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Deciphering the functional role of spatial and temporal muscle synergies in whole-body movements.

ABSTRACT: Voluntary movement is hypothesized to rely on a limited number of muscle synergies, the recruitment of which translates task goals into effective muscle activity. In this study, we investigated how to analytically characterize the functional role of different types of muscle synergies in task performance. To this end, we recorded a comprehensive dataset of muscle activity during a variety of whole-body pointing movements. We decomposed the electromyographic (EMG) signals using a space-by-time modularity model which encompasses the main types of synergies. We then used a task decoding and information theoretic analysis to probe the role of each synergy by mapping it to specific task features. We found that the temporal and spatial aspects of the movements were encoded by different temporal and spatial muscle synergies, respectively, consistent with the intuition that there should a correspondence between major attributes of movement and major features of synergies. This approach led to the development of a novel computational method for comparing muscle synergies from different participants according to their functional role. This functional similarity analysis yielded a small set of temporal and spatial synergies that describes the main features of whole-body reaching movements.

SUBMITTER: Delis I

PROVIDER: S-EPMC5976658 | biostudies-literature | 2018 May

REPOSITORIES: biostudies-literature

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Deciphering the functional role of spatial and temporal muscle synergies in whole-body movements.

Delis Ioannis I Hilt Pauline M PM Pozzo Thierry T Panzeri Stefano S Berret Bastien B

Scientific reports 20180530 1

Voluntary movement is hypothesized to rely on a limited number of muscle synergies, the recruitment of which translates task goals into effective muscle activity. In this study, we investigated how to analytically characterize the functional role of different types of muscle synergies in task performance. To this end, we recorded a comprehensive dataset of muscle activity during a variety of whole-body pointing movements. We decomposed the electromyographic (EMG) signals using a space-by-time mo ...[more]

PMID: 29849101

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Project description:Key pointsIt is theorized that the nervous system controls groups of muscles together as functional units, or 'synergies', resulting in correlated electromyographic (EMG) signals among muscles. However, such correlation does not necessarily imply group-level neural control. Oscillatory synchronization (coherence) among EMG signals implies neural coupling, but it is not clear how this relates to control of muscle synergies. EMG was recorded from seven arm muscles of 10 adult participants rotating an upper limb ergometer, and EMG-EMG coherence, EMG amplitude correlations and their relationship with each other were characterized. A novel method to derive multi-muscle synergies from EMG-EMG coherence is presented and these are compared with classically defined synergies. Coherent alpha-band (8-16 Hz) drive was strongest among muscles whose gross activity levels are well correlated within a given task. The cross-muscle distribution and temporal modulation of coherent alpha-band drive suggests a possible role in the neural coordination/monitoring of synergies.AbstractDuring movement, groups of muscles may be controlled together by the nervous system as an adaptable functional entity, or 'synergy'. The rules governing when (or if) this occurs during voluntary behaviour in humans are not well understood, at least in part because synergies are usually defined by correlated patterns of muscle activity without regard for the underlying structure of their neural control. In this study, we investigated the extent to which comodulation of muscle output (i.e. correlation of electromyographic (EMG) amplitudes) implies that muscles share intermuscular neural input (assessed via EMG-EMG coherence analysis). We first examined this relationship among pairs of upper limb muscles engaged in an arm cycling task. We then applied a novel multidimensional EMG-EMG coherence analysis allowing synergies to be characterized on the basis of shared neural drive. We found that alpha-band coherence (8-16 Hz) is related to the degree to which overall muscle activity levels correlate over time. The extension of this coherence analysis to describe the cross-muscle distribution and temporal modulation of alpha-band drive revealed a close match to the temporal and structural features of traditionally defined muscle synergies. Interestingly, the coherence-derived neural drive was inversely associated with, and preceded, changes in EMG amplitudes by ∼200 ms. Our novel characterization of how alpha-band neural drive is dynamically distributed among muscles is a fundamental step forward in understanding the neural origins and correlates of muscle synergies.

