Paired Associative Stimulation drives the emergence of motor resonance

Abstract

Background: Associative plasticity, the neurophysiological bases of Hebbian learning, has been implied in the formation of the association between sensory and motor representations of actions in the Mirror Neuron System; however, such inductor role still needs empirical support. Objective/hypothesis: We have assessed whether Paired Associative Stimulation (PAS), known to activate Hebbian associative plasticity, can induce the formation of atypical (absent in normal conditions), visuomotor associations, reshaping motor resonance. Methods: Healthy participants underwent a novel PAS protocol (mirror-PAS, m-PAS), during which they were exposed to repeated pairings of transcranial magnetic stimulation (TMS) applied over the right primary motor cortex (M1), time-locked with the view of index-finger movements of the right (ipsilateral) hand. In a first experiment, the inter-stimulus interval (ISI) between visual-action stimuli and TMS pulses was varied. 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, during the observation of both contralateral (left) and ipsilateral (right) index-finger movements. In the second experiment, the specificity of the m-PAS was assessed by presenting a visual stimulus depicting a non-biological movement.Results: Before m-PAS, the facilitation of corticospinal excitability occurred only during the view of contralateral (with respect to the TMS side) index-finger movements. The m-PAS induced new ipsilateral motor resonance responses, indexed by atypical facilitation of corticospinal excitability by the view of ipsilateral hand movements. This effect occurred only if the associative stimulation followed the chronometry of motor control (ISI of 25 ms) and if the visual stimulus of the m-PAS depicts a biological movement (human hand action). Conclusions: The present findings provide the first empirical evidence that Hebbian learning induced by a PAS protocol shapes the visual-motor matching properties of the human Mirror Neuron System.

What happened to mirror neurons?

“…Experiments that were designed to isolate the kind of learning involved in mirror neuron development have suggested that sensorimotor learning is crucial (Catmur et al, 2011;de Klerk et al, 2015;Press et al, 2012a;Fitzgibbon et al, 2016;Guidali et al, 2020;Wiggett et al, 2012). For example, replicating and extending earlier work with a similar design (e.g.…”

“…In the last decade, more evidence has emerged that learning plays an important role in the development of mirror neurons (Brunsdon et al, 2019;Catmur et al, 2011;Copete et al, 2016;de Klerk et al, 2015;Fitzgibbon et al, 2016;Furukawa et al, 2017;Guidali et al, 2020;Hou et al, 2017;McKyton et al, 2017;Orlandi et al, 2017;Press et al, 2012a;Wiggett et al, 2012;Zazio et al, 2019).…”

What Happened to Mirror Neurons?

“…In the past decade, more evidence has emerged that learning plays an important role in the development of mirror neurons ( Brunsdon et al, 2020 ; Catmur et al, 2011 ; Copete et al, 2016 ; de Klerk et al, 2015 ; Fitzgibbon et al, 2016 ; Furukawa et al, 2017 ; Guidali et al, 2020 ; Hou et al, 2017 ; McKyton et al, 2018 ; Orlandi et al, 2017 ; Press et al, 2012 ; Wiggett et al, 2012 ; Zazio et al, 2019 ). Some of the recent studies have reported greater activity in mirror-neuron brain areas in pianists and dancers than in people who lack such expertise during observation of musical performance and dance, respectively ( Furukawa et al, 2017 ; Hou et al, 2017 ; Orlandi et al, 2017 ).…”

Modulating Frontal Networks’ Timing-Dependent-Like Plasticity With Paired Associative Stimulation Protocols: Recent Advances and Future Perspectives

“…By varying the inter-stimulus interval (ISI) between these stimulations, PAS protocols can affect synaptic plasticity, inducing long-term potentiation (LTP)-like and depression (LTD)-like after-effects on cortical excitability [i.e., Spike-timing-dependent plasticity (STDP); e.g., Caporale and Dan, 2008] in the stimulated cortical area or circuit (e.g., Stefan et al, 2000;Wolters et al, 2003). Over the last 2 decades, PAS literature moved from the widely replicated, classical protocol, pairing electric stimuli with M1-TMS (i.e., M1-PAS), to more complex protocols targeting sensory and crossmodal networks (e.g., Wolters et al, 2005;Schecklmann et al, 2011;Suppa et al, 2013Suppa et al, , 2015Sowman et al, 2014;Ranieri et al, 2019;Zazio et al, 2019;Guidali et al, 2020). Overall, these peripheral-cortical protocols proved to be robust and flexible tools to non-invasively investigate and interact with the plastic properties of sensorimotor networks in humans (for a review, see: Carson and Kennedy, 2013;Suppa et al, 2017).…”