Although the basal ganglia play an important role in self-generated movement, their involvement in externally paced voluntary movement is less clear. We recorded local field potentials (LFPs) from the region of the subthalamic nuclei of eight patients with Parkinson's disease during the performance of a warned reaction time task in which an imperative cue instructed the subject to move or not to move. In 'go' trials, LFP activity in the beta frequency band ( approximately 20 Hz) decreased prior to movement, with an onset latency that strongly correlated with mean reaction time across patients. This was followed by a late post-movement increase in beta power. In contrast, in 'nogo' trials the beta power drop following imperative signals was prematurely terminated compared with go trials and reversed into an early beta power increase. These differences were manifest as power increases when go trials were subtracted from nogo trials. In six patients these relative beta power increases in nogo-go difference trials were of shorter latency than the respective reaction time. The findings suggest that, firstly, the subthalamic nucleus is involved in the preparation of externally paced voluntary movements in humans and, secondly, the degree of synchronization of subthalamic nucleus activity in the beta band may be an important determinant of whether motor programming and movement initiation is favoured or suppressed.

We test the hypothesis that interaction between the human basal ganglia and cerebral cortex involves activity in multiple functional circuits characterized by their frequency of oscillation, phase characteristics, dopamine dependency and topography. To this end we took recordings from macroelectrodes (MEs) inserted into the subthalamic nucleus (STN) in eight awake patients following functional neurosurgery for Parkinson's disease. An EEG was also recorded, as were the signals from MEs in the globus pallidus interna (GPi) in two of the cases. Coherence between EEG and ME potentials was apparent in three major frequency bands, 2-10 Hz, 10-30 Hz and 70-85 Hz. These rhythmic activities differed in their cortical topography, although coherence was always strongest over the midline. Coherence between EEG and ME potentials in the 70-85 Hz band was only recorded in patients treated with levodopa. