Highlights
- •Rhythmic Auditory Stimulation (RAS) helps for an effective gait training in PD.
- •The cerebellum may compensate for the loss of automatic and rhythmic motricity.
- •RAS reshapes the cerebellum-brain functional connectivity with regard to specific gait-cycle phases.
- •RAS may induce a recovery of the internal timing mechanisms generating and controlling motor rhythmicity.
Abstract
Rhythmic Auditory Stimulation (RAS) has been shown to be of help in an effective gait
training of people with idiopathic Parkinson's disease (PD). The cerebellum may play
an important role in RAS aftereffects by compensating the detrimental internal clock
for automatic and rhythmic motricity. However, the neurophysiological mechanisms underlying
RAS aftereffects are still poorly understood. In the present study, we tested the
contribution of the cerebellum to RAS-based gait training aftereffects in people with
PD by examining cerebellum-cerebral connectivity indices using standard EEG recording.
We enrolled 50 patients with PD who were randomly assigned to two different modalities
of treadmill gait training using GaitTrainer3 with and without RAS (non_RAS) during
an 8-week training program. We measured clinical and kinematic gait indices and electrophysiological
data (standard EEG recording during walking on GaitTrainer3) of both the gait trainings.
We found that the greater improvement in gait performance following RAS than non_RAS
training, as per clinical and kinematic assessment, was paralleled by a more evident
reshape of cerebellum-brain functional connectivity with regard to specific brain
areas (pre-motor, sensorimotor and temporal cortices) and gait-cycle phases (mainly
25–75% of the gait cycle duration). These findings suggest that the cerebellum mediates
the reshape of sensorimotor rhythms and fronto-centroparietal connectivity in relation
to specific gait-cycle phases. This may be consistent with a recovery of the internal
timing mechanisms generating and controlling motor rhythmicity, eventually improving
gait performance. The precise definition of the cerebellar role to gait functional
recovery in people with PD may be crucial to create patient-tailored rehabilitative
approaches.
Keywords
To read this article in full you will need to make a payment
Purchase one-time access:
Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online accessOne-time access price info
- For academic or personal research use, select 'Academic and Personal'
- For corporate R&D use, select 'Corporate R&D Professionals'
Subscribe:
Subscribe to Parkinsonism & Related DisordersAlready a print subscriber? Claim online access
Already an online subscriber? Sign in
Register: Create an account
Institutional Access: Sign in to ScienceDirect
References
- Gait characteristics and falls in Parkinson's disease: a systematic review and meta-analysis.Park. Relat. Disord. 2018; 57: 1-8
- Neural control of walking in people with parkinsonism.Physiology. 2016; 31: 95-107
- Effects of external cues on gait parameters of Parkinson's disease patients: a systematic review.Clin. Neurol. Neurosurg. 2014; 124: 127-134
- Can music-based movement therapy improve motor dysfunction in patients with Parkinson's disease? Systematic review and meta-analysis.Neurol. Sci. 2017; 38: 1629-1636
- Rhythmic auditory stimulation in rehabilitation of movement disorders: a review of current research.Music Perception. 2010; 27 (263–26)
- Music therapy interventions in Parkinson's disease: the state-of-the-art.Front. Neurol. 2015; 6: 185
- Time processing and motor control in movement disorders.Front. Hum. Neurosci. 2016; 10: 63
- Rhythmic auditory cues shape neural network recruitment in Parkinson's disease during repetitive motor behavior.Eur. J. Neurosci. 2019; 49: 849-858
- Specific contributions of basal ganglia and cerebellum to the neural tracking of rhythm.Cortex. 2017; 95: 156-168
