Voluntary and Reactive Recruitment of Locomotor Muscle Synergies during Perturbed Walking

The Wallace H. Coulter Department of Biomedical Engineering at Georgia Tech and Emory University, Atlanta, Georgia 30322-0535, USA.
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience (Impact Factor: 6.34). 08/2012; 32(35):12237-50. DOI: 10.1523/JNEUROSCI.6344-11.2012
Source: PubMed


The modular control of muscles in groups, often referred to as muscle synergies, has been proposed to provide a motor repertoire of actions for the robust control of movement. However, it is not clear whether muscle synergies identified in one task are also recruited by different neural pathways subserving other motor behaviors. We tested the hypothesis that voluntary and reactive modifications to walking in humans result from the recruitment of locomotor muscle synergies. We recorded the activity of 16 muscles in the right leg as subjects walked a 7.5 m path at two different speeds. To elicit a second motor behavior, midway through the path we imposed ramp and hold translation perturbations of the support surface in each of four cardinal directions. Variations in the temporal recruitment of locomotor muscle synergies could account for cycle-by-cycle variations in muscle activity across strides. Locomotor muscle synergies were also recruited in atypical phases of gait, accounting for both anticipatory gait modifications before perturbations and reactive feedback responses to perturbations. Our findings are consistent with the idea that a common pool of spatially fixed locomotor muscle synergies can be recruited by different neural pathways, including the central pattern generator for walking, brainstem pathways for balance control, and cortical pathways mediating voluntary gait modifications. Together with electrophysiological studies, our work suggests that muscle synergies may provide a library of motor subtasks that can be flexibly recruited by parallel descending pathways to generate a variety of complex natural movements in the upper and lower limbs.

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    • "This aperiodic muscle activity may be quantified by the greater variation in the recruitment coefficients (i.e., temporal variability) of the motor modules of novices during beam walking. Such aperiodic muscle activity in motor modules for the control of walking balance has been observed previously in response to discrete perturbations to walking (Chvatal and Ting 2012), but has not been well characterized. Since the activation of motor modules can be influenced by sensory inflow (Cheung et al. 2005), the differences in temporal consistency between experts and novices may be due to differences in how sensory information is processed to recruit motor modules. "

    Full-text · Dataset · Jan 2016
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    • "Thus, locomotor modules were also recruited in atypical phases of gait, accounting for both anticipatory gait modifications before perturbations and reactive feedback responses to perturbations [35] [192]. A common set of modules has been shown to account for both locomotion and reactive balance control [36] suggesting that modules form a general repertoire of motor actions that can be recruited by a variety of different neural pathways for voluntary, rhythmic, and reactive motor behaviours [35] [36]. The interconnected neural structures and their functionality underlying the biomechanical motor behaviour during gait has been described in increasing detail based on animal and human studies. "
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    ABSTRACT: We reviewed neural control and biomechanical description of gait in both non-disabled and post-stroke subjects. In addition, we reviewed most of the gait rehabilitation strategies currently in use or in development and observed their principles in relation to recent pathophysiology of post-stroke gait. In both non-disabled and post-stroke subjects, motor control is organized on a task-oriented basis using a common set of a few muscle modules to simultaneously achieve body support, balance control, and forward progression during gait. Hemiparesis following stroke is due to disruption of descending neural pathways, usually with no direct lesion of the brainstem and cerebellar structures involved in motor automatic processes. Post-stroke, improvements of motor activities including standing and locomotion are variable but are typically characterized by a common postural behaviour which involves the unaffected side more for body support and balance control, likely in response to initial muscle weakness of the affected side. Various rehabilitation strategies are regularly used or in development, targeting muscle activity, postural and gait tasks, using more or less high-technology equipment. Reduced walking speed often improves with time and with various rehabilitation strategies, but asymmetric postural behaviour during standing and walking is often reinforced, maintained, or only transitorily decreased. This asymmetric compensatory postural behaviour appears to be robust, driven by support and balance tasks maintaining the predominant use of the unaffected side over the initially impaired affected side. Based on these elements, stroke rehabilitation including affected muscle strengthening and often stretching would first need to correct the postural asymmetric pattern by exploiting postural automatic processes in various particular motor tasks secondarily beneficial to gait.
    Full-text · Article · Nov 2015 · Neurophysiologie Clinique/Clinical Neurophysiology
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    • "Motor module analysis alone cannot directly reveal changes in the locus of motor control, but comparison of motor modules across behaviors mediated by different neural circuits can be instructive. For example, young, healthy adults used a common set of motor modules for both overground walking and brainstem-mediated reactive balance responses (Chvatal and Ting, 2013), as well as visually guided anticipatory changes in gait that are likely to be mediated by cortical mechanisms (Chvatal and Ting, 2012). These motor modules may be organized in the spinal cord and then recruited by spinal, brainstem, and cortical inputs. "
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    ABSTRACT: Neuromechanical principles define the properties and problems that shape neural solutions for movement. Although the theoretical and experimental evidence is debated, we present arguments for consistent structures in motor patterns, i.e., motor modules, that are neuromechanical solutions for movement particular to an individual and shaped by evolutionary, developmental, and learning processes. As a consequence, motor modules may be useful in assessing sensorimotor deficits specific to an individual and define targets for the rational development of novel rehabilitation therapies that enhance neural plasticity and sculpt motor recovery. We propose that motor module organization is disrupted and may be improved by therapy in spinal cord injury, stroke, and Parkinson's disease. Recent studies provide insights into the yet-unknown underlying neural mechanisms of motor modules, motor impairment, and motor learning and may lead to better understanding of the causal nature of modularity and its underlying neural substrates. Copyright © 2015 Elsevier Inc. All rights reserved.
    Full-text · Article · Apr 2015 · Neuron
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