Human basal ganglia recordings from implanted deep brain stimulation electrodes and the microlesion effect

Depth recordings from the basal ganglia of patients suffering from Parkinson’s disease (PD) or dystonia have revealed local field potential (LFP) activity in specific frequency bands. Depth recordings also allow us to study LFP power spectra during different types of limb movements, thus helping to elucidate the role of the basal ganglia in specific motor tasks. Accordingly, we recorded bilateral LFP activity from the subthalamic nucleus (STN) of patients with PD (n = 9) and from the globus pallidus internum (GPi) of patients with dystonia (n = 8). Recordings were taken during the performance of repetitive passive, active and ballistic fast extensions and flexions of the elbow joint and during rest. The first result was that the frequency spectra varied task-specifically in a similar fashion in GPi and STN. The amplitude of the alpha frequency on the contralateral side was significantly higher in ballistic fast movements compared with rest, passive and active performance in both STN and GPi. In conclusion, ballistic fast movements cause synchronized basal ganglia activity in the alpha range. Because this was seen in both patient groups (PD and dystonia) we consider this activity as task-specific rather than disease-related. Introduction Diseases of the basal ganglia (BG) are known to alter the execution of limb movements in a disease-specific fashion. Neuronal coding in the BG occurs in the form of single cell depolarizations and local field potential (LFP) oscillations, which are inherently interconnected (Brown & Williams, 2005). Recordings from the human BG can be made from the subthalamic nucleus (STN) or the globus pallidus internum (GPi) which are targets for permanent deep brain stimulation (DBS) electrodes used as a therapy in Parkinson’s disease (PD) (Bergman et al., 1990; Aziz et al., 1991; Limousin et al., 1995; Krack et al., 2003; Deuschl et al., 2006) and dystonia (Bereznai et al., 2002; Vidailhet et al., 2005; Kupsch et al., 2006). Using this approach, recordings from the BG of patients have previously revealed prominent and synchronized oscillations of the LFPs at different frequencies. Low-frequency oscillations have been observed in patients with primary dystonia where LFPs have prominent power in the 3–12 Hz band within the GPi (Chen et al., 2006). This is in accordance with low-frequency neuronal burst discharge single-cell recordings in dystonia (Starr et al., 2005). In another study it was reported that temporal coupling between the pallidal oscillations and muscle activity was synchronized in the range 3–20 Hz during hypertonic cramps caused by dystonia (Liu et al., 2008). Beta frequency oscillations have been associated with the bradykinetic state of PD patients (Brown & Williams, 2005) as the power in this band is decreased when patients are under dopaminergic medication (Brown et al., 2001; Levy et al., 2002) and the degree of beta-suppression is correlated with a reduction of rigidity and bradykinesia (Kuhn et al., 2009). Higher frequency oscillations (70-Hz band) have been recorded during movements (Gatev et al., 2006; Kempf et al., 2009). The same LFP oscillations have also been confirmed to take place in the rodent STN related to movement (Brown et al., 2002). Subcortical gamma activity may be functionally related to motor cortical gamma activity, as they are phase-coupled (Cassidy et al., 2002; Williams et al., 2002), and both increase with movement (Androulidakis et al., 2007; Ball et al., 2008; Cheyne et al., 2008). In parkinsonism, gamma activity is also increased with dopaminegic therapy along with improvement in motor performance, so it was suggested that synchronized activity of the gamma band in basal ganglia may smooth the progress of motor processing (Brown et al., 2001; Brown, 2003). The movements investigated in the aforementioned studies were mostly finger or joystick movements of similar type. The objective of the current study was therefore to investigate LFPs occurring during repetitive elbow movements involving different velocities, complexity and rate of force production. Furthermore, we wished to investigate whether STN and GPi exhibit similar or different activity during these tasks. Correspondence: Dr K. Bötzel, as above. E-mail: kai.boetzel@med.uni-muenchen.de Received 30 June 2010, revised 29 November 2010, accepted 1 December 2010 European Journal of Neuroscience, Vol. 33, pp. 960–967, 2011 doi:10.1111/j.1460-9568.2010. 07577.x a 2011 The Authors. European Journal of Neuroscience a 2011 Federation of European Neuroscience Societies and Blackwell Publishing Ltd European Journal of Neuroscience