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Abnormal cerebellar volume and corticocerebellar dysfunction in early manifest Huntington’s disease

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Abstract

Evidence from animal models and neuropathological data has revealed cerebellar pathology in Huntington’s disease (HD). The extent of cerebellar dysfunction in preclinical stages and in early manifest HD is unclear. In this study, using MRI we investigated cerebellar changes in preclinical (preHD) and early manifest HD individuals. High-resolution structural MRI data at 3 Tesla were obtained from two independent preHD samples (n = 20/25 participants), from two independent cohorts of healthy controls (n = 20/24 participants) and from patients with early manifest HD (n = 20 participants). Resting-state functional MRI data were acquired from 20 healthy controls and 20 HD patients. Cerebellar volume was investigated using cerebellum-optimized voxel-based analysis methods. Corticocerebellar connectivity at rest was investigated by means of seed-region correlations. In both preHD samples, between-group analyses revealed no change of cerebellar volume. In contrast, early manifest HD patients exhibited lower right cerebellar lobule VIIa volume (p < 0.05 cluster-corrected). Within the control group regions functionally coupled to right cerebellar lobule VII comprised bilateral cerebellar regions, right prefrontal and cingulate areas, whereas within manifest HD, functional coupling was found in paracentral, lingual and inferior frontal areas. Paracentral connectivity strength in patients was associated with disease burden and motor symptoms. These data suggest intact cerebellar volume in preHD. In contrast, early manifest HD patients exhibit atrophy of specific cerebellar subregions and abnormal corticocerebellar functional coupling. In early HD, the association between paracentral lobule function and clinical parameters suggests that corticocerebellar connectivity strength is related to the evolution of HD biology and the severity of HD motor signs.

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Acknowledgments

This work was partly supported by a grant from the CHDI/High Q foundation (to R. C. W.), a non-for-profit organization dedicated to increase the understanding of Huntington’s disease and to facilitate the development of new treatment strategies for this illness (http://chdifoundation.org/). The authors would like to thank all participants and their families for their time and interest in this study. We are grateful to Jürn Wolf and Johanna Fischer for their support with data collection, and to Kathrin Brändle for excellent technical support.

Conflicts of interest

R. C. Wolf: speaker honoraria from Lundbeck and Otsuka and consultant fees from Trommsdorff. G. B. Landwehrmeyer: Consultancies: Bayer Pharma AG, CHDI, GlaxoSmithKline, Hoffmann-La Roche, Ipsen, Neurosearch Inc, Medesis, Medtronic, Novartis, Pfizer, Prana Biotechnology, Sangamo/Shire, Siena Biotech and TEVA. Advisory Boards: Ipsen, Neurosearch Inc, Medivation, Pfizer, Siena Biotech and TEVA. Honoraria: AOP Orphan Pharmaceuticals AG, Temmler Pharma GmbH. The other authors declare that they have no conflict of interest.

Ethical standard

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This article does not contain any studies with animals performed by any of the authors.

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Informed consent was obtained from all participants included in the study.

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    Authors and Affiliations

    1. Department of Psychiatry, Psychotherapy and Psychosomatics, Saarland University, Kirrberger Str. 1, 66421, Homburg, Germany

      Robert Christian Wolf & Nadine Donata Wolf

    2. Department of General Psychiatry, Center for Psychosocial Medicine, University of Heidelberg, Heidelberg, Germany

      Philipp Arthur Thomann

    3. Center for Neuroscience and Cognitive Systems@UniTN, Rovereto, Italy

      Fabio Sambataro

    4. Department for Forensic Psychiatry and Psychotherapy at the District Hospital Günzburg, Ulm University, Ulm, Germany

      Nenad Vasic

    5. Department of Neurology, University of Ulm, Ulm, Germany

      G. Bernhard Landwehrmeyer, Sigurd Dietrich Süßmuth & Michael Orth

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    1. Robert Christian Wolf
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    R. C. Wolf and P. A. Thomann contributed equally to this manuscript.

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    415_2015_7642_MOESM1_ESM.png

    Fig. 1, supplementary data GMV parameter estimates (means and standard errors) shown for bilateral striatal (putamen and caudate) and right cerebellar lobule VIIa volume. Left: controls. Right: early HD patients. Striatal regions were defined by the Automatic Anatomical Labeling (AAL) atlas, and mean GMV parameter estimates for putamen and caudate (left and right) were extracted and summed up to represent the extent of striatal volume within a group. Parameter estimates for the right cerebellar lobule VIIa were extracted from a cluster which showed significant differences in early HD patients compared to controls. * indicates significant between-group differences (p<0.000001) (PNG 122 kb)

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    Wolf, R.C., Thomann, P.A., Sambataro, F. et al. Abnormal cerebellar volume and corticocerebellar dysfunction in early manifest Huntington’s disease. J Neurol 262, 859–869 (2015). https://doi.org/10.1007/s00415-015-7642-6

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