Skip to main content
Top
Published in:

Open Access 17-05-2024 | Electromyographic | Research Article

Dissociated cerebellar contributions to feedforward gait adaptation

Authors: Karen L. Bunday, Toby J. Ellmers, M. Rashmi Wimalaratna, Luxme Nadarajah, Adolfo M. Bronstein

Published in: Experimental Brain Research | Issue 7/2024

Login to get access

Abstract

The cerebellum is important for motor adaptation. Lesions to the vestibulo-cerebellum selectively cause gait ataxia. Here we investigate how such damage affects locomotor adaptation when performing the ‘broken escalator’ paradigm. Following an auditory cue, participants were required to step from the fixed surface onto a moving platform (akin to an airport travellator). The experiment included three conditions: 10 stationary (BEFORE), 15 moving (MOVING) and 10 stationary (AFTER) trials. We assessed both behavioural (gait approach velocity and trunk sway after stepping onto the moving platform) and neuromuscular outcomes (lower leg muscle activity, EMG). Unlike controls, cerebellar patients showed reduced after-effects (AFTER trials) with respect to gait approach velocity and leg EMG activity. However, patients with cerebellar damage maintain the ability to learn the trunk movement required to maximise stability after stepping onto the moving platform (i.e., reactive postural behaviours). Importantly, our findings reveal that these patients could even initiate these behaviours in a feedforward manner, leading to an after-effect. These findings reveal that the cerebellum is crucial for feedforward locomotor control, but that adaptive locomotor behaviours learned via feedback (i.e., reactive) mechanisms may be preserved following cerebellum damage.
Appendix
Available only for authorised users
Literature
go back to reference Armutlu K, Karabudak R, Nurlu G (2001) Physiotherapy approaches in the treatment of ataxic multiple sclerosis: a pilot study. Neurorehabil Neural Repair 15:203–211PubMed Armutlu K, Karabudak R, Nurlu G (2001) Physiotherapy approaches in the treatment of ataxic multiple sclerosis: a pilot study. Neurorehabil Neural Repair 15:203–211PubMed
go back to reference Bastian AJ (2006) Learning to predict the future: the cerebellum adapts feedforward movement control. Curr Opin Neurobiol 16:645–649PubMed Bastian AJ (2006) Learning to predict the future: the cerebellum adapts feedforward movement control. Curr Opin Neurobiol 16:645–649PubMed
go back to reference Baumann O, Borra RJ, Bower JM et al (2015) Consensus Paper: the role of the cerebellum in perceptual processes. Cerebellum 14:197PubMed Baumann O, Borra RJ, Bower JM et al (2015) Consensus Paper: the role of the cerebellum in perceptual processes. Cerebellum 14:197PubMed
go back to reference Bronstein AM, Miller DH, Rudge P, Kendall BE (1987) Down beating nystagmus: magnetic resonance imaging and neuro-otological findings. J Neurol Sci 81:173–184PubMed Bronstein AM, Miller DH, Rudge P, Kendall BE (1987) Down beating nystagmus: magnetic resonance imaging and neuro-otological findings. J Neurol Sci 81:173–184PubMed
go back to reference Bronstein AM, Grunfeld EA, Faldon M, Okada T (2008) Reduced self-motion perception in patients with midline cerebellar lesions. NeuroReport 19:691–693PubMed Bronstein AM, Grunfeld EA, Faldon M, Okada T (2008) Reduced self-motion perception in patients with midline cerebellar lesions. NeuroReport 19:691–693PubMed
go back to reference Bronstein AM, Bunday KL, Reynolds R (2009) What the broken escalator Phenomenon teaches us about balance. Ann N Y Acad Sci 1164:82–88PubMed Bronstein AM, Bunday KL, Reynolds R (2009) What the broken escalator Phenomenon teaches us about balance. Ann N Y Acad Sci 1164:82–88PubMed
go back to reference Bunday KL, Bronstein AM (2008) Visuo-vestibular influences on the moving platform locomotor aftereffect. J Neurophysiol 99:1354–1365PubMed Bunday KL, Bronstein AM (2008) Visuo-vestibular influences on the moving platform locomotor aftereffect. J Neurophysiol 99:1354–1365PubMed
