Predicting and coding sound into action translation in spinal cord injured people

Motor activation in response to perception of action‐related stimuli may depend on a resonance mechanism subserving action understanding. The extent to which this mechanism is innate or learned from sensorimotor experience is still unclear. Here, we recorded EEG while people with paraplegia or tetra...

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Published in:The European journal of neuroscience Vol. 59; no. 5; pp. 1029 - 1046
Main Authors: Grisoni, Luigi, Piperno, Giulio, Moreau, Quentin, Molinari, Marco, Scivoletto, Giorgio, Aglioti, Salvatore Maria
Format: Journal Article
Language:English
Published: France Wiley Subscription Services, Inc 01.03.2024
Subjects:
action understanding
bodily representations
Correlation analysis
Data acquisition
EEG
EEG prediction potential‐ mismatch‐negativity
Lesions
motor resonance
Neural coding
Paralysis
Paraplegia
Perception
Sensorimotor system
Sound
Spinal cord
Spinal cord injuries
action understanding
bodily representations
EEG prediction potential- mismatch-negativity
motor resonance
ISSN:0953-816X, 1460-9568, 1460-9568
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Summary:Motor activation in response to perception of action‐related stimuli may depend on a resonance mechanism subserving action understanding. The extent to which this mechanism is innate or learned from sensorimotor experience is still unclear. Here, we recorded EEG while people with paraplegia or tetraplegia consequent to spinal cord injury (SCI) and healthy control participants were presented with action sounds produced by body parts (mouth, hands or feet) that were or were not affected by SCI. Non‐action sounds were used as further control. We observed reduced brain activation in subjects affected by SCI at both pre‐ and post‐stimulus latencies specifically for those actions whose effector was disconnected by the spinal lesion (i.e., hand sound for tetraplegia and leg sound for both paraplegia and tetraplegia). Correlation analyses showed that these modulations were functionally linked with the chronicity of the lesion, indicating that the longer the time the lesion‐ EEG data acquisition interval and/or the more the lesion occurred at a young age, the weaker was the cortical activity in response to these action sounds. Tellingly, source estimations confirmed that these modulations originated from a deficit in the motor resonance mechanism, by showing diminished activity in premotor (during prediction and perception) and near the primary motor (during perception) areas. Such dissociation along the cortical hierarchy is consistent with both previous reports in healthy subjects and with hierarchical predictive coding accounts. Overall, these data expand on the notion that sensorimotor experience maintains the cortical representations relevant to anticipate and perceive action‐related stimuli. We run a mismatch‐negativity based EEG study on people with acquired paraplegia or tetraplegia and healthy controls, to look for possible alteration on prediction and perception processes of action‐related sounds following a spinal lesion. We found reduced motor resonance for action sound stimuli related to the effectors disconnected by the lesion. Source estimations further suggested that the patients decrease in activity within the motor areas was a contributing factor to these alterations.
Bibliography:Funding information
Edited by: Francisco Alvarez
This work was supported by Italian Ministry of University and Research to SMA (PRIN grant, Progetti di Ricerca di Rilevante Interesse Nazionale, Edit. 2017, Prot. 2017N7WCLP).
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ISSN:0953-816X
1460-9568
1460-9568
DOI:10.1111/ejn.16258