Abstract
SEE POSTUMA DOI101093/AWW131 FOR A SCIENTIFIC COMMENTARY ON THIS ARTICLE: Resting state functional magnetic resonance imaging dysfunction within the basal ganglia network is a feature of early Parkinson's disease and may be a diagnostic biomarker of basal ganglia dysfunction. Currently, it is unclear whether these changes are present in so-called idiopathic rapid eye movement sleep behaviour disorder, a condition associated with a high rate of future conversion to Parkinson's disease. In this study, we explore the utility of resting state functional magnetic resonance imaging to detect basal ganglia network dysfunction in rapid eye movement sleep behaviour disorder. We compare these data to a set of healthy control subjects, and to a set of patients with established early Parkinson's disease. Furthermore, we explore the relationship between resting state functional magnetic resonance imaging basal ganglia network dysfunction and loss of dopaminergic neurons assessed with dopamine transporter single photon emission computerized tomography, and perform morphometric analyses to assess grey matter loss. Twenty-six patients with polysomnographically-established rapid eye movement sleep behaviour disorder, 48 patients with Parkinson's disease and 23 healthy control subjects were included in this study. Resting state networks were isolated from task-free functional magnetic resonance imaging data using dual regression with a template derived from a separate cohort of 80 elderly healthy control participants. Resting state functional magnetic resonance imaging parameter estimates were extracted from the study subjects in the basal ganglia network. In addition, eight patients with rapid eye movement sleep behaviour disorder, 10 with Parkinson's disease and 10 control subjects received (123)I-ioflupane single photon emission computerized tomography. We tested for reduction of basal ganglia network connectivity, and for loss of tracer uptake in rapid eye movement sleep behaviour disorder and Parkinson's disease relative to each other and to controls. Connectivity measures of basal ganglia network dysfunction differentiated both rapid eye movement sleep behaviour disorder and Parkinson's disease from controls with high sensitivity (96%) and specificity (74% for rapid eye movement sleep behaviour disorder, 78% for Parkinson's disease), indicating its potential as an indicator of early basal ganglia dysfunction. Rapid eye movement sleep behaviour disorder was indistinguishable from Parkinson's disease on resting state functional magnetic resonance imaging despite obvious differences on dopamine transported single photon emission computerized tomography. Basal ganglia connectivity is a promising biomarker for the detection of early basal ganglia network dysfunction, and may help to identify patients at risk of developing Parkinson's disease in the future. Future risk stratification using a polymodal approach could combine basal ganglia network connectivity with clinical and other imaging measures, with important implications for future neuroprotective trials in rapid eye movement sleep behaviour disorder.
Highlights
Significant abnormalities in resting state functional MRI have previously been reported by our group within the basal ganglia network (BGN) of patients with early Parkinson’s disease (Szewczyk-Krolikowski et al, 2014a; Rolinski et al, 2015)
Over the past 20 years, increasing evidence has emerged for idiopathic rapid eye movement (REM) sleep behaviour disorder (RBD), occurring in the absence of any other clinically defined neurological disorder, being associated with the prodromal stages of a number of neurodegenerative conditions, predominantly Parkinson’s disease (Schenck et al, 1996, 2013; Iranzo et al, 2006; Postuma et al, 2009a, b; Boot et al, 2012; Wing et al, 2012)
RBD was defined as an increase in tonic or phasic chin EMG activity during REM sleep and, either history of elaborate motor activity associated with dream content, or the presence of behavioural manifestations occurring during REM sleep during polysomnographic recordings (Lapierre and Montplaisir, 1992)
Summary
Significant abnormalities in resting state functional MRI have previously been reported by our group within the basal ganglia network (BGN) of patients with early Parkinson’s disease (Szewczyk-Krolikowski et al, 2014a; Rolinski et al, 2015). While this approach shows promise as a diagnostic biomarker in the early motor phases of Parkinson’s disease, it is unclear whether these changes are present in prodromal disease. We analysed 123I-ioflupane uptake in a subset of patients, an established surrogate of dopaminergic decline
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