go back to reference Bunday KL, Bronstein AM (2009) Locomotor adaptation and aftereffects in patients with reduced somatosensory input due to peripheral neuropathy. J Neurophysiol 102:3119–3128PubMedPubMedCentral Bunday KL, Bronstein AM (2009) Locomotor adaptation and aftereffects in patients with reduced somatosensory input due to peripheral neuropathy. J Neurophysiol 102:3119–3128PubMedPubMedCentral
go back to reference Bunday KL, Reynolds RF, Kaski D et al (2006) The effect of trial number on the emergence of the broken escalator locomotor aftereffect. Exp Brain Res 174:270–278PubMed Bunday KL, Reynolds RF, Kaski D et al (2006) The effect of trial number on the emergence of the broken escalator locomotor aftereffect. Exp Brain Res 174:270–278PubMed
go back to reference Clark DJ (2015) Automaticity of walking: functional significance, mechanisms, measurement and rehabilitation strategies. Front Hum Neurosci 9:1–13 Clark DJ (2015) Automaticity of walking: functional significance, mechanisms, measurement and rehabilitation strategies. Front Hum Neurosci 9:1–13
go back to reference Cluff T, Scott SH (2013) Rapid feedback responses correlate with reach adaptation and properties of novel upper limb loads. J Neurosci 33:15903–15914PubMedPubMedCentral Cluff T, Scott SH (2013) Rapid feedback responses correlate with reach adaptation and properties of novel upper limb loads. J Neurosci 33:15903–15914PubMedPubMedCentral
go back to reference Dieterich M, Brandt T (2008) Functional brain imaging of peripheral and central vestibular disorders. Brain 131:2538–2552PubMed Dieterich M, Brandt T (2008) Functional brain imaging of peripheral and central vestibular disorders. Brain 131:2538–2552PubMed
go back to reference Händel B, Thier P, Haarmeier T (2009) Visual motion perception deficits due to cerebellar lesions are paralleled by specific changes in cerebro-cortical activity. J Neurosci 29:15126PubMedPubMedCentral Händel B, Thier P, Haarmeier T (2009) Visual motion perception deficits due to cerebellar lesions are paralleled by specific changes in cerebro-cortical activity. J Neurosci 29:15126PubMedPubMedCentral
go back to reference Krupa DJ, Thompson RF (1997) Reversible inactivation of the cerebellar interpositus nucleus completely prevents acquisition of the classically conditioned eye-blink response. Learn Mem 3:545–556PubMed Krupa DJ, Thompson RF (1997) Reversible inactivation of the cerebellar interpositus nucleus completely prevents acquisition of the classically conditioned eye-blink response. Learn Mem 3:545–556PubMed
go back to reference Lang CE, Bastian AJ (1999) Cerebellar subjects show impaired adaptation of anticipatory EMG during catching. J Neurophysiol 82:2108–2119PubMed Lang CE, Bastian AJ (1999) Cerebellar subjects show impaired adaptation of anticipatory EMG during catching. J Neurophysiol 82:2108–2119PubMed
go back to reference Lang CE, Bastian AJ (2001) Additional somatosensory information does not improve cerebellar adaptation during catching. Clin Neurophysiol 112:895–907PubMed Lang CE, Bastian AJ (2001) Additional somatosensory information does not improve cerebellar adaptation during catching. Clin Neurophysiol 112:895–907PubMed
go back to reference Lin D, Castro P, Edwards A et al (2020) Dissociated motor learning and de-adaptation in patients with functional gait disorders. Brain 143:2594–2606PubMed Lin D, Castro P, Edwards A et al (2020) Dissociated motor learning and de-adaptation in patients with functional gait disorders. Brain 143:2594–2606PubMed
go back to reference Markov DA, Petrucco L, Kist AM, Portugues R (2021) A cerebellar internal model calibrates a feedback controller involved in sensorimotor control. Nat Commun 2021 121 12:1–21 Markov DA, Petrucco L, Kist AM, Portugues R (2021) A cerebellar internal model calibrates a feedback controller involved in sensorimotor control. Nat Commun 2021 121 12:1–21
