Robot-induced Perturbations of Human Walking Reveal a Selective Generation of Motor Adaptation

Overview

Journal Sci Robot

Specialties Biomedical Engineering
Biotechnology

Date 2020 Nov 7

PMID 33157871

Citations 26

Authors

Iahn Cajigas

Alexander Koenig

Giacomo Severini

Maurice Smith

Paolo Bonato

Affiliations

Soon will be listed here.

Abstract

The processes underlying the generation of motor adaptation in response to mechanical perturbations during human walking have been subject to debate. We used a robotic system to apply mechanical perturbations to step length and step height over consecutive gait cycles. Specifically, we studied perturbations affecting only step length, only step height, and step length and height in combination. Both step-length and step-height perturbations disrupt normal walking patterns, but step-length perturbations have a far greater impact on locomotor stability. We found a selective process of motor adaptation in that participants failed to adapt to step-height perturbations but strongly adapted to step-length perturbations, even when these adaptations increased metabolic cost. These results indicate that motor adaptation during human walking is primarily driven by locomotor stability, and only secondarily by energy expenditure and walking pattern preservation. These findings have substantial implications for the design of protocols for robot-assisted gait rehabilitation.

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References

You J, Chou Y, Lin C, Su F . Effect of slip on movement of body center of mass relative to base of support. Clin Biomech (Bristol). 2001; 16(2):167-73. DOI: 10.1016/s0268-0033(00)00076-0. View

Pai Y, Patton J . Center of mass velocity-position predictions for balance control. J Biomech. 1997; 30(4):347-54. DOI: 10.1016/s0021-9290(96)00165-0. View

Kawato M . Internal models for motor control and trajectory planning. Curr Opin Neurobiol. 1999; 9(6):718-27. DOI: 10.1016/s0959-4388(99)00028-8. View

Shadmehr R, Mussa-Ivaldi F . Adaptive representation of dynamics during learning of a motor task. J Neurosci. 1994; 14(5 Pt 2):3208-24. PMC: 6577492. View

Geyer H, Herr H . A muscle-reflex model that encodes principles of legged mechanics produces human walking dynamics and muscle activities. IEEE Trans Neural Syst Rehabil Eng. 2010; 18(3):263-73. DOI: 10.1109/TNSRE.2010.2047592. View

Hof A, Gazendam M, Sinke W . The condition for dynamic stability. J Biomech. 2004; 38(1):1-8. DOI: 10.1016/j.jbiomech.2004.03.025. View

Scheidt R, Conditt M, Secco E, Mussa-Ivaldi F . Interaction of visual and proprioceptive feedback during adaptation of human reaching movements. J Neurophysiol. 2005; 93(6):3200-13. DOI: 10.1152/jn.00947.2004. View

Aoyagi D, Ichinose W, Harkema S, Reinkensmeyer D, Bobrow J . A robot and control algorithm that can synchronously assist in naturalistic motion during body-weight-supported gait training following neurologic injury. IEEE Trans Neural Syst Rehabil Eng. 2007; 15(3):387-400. DOI: 10.1109/TNSRE.2007.903922. View

Hof A . The 'extrapolated center of mass' concept suggests a simple control of balance in walking. Hum Mov Sci. 2007; 27(1):112-25. DOI: 10.1016/j.humov.2007.08.003. View

10.

Reynolds R, Bronstein A . The broken escalator phenomenon. Aftereffect of walking onto a moving platform. Exp Brain Res. 2003; 151(3):301-8. DOI: 10.1007/s00221-003-1444-2. View

11.

Winter D . Sagittal plane balance and posture in human walking. IEEE Eng Med Biol Mag. 2009; 6(3):8-11. DOI: 10.1109/MEMB.1987.5006430. View

12.

Thoroughman K, Shadmehr R . Learning of action through adaptive combination of motor primitives. Nature. 2000; 407(6805):742-7. PMC: 2556237. DOI: 10.1038/35037588. View

13.

Emken J, Benitez R, Sideris A, Bobrow J, Reinkensmeyer D . Motor adaptation as a greedy optimization of error and effort. J Neurophysiol. 2007; 97(6):3997-4006. DOI: 10.1152/jn.01095.2006. View

14.

Bastian A . Understanding sensorimotor adaptation and learning for rehabilitation. Curr Opin Neurol. 2008; 21(6):628-33. PMC: 2954436. DOI: 10.1097/WCO.0b013e328315a293. View

15.

Choi J, Bastian A . Adaptation reveals independent control networks for human walking. Nat Neurosci. 2007; 10(8):1055-62. DOI: 10.1038/nn1930. View

16.

TOWNSEND M . Biped gait stabilization via foot placement. J Biomech. 1985; 18(1):21-38. DOI: 10.1016/0021-9290(85)90042-9. View

17.

Wolpert D, Miall R . Forward Models for Physiological Motor Control. Neural Netw. 1996; 9(8):1265-1279. DOI: 10.1016/s0893-6080(96)00035-4. View

18.

Cajigas I, Goldsmith M, Duschau-Wicke A, Riener R, Smith M, Brown E . Assessment of lower extremity motor adaptation via an extension of the force field adaptation paradigm. Annu Int Conf IEEE Eng Med Biol Soc. 2010; 2010:4522-5. PMC: 3306221. DOI: 10.1109/IEMBS.2010.5626058. View

19.

Latt M, Menz H, Fung V, Lord S . Walking speed, cadence and step length are selected to optimize the stability of head and pelvis accelerations. Exp Brain Res. 2007; 184(2):201-9. DOI: 10.1007/s00221-007-1094-x. View

20.

Selinger J, OConnor S, Wong J, Donelan J . Humans Can Continuously Optimize Energetic Cost during Walking. Curr Biol. 2015; 25(18):2452-6. DOI: 10.1016/j.cub.2015.08.016. View