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May 17, 2013 - Sébastien Celle • Robert Bartha •. Jean-Claude Barthélémy • Frédéric Roche. Received: 5 March 2013 / Accepted: 6 May 2013 / Published ...
Brain Topogr (2014) 27:293–295 DOI 10.1007/s10548-013-0293-y

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Higher Gait Variability is Associated with Decreased Parietal Gray Matter Volume Among Healthy Older Adults Olivier Beauchet • Ce´dric Annweiler • Se´bastien Celle • Robert Bartha • Jean-Claude Barthe´le´my • Fre´de´ric Roche

Received: 5 March 2013 / Accepted: 6 May 2013 / Published online: 17 May 2013 Ó Springer Science+Business Media New York 2013

Abstract The objectives of this study were to examine the association of stride time variability (STV) with gray and white matter volumes in healthy older adults, and to determine the specific location of any parenchymal loss associated with higher STV. A total of 71 participants (mean age 69.0 ± 0.8 years; 59.7 % female) were included in this study. All participants had a 1.0 Tesla 3D T1weighted MRI of the brain to measure gray and white matter volumes. STV was measured at steady-state selfAuthors’ contribution Beauchet has full access to all of the data in the study, takes responsibility for the data, the analyses and interpretation and has the right to publish any and all data, separate and apart from the attitudes of the sponsor. All authors meet all of the following criteria: (1) contributing to the conception and design, or analyzing and interpreting data; (2) drafting the article or revising it critically for important intellectual content; and (3) approving the final version to be published. O. Beauchet (&)  C. Annweiler Department of Neuroscience, Division of Geriatric Medicine, UPRES EA 4638, UNAM, Angers University Hospital, 49933 Angers Cedex 9, France e-mail: [email protected] C. Annweiler  R. Bartha Center for Functional and Metabolic Mapping, Department of Medical Biophysics, Schulich School of Medicine and Dentistry, Robarts Research Institute, The University of Western Ontario, London, ON, Canada S. Celle  J.-C. Barthe´le´my  F. Roche Service de Physiologie Clinique et de l’Exercice, CHU, Saint-Etienne, France S. Celle  J.-C. Barthe´le´my  F. Roche EA 4607 ‘‘SNA EPIS’’, Faculte´ de Me´decine Jacque Lisfranc, UJM, Saint-Etienne, France S. Celle  J.-C. Barthe´le´my  F. Roche PRES Universite´ de Lyon, 42023 Saint-Etienne, France

selected walking speed using an electronic footswitch system. We found an association between higher STV and lower gray matter volume in the right parietal lobe (e.g., angular gyrus, Brodmann area 39, cluster corrected pFWE = 0.035). There were no significant associations between STV and higher gray matter volume or change in white matter volume. To the best of our knowledge this study is the first to identify a significant association of higher STV with lower right parietal gray matter volume in healthy older adults. Keywords

Gait disorders  Motor control  MRI

Introduction Gait variability is defined as the fluctuation of stride-tostride interval (Hausdorff 2005; Beauchet et al. 2012). Low gait variability while walking at steady-state self-selected pace illustrates efficient gait control (Hausdorff 2005; Beauchet et al. 2012; Rosano et al. 2006). Stride time variability (STV) has been identified as a biomarker of cortical gait control in high-functioning older adults (Beauchet et al. 2012). Specifically, STV has been inversely associated with information updating and monitoring, suggesting that the higher levels of gait control involve processing a continuous flow of information to adapt gait to environmental conditions. Consistent with the cognitive data, emerging evidence indicates that increased gait variability is cross-sectionally associated with abnormalities observed on brain magnetic resonance imaging (MRI) (Hausdorff 2005; Rosano et al. 2006); mostly with white matter and subcortical ischemic lesions in older adults (Hausdorff 2005; Beauchet et al. 2012; Rosano et al. 2006). Less is known about the association between gait

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variability and brain atrophy among older adults free of neurodegenerative conditions (Hausdorff 2005; Beauchet et al. 2012). Safe gait requires the analysis of a flow of visual, vestibular and proprioceptive information involving the parietal lobe. In addition, increased STV is associated with unsafe gait (Hausdorff 2005; Beauchet et al. 2012). Therefore, we hypothesized that increased STV could be associated with a decrease in gray matter volume in parietal lobe. Importantly, new methods that segment brain structures and identify volumetric changes have been developed, including voxel-based morphometry (VBM) (Ashburner and Friston 2000; Hayasaka et al. 2004). The objectives of this study were to examine the association of STV with gray and white matter volumes in healthy older adults, and to determine the specific location of any parenchymal loss associated with higher STV.