go back to reference Marlin A, Mochizuki G, Staines WR, McIlroy WE (2014) Localizing evoked cortical activity associated with balance reactions: does the anterior cingulate play a role? J Neurophysiol 111:2634–2643PubMed Marlin A, Mochizuki G, Staines WR, McIlroy WE (2014) Localizing evoked cortical activity associated with balance reactions: does the anterior cingulate play a role? J Neurophysiol 111:2634–2643PubMed
go back to reference Martin TA, Keating JG, Goodkin HP et al (1996a) Throwing while looking through prisms. I. Focal olivocerebellar lesions impair adaptation. Brain 119:1183–1198PubMed Martin TA, Keating JG, Goodkin HP et al (1996a) Throwing while looking through prisms. I. Focal olivocerebellar lesions impair adaptation. Brain 119:1183–1198PubMed
go back to reference Martin TA, Keating JG, Goodkin HP et al (1996b) Throwing while looking through prisms. II. Specificity and storage of multiple gaze-throw calibrations. Brain 119:1199–1211PubMed Martin TA, Keating JG, Goodkin HP et al (1996b) Throwing while looking through prisms. II. Specificity and storage of multiple gaze-throw calibrations. Brain 119:1199–1211PubMed
go back to reference Mierau A, Hülsdünker T, Strüder HK (2015) Changes in cortical activity associated with adaptive behavior during repeated balance perturbation of unpredictable timing. Front Behav Neurosci 9:1–12 Mierau A, Hülsdünker T, Strüder HK (2015) Changes in cortical activity associated with adaptive behavior during repeated balance perturbation of unpredictable timing. Front Behav Neurosci 9:1–12
go back to reference Morton SM, Bastian AJ (2006) Cerebellar contributions to locomotor adaptations during splitbelt treadmill walking. J Neurosci 26:9107–9116PubMedPubMedCentral Morton SM, Bastian AJ (2006) Cerebellar contributions to locomotor adaptations during splitbelt treadmill walking. J Neurosci 26:9107–9116PubMedPubMedCentral
go back to reference Patel VR, Zee DS (2014) The cerebellum in eye movement control: nystagmus, coordinate frames and disconjugacy. Eye 2015 292 29:191–195 Patel VR, Zee DS (2014) The cerebellum in eye movement control: nystagmus, coordinate frames and disconjugacy. Eye 2015 292 29:191–195
go back to reference Patel PJ, Bhatt T, DelDonno SR et al (2019) Examining neural plasticity for slip-perturbation training: an fMRI study. Front Neurol 10:1–13 Patel PJ, Bhatt T, DelDonno SR et al (2019) Examining neural plasticity for slip-perturbation training: an fMRI study. Front Neurol 10:1–13
go back to reference Pierrot-Deseilligny C, Milea D (2005) Vertical Nystagmus: clinical facts and hypotheses. Brain 128:1237–1246PubMed Pierrot-Deseilligny C, Milea D (2005) Vertical Nystagmus: clinical facts and hypotheses. Brain 128:1237–1246PubMed
go back to reference Rand MK, Wunderlich DA, Martin PE et al (1998) Adaptive changes in responses to repeated locomotor perturbations in cerebellar patients. Exp Brain Res 122:31–43PubMed Rand MK, Wunderlich DA, Martin PE et al (1998) Adaptive changes in responses to repeated locomotor perturbations in cerebellar patients. Exp Brain Res 122:31–43PubMed
go back to reference Reisman DS, Bastian AJ, Morton SM (2010) Neurophysiologic and rehabilitation insights from the split-belt and other locomotor adaptation paradigms. Phys Ther 90:187–195PubMedPubMedCentral Reisman DS, Bastian AJ, Morton SM (2010) Neurophysiologic and rehabilitation insights from the split-belt and other locomotor adaptation paradigms. Phys Ther 90:187–195PubMedPubMedCentral
go back to reference Reynolds RF, Bronstein AM (2003) The broken escalator phenomenon: aftereffect of walking onto a moving platform. Exp Brain Res 151:301–308PubMed Reynolds RF, Bronstein AM (2003) The broken escalator phenomenon: aftereffect of walking onto a moving platform. Exp Brain Res 151:301–308PubMed
