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Neuronal Correlates of Functional Coupling between Reach- and Grasp-Related Components of Muscle Activity.

ABSTRACT: 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.

SUBMITTER: Geed S

PROVIDER: S-EPMC5318413 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Neuronal Correlates of Functional Coupling between Reach- and Grasp-Related Components of Muscle Activity.

Geed Shashwati S McCurdy Martha L ML van Kan Peter L E PL

Frontiers in neural circuits 20170221

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), tha ...[more]

PMID: 28270752

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Project description:PurposeRegaining hand function has been identified as the highest priority for persons with tetraplegia. In many patients, finger flexion can be restored with a tendon transfer of extensor carpi radialis longus to flexor digitorum profundus (FDP). In the absence of intrinsic function, this results in a roll-up finger movement, which tends to push large objects out of grasp. To enable patients to grasp objects of varying sizes, a functional grasp is required that has a larger excursion of fingertip-to-palm distance than can be supplied without intrinsic function. The aim of this study was to quantify the role of intrinsic muscle force in creating a functional grasp.MethodsFinger kinematics during grasp were measured on 5 cadaveric hands. To simulate finger flexion, the FDP was activated by a motor and intrinsic muscles were loaded at various levels (0, 125, 250, 375, or 500 g). Finger movement was characterized by the order of metacarpophalangeal, proximal interphalangeal, and distal interphalangeal joint flexion and by the maximal fingertip-to-palm distance during finger closure.ResultsWithout any intrinsic muscle contribution (0-g load), FDP activation resulted in flexion of all 3 joints, whereby flexion began at the proximal interphalangeal joint, followed by the distal interphalangeal joint, and then the metacarpophalangeal joint. With increasing intrinsic muscle load, finger flexion was initiated at the metacarpophalangeal joint, followed by the proximal interphalangeal and distal interphalangeal joints. This altered joint flexion order resulted in a larger maximal fingertip-to-palm distance during finger flexion. The difference between the 2 extreme conditions (0 g vs 500 g of intrinsic muscle load) was 19 mm.ConclusionsThese findings demonstrate that simultaneous activation of the FDP and the intrinsic muscles results in an apparently more functional hand closing compared with FDP activation alone because of altered kinematics and larger fingertip-to-palm distances.Clinical relevanceThese findings suggest that intrinsic muscle balancing during reconstruction of grasp in tetraplegic patients may improve function.

Dataset Information

Neuronal Correlates of Functional Coupling between Reach- and Grasp-Related Components of Muscle Activity.

Publications

Neuronal Correlates of Functional Coupling between Reach- and Grasp-Related Components of Muscle Activity.

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