Elsevier

Neurobiology of Aging

Volume 35, Issue 1, January 2014, Pages 232-239
Neurobiology of Aging

Regular article
Structural brain plasticity in Parkinson's disease induced by balance training

https://doi.org/10.1016/j.neurobiolaging.2013.06.021Get rights and content

Abstract

We investigated morphometric brain changes in patients with Parkinson's disease (PD) that are associated with balance training. A total of 20 patients and 16 healthy matched controls learned a balance task over a period of 6 weeks. Balance testing and structural magnetic resonance imaging were performed before and after 2, 4, and 6 training weeks. Balance performance was re-evaluated after ∼20 months. Balance training resulted in performance improvements in both groups. Voxel-based morphometry revealed learning-dependent gray matter changes in the left hippocampus in healthy controls. In PD patients, performance improvements were correlated with gray matter changes in the right anterior precuneus, left inferior parietal cortex, left ventral premotor cortex, bilateral anterior cingulate cortex, and left middle temporal gyrus. Furthermore, a TIME × GROUP interaction analysis revealed time-dependent gray matter changes in the right cerebellum. Our results highlight training-induced balance improvements in PD patients that may be associated with specific patterns of structural brain plasticity. In summary, we provide novel evidence for the capacity of the human brain to undergo learning-related structural plasticity even in a pathophysiological disease state such as in PD.

Introduction

The mechanisms of aging and neurodegeneration are complex and interrelated. Aging is the most important factor influencing the course and progression of Parkinson's disease (PD) (Hindle, 2010). At the same time, the severity of PD may be modulated by the presence of compensatory neuroplastic brain processes. Magnetic resonance imaging (MRI) studies suggest that, at both presymptomatic and symptomatic disease stages, an increase in gray matter (GM) volume within putamen and globus pallidus is indicative of long-term adaptation to chronic dopaminergic dysfunction (Binkofski et al., 2007, Reetz et al., 2010). Animal models of PD propose that exercise and training might trigger plastic mechanisms, and raise the hypothesis of a dynamic interplay between degenerative and regenerative mechanisms (Tillerson et al., 2001, Tillerson et al., 2002). Clinical studies provide evidence that exercise and rehabilitation programs might improve motor symptoms in PD patients and beneficially modify disease progress (Goodwin et al., 2008).

Postural instability is considered a motor symptom that is potentially related to dysfunctional mesencephalic non-dopaminergic neurotransmission, such as degeneration of cholinergic neurons in the pedunculopontine nucleus (Moro et al., 2010, Rinne et al., 2008). Postural instability enhances the risk of falling which, in turn, is associated with subsequent injuries and further disability. However recent evidence suggests that balance training might improve this symptom (Smania et al., 2010).

Are behavioral improvements in motor performance subserved by structural brain alterations? Although, to our best knowledge, this question remains unsolved in PD patients, recent findings in healthy individuals as well as in chronic stroke patients provide compelling evidence that the human brain undergoes morphological alterations in response to learning and/or rehabilitation (Boyke et al., 2008, Draganski et al., 2004, Gauthier et al., 2008). Along these lines, a recent study demonstrated an emergence of structural changes already after 2 sessions of a dynamic balance training that correlated with the individual motor skill learning of the participants (Taubert et al., 2010).

The aim of this proof-of-concept study was to investigate learning-related plasticity in GM structure in patients with PD using a complex balance task. We hypothesized the following: (A) a specific balance training results in long-term balance improvements in PD patients; (B) balance training is accompanied by morphometric GM changes; (C) PD patients exhibit differential structural changes as compared to age-matched controls; and (D) balance improvements are directly correlated with morphometric GM alterations.

Section snippets

Participants

The study procedures were approved by the ethics committee of the University of Leipzig and all participants gave their written informed consent. Patients were recruited via the outpatient clinic of the Department for Neurology, University of Leipzig. Controls were recruited from the database of volunteers of the Max Planck Institute for Human Cognitive and Brain Science. We included 20 patients that were diagnosed according to the UK brain bank criteria (Hughes et al., 1992) with mild to

Behavioral results

Baseline performance was similar between PD patients and controls (independent-sample t test; t = 0.747; p = 0.818). Performing the whole-body DBT on 6 consecutive weeks resulted in significant performance improvements in both groups (Fig. 2). The overall improvement in balance performance (mean balance performance TD 6 minus mean balance performance TD 1) differed significantly between groups (p < 0.05). Although PD patients showed an increase of 5.83 ± 1.19 seconds (mean ± SEM), the increase

Discussion

In the present study, DBT over 6 consecutive weeks resulted in significant performance improvements in PD patients as well as in age-matched controls, with a stronger improvement in the latter group. Interestingly, a behavioral follow-up test revealed skill retention even after 20 months in both patients and controls. We furthermore provide novel evidence for learning-related morphometric brain alterations in PD patients as well as age-matched healthy control participants. A group × time

Disclosure statement

All authors report no conflicts of interest.

Acknowledgements

JD and BD are supported by the Swiss National Science Foundation (NCCR Synapsy). BD is supported by the Swiss National Science Foundation (project grant Nr 320030_135679 and SPUM 33CM30_140332/1), Foundation Parkinson Switzerland, Foundation Synapsis, Novartis Foundation for medical–biological research and Deutsche Forschungsgemeinschaft (Kfo 247).

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