go back to reference Schlerf JE, Ivry RB (2011) Task goals influence online corrections and adaptation of reaching movements. J Neurophysiol 106:2622–2631PubMedPubMedCentral Schlerf JE, Ivry RB (2011) Task goals influence online corrections and adaptation of reaching movements. J Neurophysiol 106:2622–2631PubMedPubMedCentral
go back to reference Shadmehr R, Smith MA, Krakauer JW (2010) Error correction, sensory prediction, and adaptation in motor control. Annu Rev Neurosci 33:89–108PubMed Shadmehr R, Smith MA, Krakauer JW (2010) Error correction, sensory prediction, and adaptation in motor control. Annu Rev Neurosci 33:89–108PubMed
go back to reference Smith MA, Shadmehr R (2005) Intact ability to learn internal models of arm dynamics in Huntington’s disease but not cerebellar degeneration. J Neurophysiol 93:2809–2821PubMed Smith MA, Shadmehr R (2005) Intact ability to learn internal models of arm dynamics in Huntington’s disease but not cerebellar degeneration. J Neurophysiol 93:2809–2821PubMed
go back to reference Tang KS, Kaski D, Allum JHJ, Bronstein AM (2013) The effect of gait approach velocity on the broken escalator phenomenon. Exp Brain Res 226:335–346PubMed Tang KS, Kaski D, Allum JHJ, Bronstein AM (2013) The effect of gait approach velocity on the broken escalator phenomenon. Exp Brain Res 226:335–346PubMed
go back to reference Therrien AS, Bastian AJ (2019) The cerebellum as a movement sensor. Neurosci Lett 688:37–40PubMed Therrien AS, Bastian AJ (2019) The cerebellum as a movement sensor. Neurosci Lett 688:37–40PubMed
go back to reference Tseng YW, Diedrichsen J, Krakauer JW et al (2007) Sensory prediction errors drive cerebellum-dependent adaptation of reaching. J Neurophysiol 98:54–62PubMed Tseng YW, Diedrichsen J, Krakauer JW et al (2007) Sensory prediction errors drive cerebellum-dependent adaptation of reaching. J Neurophysiol 98:54–62PubMed
go back to reference Wagner JN, Glaser M, Brandt T, Strupp M (2008) Downbeat nystagmus: aetiology and comorbidity in 117 patients. J Neurol Neurosurg Psychiatry 79:672–677PubMed Wagner JN, Glaser M, Brandt T, Strupp M (2008) Downbeat nystagmus: aetiology and comorbidity in 117 patients. J Neurol Neurosurg Psychiatry 79:672–677PubMed
go back to reference Xu-Wilson M, Chen-Harris H, Zee DS, Shadmehr R (2009) Cerebellar contributions to Adaptive Control of Saccades in humans. J Neurosci 29:12930–12939PubMedPubMedCentral Xu-Wilson M, Chen-Harris H, Zee DS, Shadmehr R (2009) Cerebellar contributions to Adaptive Control of Saccades in humans. J Neurosci 29:12930–12939PubMedPubMedCentral
go back to reference Zee DS, Yee RD, Cogan DG et al (1976) Ocular motor abnormalities in hereditary cerebellar ataxia. Brain 99:207–234PubMed Zee DS, Yee RD, Cogan DG et al (1976) Ocular motor abnormalities in hereditary cerebellar ataxia. Brain 99:207–234PubMed
go back to reference Zee DS, Yamazaki A, Butler PH, Gucer G (1981) Effects of ablation of flocculus and paraflocculus of eye movements in primate. J Neurophysiol 46:878–899PubMed Zee DS, Yamazaki A, Butler PH, Gucer G (1981) Effects of ablation of flocculus and paraflocculus of eye movements in primate. J Neurophysiol 46:878–899PubMed
Metadata
Title
Dissociated cerebellar contributions to feedforward gait adaptation
Authors
Karen L. Bunday
Toby J. Ellmers
M. Rashmi Wimalaratna
Luxme Nadarajah
Adolfo M. Bronstein
Publication date
17-05-2024
Publisher
Springer Berlin Heidelberg
Published in
Experimental Brain Research / Issue 7/2024
Print ISSN: 0014-4819
Electronic ISSN: 1432-1106
DOI
https://doi.org/10.1007/s00221-024-06840-9

Other articles of this Issue 7/2024

Experimental Brain Research 7/2024 Go to the issue

Advances in Alzheimer's

Alzheimer's research and care is changing rapidly. Keep up with the latest developments from key international conferences, together with expert insights on how to integrate these advances into practice.

This content is intended for healthcare professionals outside of the UK.

Supported by:
  • Lilly
Developed by: Springer Healthcare IME
Learn more