Postural inflexibility in PD: Does it affect compensatory stepping?

doi:10.1016/j.gaitpost.2013.10.003

Gait & Posture

Volume 39, Issue 2, February 2014, Pages 700-706

https://doi.org/10.1016/j.gaitpost.2013.10.003 Get rights and content

Highlights

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Postural inflexibility is thought to affect balance maintenance in PD.
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We investigated whether postural inflexibility affects compensatory stepping.
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We compared a series of step responses to steps preceded by feet-in-place responses.
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Switch from a feet-in-place to step strategy led to deteriorated step performance.
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This switch effect was not different between PD patients and controls.

Abstract

Parkinson's disease (PD) impairs the ability to shape postural responses to contextual factors. It is unknown whether such inflexibility pertains to compensatory steps to overcome balance perturbations. Participants were instructed to recover balance in response to a platform translation. A step was necessary to recover balance when the translation was large, whereas a feet-in-place (FiP) response was sufficient when the translation was small (i.e. no step). We compared step trials that required a switch away from the current postural set (switch trials: step trials that were preceded by FiP trials) with non-switch trials (i.e. step trials were preceded by identical step trials). 51 PD patients (59 ± 7 years) were compared with 22 healthy controls (60 ± 6 years). In a second analysis, we compared a subgroup of 14 freezers (PD-FOG) with a subgroup of 14 non-freezers (PD-noFOG; matched for age, gender and disease severity). Compared to non-switch trials, switch trials resulted in poorer step execution and more steps needed to recover balance. These switching effects were similar in PD patients and controls, and in PD-FOG and PD-noFOG patients. Overall, PD patients demonstrated poorer stepping performance than controls. PD-FOG had a worse performance than PD-noFOG. Moreover, PD patients, and particularly PD-FOG patients, were less able to improve step performance with repetitive step trials, in contrast to controls. Thus, there was no PD-related deficit to switch to an alternative response strategy, neither in patients with FOG nor in patients without FOG. Difficulty to adapt the step trial-by-trial might have contributed to the absence of switch deficits in PD.

Introduction

Parkinson's disease (PD) impairs the ability to successfully overcome postural perturbations, resulting in frequent falls [1]. The underlying mechanism of this incapacitating motor symptom remains poorly understood. Potentially, an impaired ability to adjust the postural response to the context of a task negatively affects stability [2], [3], [4], [5], [6]. To appropriately respond to contextual factors, one should be able to flexibly switch between ‘sets’, thereby priming the nervous system to achieve the intended goal. In the current study we investigated whether this switching impairment contributes to the defective stepping responses in PD to overcome a postural perturbation.

Effects of ‘set’ have been assessed by exposing subjects to randomly sized perturbations and contrasting their performance with responses to blocks of identical perturbations [7], [8], [9], or to instruct the participants to respond with a certain strategy, for instance stepping [9], “resisting” or “giving” [2], [10]. These manipulations generally result in modulation of the magnitude of the early, automatic postural response that helps stabilize the body. PD impairs this flexible adaptation driven by contextual factors [2], [3], [4], [5], [6]. Previous research, however, was restricted to changes within one type of postural strategy set, in which the centre of mass (COM) is controlled without changing the base of support (feet-in-place strategy). With more challenging perturbations, balance is usually recovered by changing (enlarging) the base of support, i.e. by grasping for support or taking a compensatory step [11].

A very characteristic feature of postural instability in PD patients is their difficulty in taking compensatory steps in response to balance perturbations, particularly in the backward direction [3], [12]. We aimed to investigate whether inflexibility to changing between postural response sets (i.e. from feet-in-place to change-in-support strategy) may contribute to their impairments in compensatory stepping. For this purpose, we compared compensatory stepping responses to backward balance perturbations preceded by a series of feet-in-place (FiP) responses (inducing a switch away from the current postural set) with stepping responses preceded by a sequence of stepping responses (i.e. non-switch).

A second aim was to investigate whether postural inflexibility may be related to freezing of gait (FOG). FOG episodes often occur when changes in the intention of movement are required, such as turning and gait initiation [13]. Interestingly, PD patients with FOG demonstrate more severe set switching impairments in the cognitive domain compared to non-freezing PD patients [14]. We therefore conducted a matched subgroup analysis to compare the effects of changes in postural set between PD patients with and without FOG.

