Neuromuscular constraints on muscle coordination during overground walking in persons with chronic incomplete spinal cord injury
Introduction
Incomplete spinal cord injury (iSCI) disrupts motor commands to spinal locomotor circuitry and often severely limits the ability to coordinate muscles for overground walking. While a healthy motor system is capable of coordinating many muscles spanning multiple joints for safe and efficient walking, this ability is impaired following iSCI. More than 75% of persons with motor incomplete injuries regain some walking capacity (van Hedel and Dietz, 2009), but many do not fully return to community walking (Field-Fote and Roach, 2011, van Hedel and Dietz, 2010). Unfortunately, we do not fully understand the underlying neuromuscular mechanisms that might contribute to this shortcoming nor how specific changes in muscle co-activity impair overground walking after chronic iSCI.
Inappropriate muscle activity is a source of many of the clinically observed walking deficits that emerge in persons with chronic iSCI (Gorassini et al., 2009, Maegele et al., 2002). Locomotor training studies often target impaired muscle activity timing, agonist–antagonist joint level muscle coactivity, and electromyography (EMG) burst durations in an effort to improve walking ability (Gorassini et al., 2009, Grasso et al., 2004, Ivanenko et al., 2003, Ivanenko et al., 2004, Maegele et al., 2002, Visintin and Barbeau, 1994). However, these studies primarily focus on treadmill and body-weight support training and not overground walking. Although treadmill walking permits greater experimental control of walking conditions like speed and body-weight support, the ability to coordinate muscles during these more constrained tasks does not necessarily translate to overground or community ambulation which often require assistive devices such as a cane, walker, or crutches (Lee and Hidler, 2008). Even though the mean kinematic trajectories are similar between treadmill and overground walking, overground walking inherently requires greater step-to-step variability (Dingwell et al., 2001). Overground walking is a highly complex motor task that requires flexible motor control strategies that adapt muscle coordination to step-to-step variations in environmental and mechanical demands (Chvatal and Ting, 2012, Dingwell et al., 2001, Nielsen, 2003), especially compared to more controlled locomotor demands such as single-speed treadmill walking (Dingwell et al., 2001).
The complexity of neuromuscular control required for overground walking is deficient after iSCI, resulting in numerous walking deficits. For example, persons with iSCI present an inability to modulate walking speed outside a small range of slow speeds (Pepin et al., 2003), a dependence on assistive devices (van Hedel and Dietz, 2009), and a failure to adjust to environmental perturbations that subsequently lead to increased falls (Brotherton et al., 2007). The extent of these walking deficits vary widely with injury level, severity, and the pathways damaged, making it difficult to assess the underlying neuromuscular mechanisms (van Hedel and Dietz, 2010).
To date, it is unclear to what extent inappropriate muscle coordination contributes to overground walking deficits after chronic iSCI. Quantifying the contribution of altered muscle coordination is particularly challenging due in part to the large number of muscles that contribute to overground walking. Non-negative matrix factorization (NNMF) quantifies this complexity via extraction of motor modules, or groups of consistently co-activated muscles, that represent the “building blocks” of muscle coordination. Motor modules can be characterized in terms of number, composition (i.e., number of muscles per motor module), and activation (i.e., duration and amplitude). Motor modules can be flexibly activated in combination to produce a wide range of muscle coordination patterns during various motor tasks, with each module achieving a specific biomechanical outcome that subserves the overall biomechanical goal (Cappellini et al., 2006, Chvatal and Ting, 2012, Chvatal et al., 2011, d’Avella et al., 2011, Drew et al., 2008, Fox et al., 2013, Ivanenko et al., 2004, Neptune et al., 2009, Overduin et al., 2008, Torres-Oviedo et al., 2006). Motor modules also are useful in identifying constraints on muscle coordination related to gait deficits in neurologic pathologies such as stroke, spinal cord injury, and Parkinson’s disease (Allen et al., 2013, Bowden et al., 2010, Cheung et al., 2009b, Clark et al., 2010, Fox et al., 2013, Rodriguez et al., 2013). Following hemiparetic stroke, as well as, Parkinson’s disease, persons exhibit fewer motor modules during walking (Clark et al., 2010, Rodriguez et al., 2013). This reduction is closely related to limited walking speed and walking complexity. Similar findings have been made in pediatric spinal cord injury (Fox et al., 2013), but not explored in adult spinal cord injury. Additionally, most studies have focused on module number without extensive exploration of module composition or activation across the gait cycle.
Thus, the purpose of this study was to quantify neuromuscular deficits in muscle coordination during overground walking in persons with chronic iSCI. We hypothesized that overground muscle coordination is constrained by greater muscle co-activity in persons with iSCI as compared to age-matched (AB) controls. We predict that persons with iSCI have fewer motor modules, as well as, altered composition (i.e., increased number of muscles per motor module) and activation (i.e., increased duration) of motor modules as compared to AB controls. We examined motor modules from 14 muscles during a cadence-matched overground-walking task and revealed that changes in motor module number, composition, and activation contribute to deficits in overground walking after iSCI. Understanding the subject-specific neuromuscular constraints on muscle coordination is critical for effectively developing therapies that are more tailored to a heterogeneous population of persons with chronic iSCI and to the complexities of community ambulation.
Section snippets
Study population
Eight persons with iSCI (34.4 ± 3.8 years; mean ± 1 standard error) and eight age-matched AB controls (34.1 ± 4.1 years) participated in this study (Table 1). AB subjects also were selected to match gender and approximate body type. Ethical approval for the study was received from the Emory University Institutional Review Board (IRB protocol STU00044670); informed consent and HIPAA authorization were obtained from all subjects prior to their participation in accordance with the Declaration of Helsinki.
Reduced number of motor modules during overground walking after chronic iSCI
Persons with iSCI required fewer motor modules to account for their muscle coordination patterns during overground walking as compared to AB controls (Fig. 2A). AB controls exhibited 5.9 ± 0.4 motor modules as compared to 4.1 ± 0.6 motor modules for persons with iSCI (U14 = 11.000, p = 0.024). Six of eight iSCI subjects required less than 5 modules to account for the variability of muscle coordination patterns, while all AB subjects required more than 5 modules, suggesting AB subjects have greater
Discussion
The purpose of this study was to quantify altered muscle coordination during overground walking in persons with chronic iSCI. In particular, we predicted that during overground walking, persons with iSCI have fewer motor modules, greater number of muscles within each motor module (composition), and altered activation of motor modules as compared to age-matched AB controls. Indeed, our results showed that persons with iSCI required fewer motor modules to explain the observed muscle coordination
Acknowledgements
This work was supported in part by NIH Grant K12 HD055931, DOD Grant SC090355, as well as, a Grant from the Petit Institute for Bioengineering & Bioscience. The authors are very grateful to the participants. The authors would also like to thank Monica Danneman, Jillian Dean, David Gustafson, and Caitlin Manuel for their assistance with data collection and Victoria Stahl for her assistance with technical issues and manuscript proofing.
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