A shift from prospective to reactive modulation of beta-band oscillations in Parkinson's disease Erik S. te Woerd a,b , Robert Oostenveld b , Floris P. de Lange b , Peter Praamstra a,b, ⁎ a Radboud University Medical Centre, Dept. of Neurology, Radboud University Nijmegen, Nijmegen, The Netherlands b Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, The Netherlands abstract article info Article history: Accepted 16 June 2014 Available online 24 June 2014 Keywords: Basal ganglia Entrainment MEG Neural oscillations Parkinson's disease Increased beta (13–30 Hz) oscillatory synchrony in basal ganglia–cortical circuits is a physiological characteristic of Parkinson's disease (PD). While the function of the beta rhythm is unknown, there is evidence that its modu- lation serves a predictive role, in preparation of future actions. We investigate the relation between predictive beta modulation and entrainment of brain oscillations in a task inviting behavioral entrainment by a regular task structure. MEG was recorded during a serial choice response task, in a group of 12 PD patients and 12 control subjects. In one condition, the reaction stimuli allowed for temporal preparation only (random condition), while in a second condition (predictable condition) the reaction stimuli allowed both temporal and effector preparation. Reaction times were identical between groups, and both groups benefited equally from the known effector side in the predictable condition. Analysis of oscillatory activity, by contrast, revealed marked differences between groups. In patients, the proportion of preparatory beta power desynchronization preceding the reaction stimuli was significantly smaller than in controls, while the proportion of beta desynchronization following the events was larger. In addition to this shift from prospective to reactive modulation of beta-band oscillations, patients showed a trend to reduced motor cortical pre-stimulus delta phase synchronization, and later gamma power syn- chronization than controls. Delta phase synchronization was, furthermore, significantly correlated with predic- tive beta desynchronization, supporting the relevance of hierarchical coupling between oscillations of different frequencies for the analysis of oscillatory changes in PD. Together, these features of task-related oscillatory activ- ity indicate that entrainment fails to engender the same predictive mode of motor activation in PD patients as in healthy controls. © 2014 Elsevier Inc. All rights reserved. Introduction It is well-established that basal ganglia dysfunction in Parkinson's disease (PD) is accompanied by an excess of oscillatory synchrony in the beta band (for reviews see Boraud et al., 2005; Hammond et al., 2007). This holds true for local field potentials in the basal ganglia and, less frequently observed, cortical beta oscillations measured by means of EEG or MEG (Crowell et al., 2012; Pollok et al., 2012). Correla- tions between clinical improvement and attenuation of STN beta power by dopaminergic medication and/or deep brain stimulation of the STN (Giannicola et al., 2010; Kühn et al., 2008; Ray et al., 2008) have sug- gested that high beta power may contribute to parkinsonian bradykine- sia and rigidity. The possibility of a causal rather than epiphenomenonal relation is supported by evidence that driving of cortical activity at beta frequencies slows down movement (Joundi et al., 2012; Pogosyan et al., 2009). Within the context of research on the basal ganglia and PD, there is recent emphasis on beta modulation having an anticipatory role (Jenkinson and Brown, 2011; Oswal et al., 2012). Beta power is both down-regulated following a cue to prepare a movement, and up- regulated in anticipation of a postural challenge (Androulidakis et al., 2007a). Such features of beta activity underlie the proposal that beta activity in the basal ganglia and cortex may form an “internal likeli- hood index of the need for a novel voluntary action” (Jenkinson and Brown, 2011), driven by salient internal and external cues. The prospec- tive nature of beta power modulation is a feature that beta oscilla- tions share with slow brain potentials such as the readiness potential (RP) and the contingent negative variation (CNV). Indeed, both RP and CNV are sensitive to altered (movement) preparatory processes in PD (Cunnington et al., 1995; Jahanshahi et al., 1995; Praamstra and Pope, 2007; Praamstra et al., 1996a,b; Wascher et al., 1997). The observation that compromised preparatory processes in PD are reflected in slow brain potentials as well as beta oscillations may be more than coincidental, especially if slow brain potentials are due to phase resetting of slow oscillations (Schroeder and Lakatos, 2009; Stefanics et al., 2010). A rapidly accumulating body of work has outlined a hierarchical coupling between oscillations of different frequencies NeuroImage 100 (2014) 507–519 ⁎ Corresponding author at: Radboud University Medical Centre, Dept. of Neurology, PO Box 9101, 6500 HB Nijmegen, The Netherlands. Fax: +31 24 3541122. E-mail address: peter.praamstra@radboudumc.nl (P. Praamstra). http://dx.doi.org/10.1016/j.neuroimage.2014.06.039 1053-8119/© 2014 Elsevier Inc. All rights reserved. Contents lists available at ScienceDirect NeuroImage journal homepage: www.elsevier.com/locate/ynimg