- The role of the basal ganglia in beat perception: neuroimaging and neuropsychological investigations.Ann. N. Y. Acad. Sci. 2009; 1169: 35-45
- Modulation of motor cortical excitability with auditory stimulation.J. Neurophysiol. 2018; 120: 920-925
- Walking to your right music: a randomized controlled trial on the novel use of treadmill plus music in Parkinson's disease.J. NeuroEng. Rehabil. 2019; 16: 68
- Cortico-basal ganglia and cortico-cerebellar circuits in Parkinson's disease: pathophysiology or compensation?.Behav. Neurosci. 2013; 127: 222-236
- Cerebellar networks with the cerebral cortex and basal ganglia.Trends Cognit. Sci. 2013; 17: 241-254
- Differential input of the supplementary motor area to a dedicated temporal processing network: functional and clinical implications.Front. Integr. Neurosci. 2011; 5: 86
- Effects of auditory rhythm and music on gait disturbances in Parkinson's disease.Front. Neurol. 2015; 6: 234
- Future perspectives on neural mechanisms underlying rhythm and music based neurorehabilitation in Parkinson's disease.Ageing Res. Rev. 2018; 47: 133-139
- Music therapy in Parkinson's disease.J. Am. Med. Dir. Assoc. 2018; 19: 1054-1062
- Cerebellar control of gait and interlimb coordination.Brain Struct. Funct. 2015; 220: 3513-3536
- Consensus paper: roles of the cerebellum in motor control--the diversity of ideas on cerebellar involvement in movement.Cerebellum. 2012; 11: 457-487
- Functional topography of the cerebellum for motor and cognitive tasks: an fMRI study.Neuroimage. 2012; 59: 1560-1570
- Cerebellar role in Parkinson's disease.J. Neurophysiol. 2016; 116: 917-919
- The basal ganglia and the cerebellum: nodes in an integrated network.Nat. Rev. Neurosci. 2018; 19: 338-350
- What do we know about the influence of the cerebellum on walking ability? Promising findings from transcranial alternating current stimulation.Cerebellum. 2017; 16: 859-867
- Switching on depression and potentiation in the cerebellum.Cell Rep. 2018; 22: 722-733
- Listening to musical rhythms recruits motor regions of the brain.Cerebr. Cortex. 2008; 18: 2844-2854
- La Textura del Sistema Nerviosa del Hombre y los Vertebrados.Moya, Madrid1904
- Multi-electrode analysis of field potentials in the turtle cerebellum: an electrophysiological method for monitoring continous spatial parameters.Brain Res. 1972; 44 (676–645)
- Timing and plasticity in the cerebellum: focus on the granular layer.Trends Neurosci. 2009; 32: 30-40
- Oscillatory activity of the human cerebellum: the intracranial electrocerebellogram revisited.Neurosci. Biobehav. Rev. 2013; 37: 585-593
- Visual gamma oscillations: the effects of stimulus type, visual field coverage and stimulus motion on MEG and EEG recordings.Neuroimage. 2013; 69: 223-230
- Muscle afferent inputs from the hand activate human cerebellum sequentially through parallel and climbing fiber systems.Clin. Neurophysiol. 2003; 114: 2107-2117
- The human electrocerebellogram(ECeG) recorded non-invasively using scalp electrodes.Neurosci. Lett. 2018; 682: 124-131
- Study of the spontaneous electric activity of the human cerebellum.Acta Neurol. Psychiatr. Belg. 1964; 64: 825-831
- The electrocerebellogram.Clin. EEG Neurosci. 2004; 35: 112-115
- High-density EEG in current clinical practice and opportunities for the future.J. Clin. Neurophysiol. 2021; 38: 112-123
- Can EEG and MEG detect signals from the human cerebellum?.Neuroimage. 2020; 215: 116817
- Spatiotemporal firing patterns in the cerebellum.Nat. Rev. Neurosci. 2011; 12: 327-344
- Rhythmic auditory-motor facilitation of gait patterns in patients with Parkinson's disease.J. Neurol. Neurosurg. Psychiatr. 1997; 62: 22-26
Article info
Publication history
Published online: February 23, 2022
Accepted:
February 17,
2022
Received in revised form:
February 6,
2022
Received:
January 5,
2021
Identification
Copyright
© 2022 Elsevier Ltd. All rights reserved.
