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Brain. 2015 Dec;138(Pt 12):3598-609. doi: 10.1093/brain/awv282. Epub 2015 Sep 29.

The visual perception of natural motion: abnormal task-related neural activity in DYT1 dystonia.

Author information

1
1 Center for Neurosciences, The Feinstein Institute for Medical Research, Manhasset, NY 11030, USA.
2
2 Department of Neurology, NYU Langone Medical Center, New York, NY 10016, USA.
3
3 Department of Rehabilitation Medicine, NYU Langone Medical Center, New York, NY 10016, USA.
4
4 Mirken Department of Neurology, Beth Israel Medical Center, New York, NY 10003, USA.
5
1 Center for Neurosciences, The Feinstein Institute for Medical Research, Manhasset, NY 11030, USA 5 Department of Radiology, Albert Einstein College of Medicine, Bronx, NY 10461, USA 6 Institute of Biomedical Engineering, Boğaziçi University, Istanbul, Turkey.
6
1 Center for Neurosciences, The Feinstein Institute for Medical Research, Manhasset, NY 11030, USA david1@nshs.edu.

Abstract

Although primary dystonia is defined by its characteristic motor manifestations, non-motor signs and symptoms have increasingly been recognized in this disorder. Recent neuroimaging studies have related the motor features of primary dystonia to connectivity changes in cerebello-thalamo-cortical pathways. It is not known, however, whether the non-motor manifestations of the disorder are associated with similar circuit abnormalities. To explore this possibility, we used functional magnetic resonance imaging to study primary dystonia and healthy volunteer subjects while they performed a motion perception task in which elliptical target trajectories were visually tracked on a computer screen. Prior functional magnetic resonance imaging studies of healthy subjects performing this task have revealed selective activation of motor regions during the perception of 'natural' versus 'unnatural' motion (defined respectively as trajectories with kinematic properties that either comply with or violate the two-thirds power law of motion). Several regions with significant connectivity changes in primary dystonia were situated in proximity to normal motion perception pathways, suggesting that abnormalities of these circuits may also be present in this disorder. To determine whether activation responses to natural versus unnatural motion in primary dystonia differ from normal, we used functional magnetic resonance imaging to study 10 DYT1 dystonia and 10 healthy control subjects at rest and during the perception of 'natural' and 'unnatural' motion. Both groups exhibited significant activation changes across perceptual conditions in the cerebellum, pons, and subthalamic nucleus. The two groups differed, however, in their responses to 'natural' versus 'unnatural' motion in these regions. In healthy subjects, regional activation was greater during the perception of natural (versus unnatural) motion (P < 0.05). By contrast, in DYT1 dystonia subjects, activation was relatively greater during the perception of unnatural (versus natural) motion (P < 0.01). To explore the microstructural basis for these functional changes, the regions with significant interaction effects (i.e. those with group differences in activation across perceptual conditions) were used as seeds for tractographic analysis of diffusion tensor imaging scans acquired in the same subjects. Fibre pathways specifically connecting each of the significant functional magnetic resonance imaging clusters to the cerebellum were reconstructed. Of the various reconstructed pathways that were analysed, the ponto-cerebellar projection alone differed between groups, with reduced fibre integrity in dystonia (P < 0.001). In aggregate, the findings suggest that the normal pattern of brain activation in response to motion perception is disrupted in DYT1 dystonia. Thus, it is unlikely that the circuit changes that underlie this disorder are limited to primary sensorimotor pathways.

KEYWORDS:

DYT1 dystonia; diffusion tensor imaging; functional MRI; motion perception; two-thirds power law

PMID:
26419798
PMCID:
PMC4840548
DOI:
10.1093/brain/awv282
[Indexed for MEDLINE]
Free PMC Article

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