Section snippets

Subjects

Fifty-one patients with Parkinson's disease (69% men, age 59 ± 7) were recruited from the outpatient clinic of the Radboud University Nijmegen Medical Centre and were screened by a neurologist trained in movement disorders. Inclusion criteria were Parkinson's disease (UK Brain Bank Criteria) [15], Hoehn & Yahr (H&Y) stage <3 [16], and aged between 18 and 70 years. Exclusion criteria were Mini Mental State Examination <24 [17], clinically relevant depression or anxiety disorders according to

PD patients vs. healthy controls (Fig. 2)

Across postural set conditions, PD patients did not differ from healthy subjects with regard to step onset (F_1,71 = 0.42, p = 0.518), or step length (F_1,71 = 2.52, p = 0.117). Yet, PD patients had 3° smaller leg angles (F_1,71 = 7.84, p = 0.007) and 4.2° larger trunk angles (F_1,69 = 7.04, p = 0.010) than healthy subjects. Furthermore, PD patients needed significantly more steps than healthy controls to overcome the perturbation (respectively 1.4 ± 0.1 vs. 1.1 ± 0.1 steps; F_1,71 = 6.10, p = 0.016).

Compared with

Discussion

We investigated whether step characteristics are affected by the need to switch away from a postural response set, and whether patients with PD with and without freezing are impaired in this kind of switching. Our results show that the body configuration at the end of the step was less beneficial when participants needed to switch from a feet-in-place set to a step response and that more steps were needed to recover balance. However, these switching effects were similar for PD patients and

Conflict of interest statement

There is no conflict of interest for any of the authors.

Acknowledgements

This work was supported by the Stichting Internationaal Parkinson Fonds. This sponsor did not have any involvement in the study design, in the collection, analysis and interpretation of the data, in the writing of the manuscript, and in the decision to submit the manuscript for publication. VW is financially supported by the Netherlands Organization for Scientific Research (NWO Grant 916.10.106).

References (34)

R.K. Chong et al.
Parkinson's disease impairs the ability to change set quickly
J Neurol Sci
(2000)
F.B. Horak et al.
Postural inflexibility in parkinsonian subjects
J Neurol Sci
(1992)
D.J. Beckley et al.
Long latency postural responses are functionally modified by cognitive set
Electroencephalogr Clin Neurophysiol
(1991)
W.E. McIlroy et al.
Changes in early ‘automatic’ postural responses associated with the prior-planning and execution of a compensatory step
Brain Res
(1993)
B.R. Bloem et al.
Postural reflexes in Parkinson's disease during ‘resist’ and ‘yield’ tasks
J Neurol Sci
(1995)
A.H. Snijders et al.
Freezer or non-freezer: clinical assessment of freezing of gait
Parkinsonism Relat Disord
(2012)
M.F. Folstein et al.
Mini-mental state: a practical method for grading the cognitive state of patients for the clinician
J Psychiatr Res
(1975)
A. Nieuwboer et al.
Reliability of the new freezing of gait questionnaire: agreement between patients with Parkinson's disease and their carers
Gait Posture
(2009)
R.B. Davis et al.
A gait analysis data collection and reduction technique
Hum Mov Sci
(1991)
J.H. Allum et al.
Review of first trial responses in balance control: influence of vestibular loss and Parkinson's disease
Hum Mov Sci
(2011)

W. Nanhoe-Mahabier et al.

First trial reactions and habituation rates over successive balance perturbations in Parkinson's disease

Neuroscience

(2012)

V. Weerdesteyn et al.

The body configuration at step contact critically determines the successfulness of balance recovery in response to large backward perturbations

Gait Posture

(2012)

V. Dietz et al.

Balance control in Parkinson's disease

Gait Posture

(1993)

J.V. Jacobs et al.

Abnormal proprioceptive-motor integration contributes to hypometric postural responses of subjects with Parkinson's disease

Neuroscience

(2006)

J.V. Jacobs et al.

Changes in the activity of the cerebral cortex relate to postural response modification when warned of a perturbation

Clin Neurophysiol

(2008)

B.R. Bloem et al.

Prospective assessment of falls in Parkinson's disease

J Neurol

(2001)

D. Dimitrova et al.

Postural muscle responses to multidirectional translations in patients with Parkinson's disease

J Neurophysiol

(2004)

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Postural inflexibility in PD: Does it affect compensatory stepping?

Highlights

Abstract

Introduction

Section snippets

Subjects

PD patients vs. healthy controls (Fig. 2)

Discussion

Conflict of interest statement

Acknowledgements

J Neurol Sci

J Neurol Sci

Electroencephalogr Clin Neurophysiol

Brain Res

J Neurol Sci

Parkinsonism Relat Disord

J Psychiatr Res

Gait Posture

Hum Mov Sci

Hum Mov Sci

Neuroscience

Gait Posture

Gait Posture

Neuroscience

Clin Neurophysiol

Prospective assessment of falls in Parkinson's disease

J Neurol

Postural muscle responses to multidirectional translations in patients with Parkinson's disease

J Neurophysiol