Methods A total of 71 participants (mean age 69.0 ± 0.8 years [range 66–72]; 59.7 % female) from the PROOF cohort were included in this study after having given their written informed consent for research. Sampling and data collection procedures of the PROOF study have been described elsewhere in detail (Barthelemy et al. 2007). Inclusion criteria for the present analysis were: age C65 years, no cerebrovascular brain abnormalities (no relevant leukoaraiosis [Fazekas score\2 (Fazekas et al. 2002)] and no lacunas), and no chronic conditions influencing gait variability. All participants had a 1.0 Tesla 3D T1-weighted MRI of the brain to measure gray and white matter volumes. Additionally, fluid attenuated inversion recovery (FLAIR) imaging was performed to rate leukoaraiosis using the Fazekas standardized scale (Fazekas et al. 2002). VBM was performed with Statistical Parametric Mapping (SPM) version 8 to classify voxels into gray and white matter, and realign images to a standard space. STV was measured at steady-state selfselected walking speed in a 20 m long corridor using the SMTECÒ footswitches system (SMTECÒ, Sport & Medical Technologies SA, Nyon Switzerland). This system includes a pair of innersoles fitted inside the participant’s shoes. Each innersole contains two independent footswitches, one placed at the heel and another at the toe, which are linked to a portable data recorder worn at waist. The entire study protocol was approved by the local Ethical Committee of SaintEtienne, France. The associations between local gray or white matter volumes (dependent variables) and STV (independent variable) were examined with SPM8 multiple linear regression models after adjustment for age, gender, body mass index (BMI) and total brain matter (TBM) volume. Statistical thresholds for VBM analyses were set at

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uncorrected P \ 0.001 at voxel level and corrected P \ 0.05 at cluster level using random field theory and non-stationary correction (defaults.stats.rft.nonstat = 1).

Results In the studied sample of healthy older adults, STV was 1.9 ± 0.9 % [range 0.6–5.9], BMI was 25.5 ± 3.4 kg/m2 [range 19.7–35.9] and TBM volume was 1,177.8 ± 107.7 mL [range 1,001.7–1,491.7]. As shown in Fig. 1, we found an association between higher STV and lower gray matter volume in the right parietal lobe (e.g., angular gyrus, Brodmann area 39, Montreal Neurological Institute coordinates in millimeters X = 48, Y = -48 and Z = 35; cluster size = 492 voxels; cluster corrected pFWE = 0.035). There were no significant associations between STV and higher gray matter volume or change in white matter volume.

Discussion To the best of our knowledge this study is the first to identify a significant association of higher STV with lower right parietal gray matter volume in healthy older adults, particularly within the angular gyrus (Brodmann area 39). Poor gait performance has been mainly associated with white matter ischemic lesions (i.e., leukoaraiosis and/or lacunas) (Hausdorff 2005; Beauchet et al. 2012; Rosano et al. 2006), or with smaller prefrontal area among older adults without stroke (Rosano et al. 2006). In addition, an association between poor gait performance and smaller parietal lobe was previously found (Rosano et al. 2007; 2008) when using the mean values of gait parameters as the outcomes measures. Specifically, both shorter steps and longer double support time were associated with smaller gray matter of the right superior and bilateral inferior parietal lobules. These results suggested that parietal cortex, which regulated our coordinates in relationship to the surrounding environment, may impair gait regulation. The current study is consistent with these results and illustrates the likely involvement of frontal-subcortical executive dysfunction in gait control impairment (Beauchet et al. 2012). The domain-specific executive subfunction associated with gait variability has been shown to be the ability to process and update contextual information to continuously adapt gait to environmental perturbations (Beauchet et al. 2012). Since the posterior parietal cortex is involved in multimodal processing, particularly in visual and spatial information (Gottlieb 2007), our finding of an association between higher STV and lower parietal gray matter volume is consistent with previous literature. For instance, the

