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Modulating motor resonance with paired associative stimulation: Neurophysiological and behavioral outcomes

Giacomo Guidali,Michela Picardi,Chiara Gramegna, Nadia Bolognini

CORTEX(2023)

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Abstract
In the human brain, paired associative stimulation (PAS), a non-invasive brain stimulation technique based on Hebbian learning principles, can be used to model motor resonance, the inner activation of an observer's motor system by action observation. Indeed, the newly developed mirror PAS (m-PAS) protocol, through the repeatedly pairing of transcranial magnetic stimulation (TMS) pulses over the primary motor cortex (M1) and visual stimuli depicting index-finger movements, allows the emergence of a new, atypical pattern of cortico-spinal excitability. In the present study, we performed two experiments to explore (a) the debated hemispheric lateralization of the action-observation network and (b) the behavioral after-effects of m-PAS, particularly concerning a core function of the MNS: automatic imitation.In Experiment 1, healthy participants underwent two sessions of m-PAS, delivered over the right and left M1. Before and after each m-PAS session, motor resonance was assessed by recording motor-evoked potentials induced by single-pulse TMS applied to the right M1 while observing contralateral (left) and ipsilateral (right) index-finger movements or static hands. In Experiment 2, participants performed an imitative compatibility task before and after the m-PAS targeting the right M1. Results showed that only m-PAS targeting the right hemisphere, non-dominant in right-handed people, induced the emergence of motor resonance for the conditioned movement, absent before the stimulation. This effect is not present when m-PAS target the M1 of the left hemisphere. Importantly, the protocol also affects behavior, modulating automatic imitation in a strictly somatotopic fashion (i.e., influencing the imitation of the conditioned finger movement). Overall, this evidence shows that the m-PAS can be used to drive new associations between the perception of actions and their corresponding motor programs, measurable both at a neurophysiological and behavioral level. At least for simple, not goal-directed, movements, the induction of motor resonance and automatic imitation effects are gov-erned by mototopic and somatotopic rules.(c) 2023 Elsevier Ltd. All rights reserved.
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Key words
Paired associative stimulation,Action observation,Transcranial magnetic stimulation,Imitation,Mirror neuron system,Plasticity
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