Abstract
Electroencephalography (EEG) of brain activity can be represented in terms of dynamically changing topographies (microstates). Notably, spontaneous brain activity recorded at rest can be characterized by four distinctive topographies. Despite their well-established role during resting state, their implication in the generation of motor behavior is debated. Evidence of such a functional role of spontaneous brain activity would provide support for the design of novel and sensitive biomarkers in neurological disorders. Here we examined whether and to what extent intrinsic brain activity contributes and plays a functional role during natural motor behaviors. For this we first extracted subject-specific EEG microstates and muscle synergies during reaching-and-grasping movements in healthy volunteers. We show that, in every subject, well-known resting-state microstates persist during movement execution with similar topographies and temporal characteristics, but are supplemented by novel task-related microstates. We then show that the subject-specific microstates’ dynamical organization correlates with the activation of muscle synergies and can be used to decode individual grasping movements with high accuracy. These findings provide first evidence that spontaneous brain activity encodes detailed information about motor control, offering as such the prospect of a novel tool for the definition of subject-specific biomarkers of brain plasticity and recovery in neuro-motor disorders.
Highlights
A large body of neuroimaging[1,2,3] and computational[4,5] research has revealed the complexity and richness of spontaneous brain activity measured at rest
The use of spontaneous brain activity as a biomarker of recovery mechanisms and neural deficits in neuro-motor disorders is contingent on the demonstration that: 1) this intrinsic activity plays a functional role in motor behaviors, and 2) that this relation with sensory-motor tasks can be extracted in each subject independently
We introduced a multi-modal experimental framework employing high-density EEG and muscle synergies analysis to uncover the functional role of spontaneous brain activity during the execution of volitional arm and hand movements
Summary
A large body of neuroimaging[1,2,3] and computational[4,5] research has revealed the complexity and richness of spontaneous brain activity measured at rest. Highlighting a functional role of the resting-state activity would be of great clinical value, potentially providing novel, rich, and sensitive biomarkers for neurological disorders, which impair patients’ ability to perform sensory-motor tasks[8]. These biomarkers could maximize therapeutic effects by informing personalization of therapy selection, timing, and duration[9]. The use of spontaneous brain activity as a biomarker of recovery mechanisms and neural deficits in neuro-motor disorders is contingent on the demonstration that: 1) this intrinsic activity plays a functional role in motor behaviors, and 2) that this relation with sensory-motor tasks can be extracted in each subject independently. Cortical motor neuron activity seems to encode the recruitment of motor primitives in the form of spatiotemporal muscular and kinematic synergies[26,27,28]
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