Project description:Understanding the impact of weightlessness on human behavior during the forthcoming long-term space missions is of critical importance, especially when considering the efficiency of goal-directed movements in these unusual environments. Several studies provided a large set of evidence that gravity is taken into account during the planning stage of arm reaching movements to optimally anticipate its consequence upon the moving limbs. However, less is known about sensorimotor changes required to face weightless environments when individuals have to perform fast and accurate goal-directed actions with whole-body displacement. We thus aimed at characterizing kinematic features of whole-body reaching movements in microgravity, involving high spatiotemporal constraints of execution, to question whether and how humans are able to maintain the performance of a functional behavior in the standards of normogravity execution. Seven participants were asked to reach as fast and as accurately as possible visual targets while standing during microgravity episodes in parabolic flight. Small and large targets were presented either close or far from the participants (requiring, in the latter case, additional whole-body displacement). Results reported that participants successfully performed the reaching task with general temporal features of movement (e.g., movement speed) close to land observations. However, our analyses also demonstrated substantial kinematic changes related to the temporal structure of focal movement and the postural strategy to successfully perform -constrained- whole-body reaching movements in microgravity. These immediate reorganizations are likely achieved by rapidly taking into account the absence of gravity in motor preparation and execution (presumably from cues about body limbs unweighting). Specifically, when compared to normogravity, the arm deceleration phase substantially increased. Furthermore, greater whole-body forward displacements due to smaller trunk flexions occurred when reaching far targets in microgravity. Remarkably, these changes of focal kinematics and postural strategy appear close to those previously reported when participants performed the same task underwater with neutral buoyancy applied to body limbs. Overall, these novel findings reveal that humans are able to maintain the performance of functional goal-directed whole-body actions in weightlessness by successfully managing spatiotemporal constraints of execution in this unusual environment.

Project description:Reductions in skeletal muscle mass and function are often reported in patients with cancer-associated weight loss and are associated with reduced quality of life, impaired treatment tolerance, and increased mortality. Although cellular changes, including altered mitochondrial function, have been reported in animals, such changes have been incompletely characterized in humans with cancer. Whole body and skeletal muscle physical function, skeletal muscle mitochondrial function, and whole body protein turnover were assessed in eight patients with cancer-associated weight loss (10.1 ± 4.2% body weight over 6-12 mo) and 19 age-, sex-, and body mass index (BMI)-matched healthy controls to characterize skeletal muscle changes at the whole body, muscle, and cellular level. Potential pathways involved in cancer-induced alterations in metabolism and mitochondrial function were explored by interrogating skeletal muscle and plasma metabolomes. Despite similar lean mass compared with control participants, patients with cancer exhibited reduced habitual physical activity (57% fewer daily steps), cardiorespiratory fitness [22% lower V̇o2peak (mL/kg/min)] and leg strength (35% lower isokinetic knee extensor strength), and greater leg neuromuscular fatigue (36% greater decline in knee extensor torque). Concomitant with these functional declines, patients with cancer had lower mitochondrial oxidative capacity [25% lower State 3 O2 flux (pmol/s/mg tissue)] and ATP production [23% lower State 3 ATP production (pmol/s/mg tissue)] and alterations in phospholipid metabolite profiles indicative of mitochondrial abnormalities. Whole body protein turnover was unchanged. These findings demonstrate mitochondrial abnormalities concomitant with whole body and skeletal muscle functional derangements associated with human cancer, supporting future work studying the role of mitochondria in the muscle deficits associated with cancer.NEW & NOTEWORTHY To our knowledge, this is the first study to suggest that skeletal muscle mitochondrial deficits are associated with cancer-associated weight loss in humans. Mitochondrial deficits were concurrent with reductions in whole body and skeletal muscle functional capacity. Whether mitochondrial deficits are causal or secondary to cancer-associated weight loss and functional deficits remains to be determined, but this study supports further exploration of mitochondria as a driver of cancer-associated losses in muscle mass and function.

Dataset Information

Deciphering the functional role of spatial and temporal muscle synergies in whole-body movements.

Publications

Deciphering the functional role of spatial and temporal muscle synergies in whole-body movements.

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