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Fig. 1 Stride time variabilityrelated decrease in gray matter volume of the right angula gyrus. Results of average gray matter map of participants (n = 71) are presented in the neurological convention (i.e., Montreal Neurological Institute coordinate values above refer to the distance in millimeters relative to the midline for sagittal sections in this figure [? = right; - = left] and to the anterior commissure for coronal sections [? = anterior; - = posterior]. In each section, white matter and cerebrospinal fluid are blackened. Identified in color are brain regions in which stride time variability is associated with low gray matter volume. Color-scaled t values (color bar) were derived from a general linear model of voxelwise gray matter volume that included age, gender, body mass index and total brain matter volume as covariables. The cluster corrected pFWE was calculated at 0.035 (Color figure online)

parietal lobe is able to map objects perceived visually into body coordinate positions (Gottlieb 2007). It is thus possible that focal neurodegeneration in the parietal cortex alters the regulation of our coordinates in relationship to the surrounding environment with subsequent impairment in gait regularity. The localisation of smaller parietal volume on the right side found in our study has previously been reported (Rosano et al. 2007; Rosano et al. 2008), but the reason for this lateralization remains unclear. A future prospective analysis of this cohort should elucidate whether healthy older adults with parietal atrophy are more likely to develop gait disorders and to fall. Acknowledgments The PROOF study group would like to thank all persons who took part in this study. This study was supported by a Grant from the French Minister of Health (Cellule Projet Hospitalier de Recherche Clinique National, Direction interre´gionale de la Recherche Clinique, CHU Saint-Etienne; Appel d’Offre 1998 and Appel d’Offre 2002), by Associations SYNAPSE and ONDAINE. Conflict of interest

The authors report no conflicts of interest.

References Ashburner J, Friston KJ (2000) Voxel-based morphometry-the methods. Neuroimage 11:805–821

Barthelemy JC, Pichot V, Dauphinot V, Celle S, Laurent B, Garcin A, Kerleroux J, Lacour JR, Kossovsky M, Gaspoz JM, Roche F (2007) Autonomic nervous system activity and decline as prognostic indicators of cardiovascular and cerebrovascular events: the ‘PROOF’ Study. Study design and population sample. Associations with sleep-related breathing disorders: the ‘SYNAPSE’ Study. Neuroepidemiology 29:18–28 Beauchet O, Annweiler C, Montero-Odasso M, Fantino B, Herrmann FR, Allali G (2012) Gait control: a specific subdomain of executive function? J Neuroeng Rehabil 9:12 Fazekas F, Barkhof F, Wahlund LO, Pantoni L, Erkinjuntti T, Scheltens P, Schmidt R (2002) CT and MRI rating of white matter lesions. Cerebrovasc Dis 13(Suppl 2):31–36 Gottlieb J (2007) From thought to action: the parietal cortex as a bridge between perception, action, and cognition. Neuron 53:9–16 Hausdorff JM (2005) Gait variability: methods, modeling and meaning. J Neuroeng Rehabil 2:19 Hayasaka S, Phan KL, Liberzon I, Worsley KJ, Nichols TE (2004) Nonstationary cluster-size inference with random field and permutation methods. Neuroimage 22:676–687 Rosano C, Brach J, Longstreth WT Jr, Newman AB (2006) Quantitative measures of gait characteristics indicate prevalence of underlying subclinical structural brain abnormalities in highfunctioning older adults. Neuroepidemiology 26:52–60 Rosano C, Aizenstein HJ, Studenski S, Newman AB (2007) A regions-of-interest volumetric analysis of mobility limitations in community-dwelling older adults. J Gerontol A 62:1048–1055 Rosano C, Aiznstein H, Brach J, Longenberger A, Studenski S, Newman AB (2008) Special article: gait measures indicate underlying focal gray matter atrophy in the brain of older adults. J Gerontol A 63:1380–1388

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