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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    • "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.
    Neuron 04/2015; 86(1):38-54. DOI:10.1016/j.neuron.2015.02.042 · 15.05 Impact Factor
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    • "As muscle synergies are associated with functional subtasks of the gait cycle (Chvatal and Ting 2012; Ivanenko et al. 2006), the number of synergies provides information about the complexity of control (Clark et al. 2010), whereas changes in the composition/activation of synergies can indicate whether and how the control of these motor subtasks is altered (Safavynia et al. 2011). Investigation of muscle synergies provides an ideal method to probe the effect of pain on neural control strategies during multisegmental tasks such as walking. "
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    ABSTRACT: This study aimed to examine how acute muscle pain affects muscle coordination during gait with consideration of muscle synergies (i.e. group of muscles activated in synchrony), amplitude of muscle activity and kinematics. A secondary aim was to determine whether any adaptation was specific to pain location. Sixteen participants walked on a treadmill during 5 conditions (Control, low back pain (LBP), Washout LBP, calf pain (CalfP), and Washout CalfP). Five muscle synergies were identified for all the conditions. Cross validation analysis showed that muscle synergy vectors extracted for the Control condition accounted for >81% of variance accounted for of the other conditions. Muscle synergies were altered very little in some participants (n=7 for LBP; n=10 for CalfP), but were more affected in the others (n=9 for LBP; n=6 for CalfP). No systematic differences between pain locations were observed. Considering all participants, synergies related to propulsion and weight acceptance were largely unaffected by pain, whereas synergies related to other functions (trunk control and leg deceleration) were more affected. Gastrocnemii activity was less during both CalfP and LBP than Control. Soleus activity was further reduced during CalfP and this was associated with reduced plantarflexion. Some lower leg muscles exhibited adaptations depending on pain location (e.g. greater vastus lateralis and rectus femoris activity during CalfP than LBP). Overall, these changes in muscle coordination involve a participant-specific strategy that is important to further explore as it may explain why some people are more likely to develop persistence of a painful condition.
    Journal of Neurophysiology 10/2014; 113(1). DOI:10.1152/jn.00557.2014 · 2.89 Impact Factor
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    • "Module number increased if individual muscles were not reconstructed with greater than 75% VAF and the addition of another module increased this muscle's fit by more than 5%. These criteria are considered conservative to ensure goodness of reconstruction (Chvatal and Ting, 2012; Clark et al., 2010). "
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    ABSTRACT: Objective Incomplete spinal cord injury (iSCI) disrupts motor control and limits the ability to coordinate muscles for overground walking. Inappropriate muscle activity has been proposed as a source of clinically observed walking deficits after iSCI. We hypothesized that persons with iSCI exhibit lower locomotor complexity compared to able-body (AB) controls as reflected by fewer motor modules, as well as, altered module composition and activation. Methods Eight persons with iSCI and eight age-matched AB controls walked overground at prescribed cadences. Electromyograms of fourteen single leg muscles were recorded. Non-negative matrix factorization was used to identify the composition and activation of motor modules, which represent groups of consistently co-activated muscles that accounted for 90% of variability in muscle activity. Results Motor module number, composition, and activation were significantly altered in persons with iSCI as compared to AB controls during overground walking at self-selected cadences. However, there was no significant difference in module number between persons with iSCI and AB controls when cadence and assistive device were matched. Conclusions Muscle coordination during overground walking is impaired after chronic iSCI. Significance Our results are indicative of neuromuscular constraints on muscle coordination after iSCI. Altered muscle coordination contributes to person-specific gait deficits during overground walking.
    Clinical neurophysiology: official journal of the International Federation of Clinical Neurophysiology 10/2014; 125(10). DOI:10.1016/j.clinph.2014.02.001 · 3.10 Impact Factor
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