 2017;Perasso et al 2019) and after (Steyvers et al 2003;Forner-Cordero et al 2008;Marconi et al 2008) the stimulation.…”

Section: Introductionmentioning

confidence: 97%

Kinaesthetic illusion shapes the cortical plasticity evoked by action observation

Bisio

Biggio

Avanzino

et al. 2019

The Journal of Physiology

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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.

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Section: Introductionmentioning

confidence: 97%

Kinaesthetic illusion shapes the cortical plasticity evoked by action observation

Bisio

Biggio

Avanzino

et al. 2019

The Journal of Physiology

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“…Regarding AO, the number of studies have shown increased motor cortex excitability as a result of the increased activity of the mirror neuron system that projects onto M1 (Bassolino et al., 2014; Cook et al., 2014; Iacoboni et al., 2009; Rizzolatti & Craighero, 2004), the effects of which appear as changes in movement kinematics (Avanzino et al., 2015; Bisio et al., 2010; Bove et al., 2009; Lagravinese et al., 2017). Concerning KI, it is known that once muscle spindles are activated (via endogenous mechanisms during movement execution or by exogenous mechanical vibration), the afferent sensory signals reach M1 and induce a significant increase in its excitability (Kito et al., 2006; Naito & Ehrsson, 2001; Naito et al., 1999; Perasso et al., 2019).…”

Section: Discussionmentioning

confidence: 99%

“…Myriad studies have focused on the possibility to modulate primary motor cortex (M1) excitability through external cortical (Nitsche et al., 2008; Siebner & Rothwell, 2003) and peripheral (Kito et al., 2006; Naito & Ehrsson, 2001; Naito et al., 1999; Perasso et al., 2019) stimulations, and also through cognitive techniques, such as action observation (Rizzolatti & Craighero, 2004) and motor imagery (Jeannerod, 2001). These stimulations can act acutely, leading to an instantaneous and transient augmentation of M1 activity (Fadiga et al., ,,1995, 1999; Naito et al., 1999), but they can also evoke long‐lasting changes (Bonassi et al., 2020; Chipchase et al., 2011; Lagravinese et al., 2017; Pascual‐Leone et al., 1995; Ridding et al., 2000; Schabrun et al., 2012; Ziemann et al., 2008).…”

Section: Introductionmentioning

confidence: 99%

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

Bisio

Biggio

Canepa

et al. 2021

Eur J of Neuroscience

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Action observation combined with proprioceptive stimulation able to induce a kinesthetic illusion of movement (AO‐KI) was shown to elicit a plastic increase in primary motor cortex (M1) excitability, with promising applications in rehabilitative interventions. Nevertheless, the known individual variability in response to combined stimulation protocols limits its application. The aim of this study was to examine whether a relationship exists between changes in M1 excitability during AO‐KI and the long‐lasting changes in M1 induced by AO‐KI. Fifteen volunteers received a conditioning protocol consisting in watching a video showing a thumb‐opposition movement and a simultaneous proprioceptive stimulation that evoked an illusory kinesthetic experience of their thumbs closing. M1 excitability was evaluated by means of single‐pulse transcranial magnetic stimulation before, DURING the conditioning protocol, and up to 60 min AFTER it was administered. M1 excitability significantly increased during AO‐KI with respect to a rest condition. Furthermore, AO‐KI induced a long‐lasting increase in M1 excitability up to 60 min after administration. Finally, a significant positive correlation appeared between M1 excitability changes during and after AO‐KI; that is, participants who were more responsive during AO‐KI showed greater motor cortical activity changes after it. These findings suggest that M1 response during AO‐KI can be considered a neurophysiological marker of individual responsiveness to the combined stimulation since it was predictive of its efficacy in inducing long‐lasting M1 increase excitability. This information would allow knowing in advance whether an individual will be a responder to AO‐KI.

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“…Recently Perasso et al (69) investigated the possibility to consolidate the cortical aftereffect of NMV by combining tendon vibration with a concomitant high-frequency 5-Hz rTMS protocol. The group found that this protocol induced a pattern of unbalanced M1 excitability between vibrated muscle and its antagonist with increased excitability of the agonist and decreased excitability of the antagonist muscle cortical areas, which persisted up to 30 min, demonstrating a synergic effect.…”

Section: Discussionmentioning

confidence: 99%

“…Even though NIBS and NMV are two conceptually different treatment strategies for visuospatial neglect, a review of the effects of both may provide more solid ground for an eventual study of the combined effects of the two of them for a more effective therapy of visuospatial neglect, as already pointed out in a very recently published study. 70…”

Section: Introductionmentioning

confidence: 99%

Noninvasive Brain Stimulation and Noninvasive Peripheral Stimulation for Neglect Syndrome Following Acquired Brain Injury

Lucente

Valls‐Solé

Murillo

et al. 2020

Neuromodulation: Technology at the Neural Interface

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Background: Hemispatial neglect is a frequent condition usually following non-dominant hemispheric brain injury. It strongly affects rehabilitation strategies and everyday life activities. It is associated with behavioural and cognitive disability with a strong impact on patient's life. Methods: We reviewed the published literature on the use of noninvasive brain stimulation, including repetitive transcranial magnetic stimulation (rTMS) and transcranial direct current stimulation (tDCS), and of non-invasive peripheral muscle stimulation, as therapeutic strategies for rehabilitation of neglect after acquired brain injury (ABI), such as in stroke or in traumatic injuries. The studies were grouped as controlled or uncontrolled studies in each stimulation technics. Results: Thirty-four studies were identified and 16 on rTMS, 10 on tDCS and 8 on vibration. All studies were conducted in adult patients who suffered a stroke, except for one that was conducted in a patient suffering traumatic ABI and another that was conducted in a patient with brain tumour. In spite of significant variability in treatment protocols, patients' features and assessment of neglect, improvement was reported in almost all studies with no side effects. Conclusion: Non-invasive brain stimulation and neuromuscular vibration are promising therapeutic neuromodulatory approaches for treatment of neglect. Further randomized-controlled studies are needed to corroborate their effectiveness as separate and combined techniques.

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Boosting and consolidating the proprioceptive cortical aftereffect by combining tendon vibration and repetitive TMS over primary motor cortex

Cited by 5 publications

References 23 publications

Kinaesthetic illusion shapes the cortical plasticity evoked by action observation

Kinaesthetic illusion shapes the cortical plasticity evoked by action observation

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

Noninvasive Brain Stimulation and Noninvasive Peripheral Stimulation for Neglect Syndrome Following Acquired Brain Injury

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