Two biomechanical strategies for locomotor adaptation to split-belt treadmill walking in subjects with and without transtibial amputation
Introduction
When walking under novel conditions, the nervous system gradually modifies locomotor control in response to sensory feedback. Adaptation is characterized biomechanically by a movement parameter changing gradually in response to an altered environment (Martin et al., 1996) and by aftereffects, which linger when the environmental perturbation is removed. Because aftereffects do not immediately dissipate when the perturbation is removed, they indicate predictive control of movement (Ogawa et al., 2014, Kagerer et al., 2007).
Locomotor adaptation can be studied during split-belt treadmill walking, in which each belt moves at a different speed (Prokop et al., 1995). Over several minutes of split-belt walking, interlimb parameters such as step length symmetry and double support time adapt (Reisman et al., 2005). Step length symmetry adaptation is a robust finding replicated in stroke survivors (Reisman et al., 2007, Reisman et al., 2013), Parkinson׳s disease patients (Roemmich et al., 2014a, Roemmich et al., 2014b), and many conditions in healthy subjects (Malone and Bastian, 2010, Torres-Oviedo and Bastian, 2010, Torres-Oviedo and Bastian, 2012, Finley et al., 2014). During split-belt walking, ground reaction forces (GRF) exhibit predictive changes at initial contact, although vertical GRF in single support and propulsive GRF changes immediately, indicating reactive control (Mawase et al., 2013, Ogawa et al., 2014). Over the course of split-belt adaptation, subjects reduce muscle activity and metabolic power (Finley et al., 2013).
Metabolic power decreases during split-belt adaptation, but changes in joint mechanical work that may cause this improved efficiency are unknown. During steady walking, metabolic cost is determined largely by trailing leg work in the step-to-step transition (STS), which increases with metabolic rate (Donelan et al., 2002a). Trailing leg work in STS is more efficient than single support work (Kuo, 2002) and comes predominantly from the ankle while single support work comes more from the hip (Farris and Sawicki, 2012, Zelik et al., 2015). This result explains increased metabolic cost in trans-tibial amputees (Houdijk et al., 2009a, Houdijk et al., 2009b, Adamczyk and Kuo, 2015) and healthy subjects with immobilized ankles (Wutzke et al., 2012). However, changes in joint work during split-belt adaptation are largely unknown. Only ankle work in late stance and hip work in swing have been quantified in split-belt adaptation (Roemmich et al., 2014a, Hinkel-Lipsker and Hahn, 2016). Furthermore, split-belt walking has not been tested on trans-tibial amputees. Because trans-tibial amputees have limited propulsion from their prosthesis (Silverman et al., 2008, Fey et al., 2011), split-belt walking with the prosthesis on the fast belt is a useful model of compensation during locomotor adaptation.
The purposes of this study were to: (1) determine how joint work changes as subjects adapt to split-belt walking; and, (2) explore biomechanical compensation mechanisms trans-tibial amputees use during split-belt walking. Our primary hypothesis is that controls would reduce hip work and increase trailing leg STS ankle work on the fast belt over adaptation. We propose this switch from hip work to trailing ankle work as a joint-level biomechanical mechanism for reducing metabolic power during split-belt adaptation. Our primary focus was work from the fast leg joints, which have much higher work than slow leg joints and should thus contribute more to metabolic power. Given that amputees lack a biological ankle on the fast belt, have less adaptability on the amputated side (Houdijk et al., 2012), and do more work with the intact than the amputated leg (Houdijk et al., 2009a, Houdijk et al., 2009b, Adamczyk and Kuo, 2015), we further hypothesized that amputees would be unable to increase fast (prosthetic) leg ankle work and would instead increase slow (intact) leg work as they adapted. Lastly, based on decreasing slow leg braking force during able-bodied split-belt adaptation (Ogawa et al., 2014), we hypothesize that, for both amputees and controls, slow leg collisional energy loss would decrease as subjects adapted.
Section snippets
Subjects
Eight trans-tibial amputees (6 male, 1 congenital, 7 traumatic, BW:80.4±16.9 kg, intact leg length:92.0±6.4 cm) and eight matched controls (6 male, BW:81.5±14.1 kg, leg length:91.8±4.7 cm) gave informed consent prior to participating in this study approved by the Georgia Tech Institutional Review Board. Amputees wore their own prostheses with energy storage and return feet, passive elastic feet that provide more propulsion than a solid-ankle cushioned heel foot but less than a powered ankle (
Results
All subjects displayed stereotypical responses in step kinematics. Compared to baseline, both controls and amputees exhibited negative step length asymmetry in early adaptation (controls: ES=2.74; p=0.034; amputees: ES=1.51; p=0.013) and positive asymmetry in early post-adaptation (controls: p=0.031; amputees: p=0.031). Although they appear to overshoot zero asymmetry as they adapt, neither group significantly differed from baseline step length symmetry in late adaptation (controls: ES=1.17; p
Step length symmetry has typical adaptation pattern in both controls and amputees
Changes in step length symmetry were consistent with previous studies (Reisman et al., 2005, Malone and Bastian, 2010, Vazquez et al., 2015). Both controls and amputees initially responded to split-belt walking by taking longer steps with the slow leg leading, but returned to baseline step length symmetry by late adaptation. Both groups had the opposite aftereffect in early post-adaptation, indicating predictive control. Therefore, the lack of sensory feedback in the amputees’ distal limb did
Conclusion
Control subjects adapt to split-belt walking using two strategies: they change ankle work timing, increasing fast ankle work during STS while reducing inefficient hip work, and they allow their CoM to move farther backward during fast single support while limiting backward motion on the slow belt. Because amputees had their prostheses on the fast belt, they quickly relied on the CoM displacement strategy throughout adaptation, but they still adapted step length symmetry without using the ankle
Conflicts of interest
The authors have no conflicts of interest to disclose.
Acknowledgments
This research was funded through NIH Grants NICHD 5T32-HD-055180 and NINDS 5R01NS069655.
References (41)
- et al.
Simultaneous positive and negative external mechanical work in human walking
J. Biomech.
(2002) - et al.
The influence of energy storage and return foot stiffness on walking mechanics and muscle activity in below-knee amputees
Clin. Biomech.
(2011) - et al.
The energy cost for the step-to-step transition in amputee walking
Gait Posture
(2009) - et al.
The relative contribution of ankle moment and trailing limb angle to propulsive force during gait
Human Mov. Sci.
(2015) - et al.
The effect of prosthetic foot push-off on mechanical loading associated with knee osteoarthritis in lower extremity amputees
Gait Posture
(2011) - et al.
Effects of dopaminergic therapy on locomotor adaptation and adaptive learning in persons with Parkinson׳s disease
Behav. Brain Res.
(2014) - et al.
Locomotor adaptation and locomotor adaptive learning in Parkinson׳s disease and normal aging
Clin. Neurophysiol.
(2014) - et al.
A collisional model of the energetic cost of support qualitatively explains leg sequencing in walking and galloping, pseudo-elastic leg behavior in running and the walk-to-run transition
J. Theor. Biol.
(2005) - et al.
Compensatory mechanisms in below-knee amputee gait in response to increasing steady-state walking speeds
Gait Posture
(2008) - et al.
The influence of a unilateral fixed ankle on metabolic and mechanical demands during walking in unimpaired young adults
J. Biomech.
(2012)