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Motor "dexterity"?: Evidence that left hemisphere lateralization of motor circuit connectivity is associated with better motor performance in children.

ABSTRACT: Motor control relies on well-established motor circuits, which are critical for typical child development. Although many imaging studies have examined task activation during motor performance, none have examined the relationship between functional intrinsic connectivity and motor ability. The current study investigated the relationship between resting state functional connectivity within the motor network and motor performance assessment outside of the scanner in 40 typically developing right-handed children. Better motor performance correlated with greater left-lateralized (mean left hemisphere-mean right hemisphere) motor circuit connectivity. Speed, rhythmicity, and control of movements were associated with connectivity within different individual region pairs: faster speed was associated with more left-lateralized putamen-thalamus connectivity, less overflow with more left-lateralized supplementary motor-primary motor connectivity, and less dysrhythmia with more left-lateralized supplementary motor-anterior cerebellar connectivity. These findings suggest that for right-handed children, superior motor development depends on the establishment of left-hemisphere dominance in intrinsic motor network connectivity.

SUBMITTER: Barber AD

PROVIDER: S-EPMC3236793 | biostudies-literature | 2012 Jan

REPOSITORIES: biostudies-literature

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Motor "dexterity"?: Evidence that left hemisphere lateralization of motor circuit connectivity is associated with better motor performance in children.

Barber Anita D AD Srinivasan Priti P Joel Suresh E SE Caffo Brian S BS Pekar James J JJ Mostofsky Stewart H SH

Cerebral cortex (New York, N.Y. : 1991) 20110525 1

Motor control relies on well-established motor circuits, which are critical for typical child development. Although many imaging studies have examined task activation during motor performance, none have examined the relationship between functional intrinsic connectivity and motor ability. The current study investigated the relationship between resting state functional connectivity within the motor network and motor performance assessment outside of the scanner in 40 typically developing right-ha ...[more]

PMID: 21613469

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Project description:Depending on the lesion site, a stroke typically affects various aspects of cognitive control. While executing a task, the performance monitoring system constantly compares an intended action plan with the executed action and thereby registers inaccurate actions in case of any mismatch. When errors occur, the performance monitoring system signals the need for more cognitive control, which is most efficient when the subject notices errors rather than processing them subconsciously. The current study aimed to investigate performance monitoring and error detection in a large sample of patients with left hemisphere (LH) stroke. In addition to clinical and neuropsychological tests, 24 LH stroke patients and 32 healthy age-matched controls performed a Go/Nogo task with simultaneous electroencephalography (EEG) measurements. This set-up enabled us to compare performance monitoring at the behavioral and the neural level. EEG data were analyzed using event-related potentials [ERPs; e.g., the error-related negativity (Ne/ERN) and error positivity (Pe)] and additionally more sensitive whole-brain multivariate pattern classification analyses (MVPA). We hypothesized that LH stroke patients would show behavioural deficits in error detection when compared to healthy controls, mirrored by differences in neural signals, in particular reflected in the Pe component. Interestingly, despite clinically relevant cognitive deficits (e.g., aphasia and apraxia) including executive dysfunction (trail making test), we did not observe any behavioral impairments related to performance monitoring and error processing in the current LH stroke patients. Patients also showed similar results for Ne/ERN and Pe components, compared to the control group, and a highly similar prediction of errors from multivariate signals. ERP abnormalities during stimulus processing (i.e., N2 and P3) demonstrated the specificity of these findings in the current LH stroke patients. In contrast to previous studies, by employing a relatively large patient sample, a well-controlled experimental paradigm with a standardized error signaling procedure, and advanced data analysis, we were able to show that performance monitoring (of simple actions) is a preserved cognitive control function in LH stroke patients that might constitute a useful resource in rehabilitative therapies for re-learning impeded functions.

Project description:Increasing evidence indicates that focal lesions following stroke cause alterations in connectivity among functional brain networks. Functional connectivity between hemispheres has been shown to be particularly critical for predicting stroke-related behavioral deficits and recovery of motor function and attention. Much less is known, however, about the relevance of interhemispheric functional connectivity for cognitive abilities like praxis that rely on strongly lateralized brain networks. In the current study, we examine correlations between symptoms of apraxia-a disorder of skilled action that cannot be attributed to lower-level sensory or motor impairments-and spontaneous, resting brain activity in functional MRI in chronic left hemisphere stroke patients and neurologically-intact control participants. Using a data-driven approach, we identified 32 regions-of-interest in which pairwise functional connectivity correlated with two distinct measures of apraxia, even when controlling for age, head motion, lesion volume, and other artifacts: overall ability to pantomime the typical use of a tool, and disproportionate difficulty pantomiming the use of tools associated with different, competing use and grasp-to-move actions (e.g., setting a kitchen timer versus picking it up). Better performance on both measures correlated with stronger interhemispheric functional connectivity. Relevant regions in the right hemisphere were often homologous to left hemisphere areas associated with tool use and action. Additionally, relative to overall pantomime accuracy, disproportionate difficulty pantomiming the use of tools associated with competing use and grasp actions was associated with weakened functional connectivity among a more strongly left-lateralized and peri-Sylvian set of brain regions. Finally, patient performance on both measures of apraxia was best predicted by a model that incorporated information about lesion location and functional connectivity, and functional connectivity continued to explain unique variance in behavior even after accounting for lesion loci. These results indicate that interhemispheric functional connectivity is relevant even for a strongly lateralized cognitive ability like praxis and emphasize the importance of the right hemisphere in skilled action.

Dataset Information

Motor "dexterity"?: Evidence that left hemisphere lateralization of motor circuit connectivity is associated with better motor performance in children.

Publications

Motor "dexterity"?: Evidence that left hemisphere lateralization of motor circuit connectivity is associated with better motor performance in children.

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