Dataset Information

Relations between infants' emerging reach-grasp competence and event-related desynchronization in EEG.

ABSTRACT: Recent reports of similar patterns of brain electrical activity (electroencephalogram: EEG) during action execution and observation, recorded from scalp locations over motor-related regions in infants and adults, have raised the possibility that two foundational abilities--controlling one's own intentional actions and perceiving others' actions--may be integrally related during ontogeny. However, to our knowledge, there are no published reports of the relations between developments in motor skill (i.e. recording actual motor skill performance) and EEG during both action execution and action observation. In the present study we collected EEG from 21 9-month-olds who were given opportunities to reach for toys and who also observed an experimenter reach for toys. Event-related desynchronization (ERD) was computed from the EEG during the reaching events. We assessed infants' reaching-grasping competence, including reach latency, errors, preshaping of the hand, and bimanual reaches, and found that desynchronization recorded in scalp electrodes over motor-related regions during action observation was associated with action competence during execution. Infants who were more competent reachers, compared to less competent reachers, exhibited greater ERD while observing reaching-grasping. These results provide initial evidence for an early emerging neural system integrating one's own actions with the perception of others' actions.

SUBMITTER: Cannon EN

PROVIDER: S-EPMC7470427 | biostudies-literature | 2016 Jan

REPOSITORIES: biostudies-literature

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Relations between infants' emerging reach-grasp competence and event-related desynchronization in EEG.

Cannon Erin N EN Simpson Elizabeth A EA Fox Nathan A NA Vanderwert Ross E RE Woodward Amanda L AL Ferrari Pier F PF

Developmental science 20150305 1

Recent reports of similar patterns of brain electrical activity (electroencephalogram: EEG) during action execution and observation, recorded from scalp locations over motor-related regions in infants and adults, have raised the possibility that two foundational abilities--controlling one's own intentional actions and perceiving others' actions--may be integrally related during ontogeny. However, to our knowledge, there are no published reports of the relations between developments in motor skil ...[more]

PMID: 25754667

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Project description:Coordinated reach-to-grasp movements require precise spatiotemporal synchrony between proximal forelimb muscles (shoulder, elbow) that transport the hand toward a target during reach, and distal muscles (wrist, digit) that simultaneously preshape and orient the hand for grasp. The precise mechanisms through which the redundant neuromuscular circuitry coordinates reach with grasp, however, remain unclear. Recently, Geed and Van Kan (2016) demonstrated, using exploratory factor analysis (EFA), that limited numbers of global, template-like transport/preshape- and grasp-related muscle components underlie the complexity and variability of intramuscular electromyograms (EMGs) of up to 21 distal and proximal muscles recorded while monkeys performed reach-to-grasp tasks. Importantly, transport/preshape- and grasp-related muscle components showed invariant spatiotemporal coupling, which provides a potential mechanism for coordinating forelimb muscles during reach-to-grasp movements. In the present study, we tested whether ensemble discharges of forelimb neurons in the cerebellar nucleus interpositus (NI) and its target, the magnocellular red nucleus (RNm), a source of rubrospinal fibers, function as neuronal correlates of the transport/preshape- and grasp-related muscle components we identified. EFA applied to single-unit discharges of populations of NI and RNm neurons recorded while the same monkeys that were used previously performed the same reach-to-grasp tasks, revealed neuronal components in the ensemble discharges of both NI and RNm neuronal populations with characteristics broadly similar to muscle components. Subsets of NI and RNm neuronal components were strongly and significantly crosscorrelated with subsets of muscle components, suggesting that similar functional units of reach-to-grasp behavior are expressed by NI and RNm neuronal populations and forelimb muscles. Importantly, like transport/preshape- and grasp-related muscle components, their NI and RNm neuronal correlates showed invariant spatiotemporal coupling. Clinical and lesion studies have reported disruption of coupling between reach and grasp following cerebellar damage; the present results expand on those studies by identifying a neuronal mechanism that may underlie cerebellar contributions to spatiotemporal coordination of distal and proximal limb muscles during reaching to grasp. We conclude that finding similar functional units of behavior expressed at multiple levels of information processing along interposito-rubrospinal pathways and forelimb muscles supports the hypothesis that functionally related populations of NI and RNm neurons act synergistically in the control of complex coordinated motor behaviors.

Project description:This study applied a comprehensive electroencephalography (EEG) analysis for movement-related cortical potentials (MRCPs) and event-related desynchronization (ERD) in order to understand movement-related brain activity changes during movement preparation and execution stage of unilateral wrist extension. Thirty-four healthy subjects completed two event-related potential tests in the same sequence. Unilateral wrist extension was involved in both tests as the movement task. Instruction Response Movement (IRM) was a brisk movement response task with visual "go" signal, while Cued Instruction Response Movement (CIRM) added a visual cue contenting the direction information to create a prolonged motor preparation stage. Recorded EEG data were segmented and averaged to show time domain changes and then transformed into time-frequency mapping to show the time-frequency changes. All components were calculated and compared among C3, Cz, and C4 locations. The motor potential appeared bilaterally in both tests' movement execution stages, and Cz had the largest peak value among the investigated locations (p < 0.01). In CIRM, a contingent negative variation (CNV) component presented bilaterally during the movement preparation stage with the largest amplitude at Cz. ERD of the mu rhythm (mu ERD) presented bilateral sensorimotor cortices during movement execution stages in both tests and was the smallest at Cz among the investigated locations. In the movement preparation stage of CIRM, mu ERD presented mainly in the contralateral sensory motor cortex area (C3 and C4 for right and left wrist movements, respectively) and showed significant differences between different locations. EEG changes in the time and time-frequency domains showed different topographical features. Movement execution was controlled bilaterally, while movement preparation was controlled mainly by contralateral sensorimotor cortices. Mu ERD was found to have stronger contra-lateralization features in the movement preparation stage and might be a better indicator for detecting movement intentions. This information could be helpful and might provide comprehensive information for studying movement disorders (such as those in post-stroke hemiplegic patients) or for facilitating the development of neuro-rehabilitation engineering technology such as brain computer interface.

Dataset Information

Relations between infants' emerging reach-grasp competence and event-related desynchronization in EEG.

Publications

Relations between infants' emerging reach-grasp competence and event-related desynchronization in EEG.

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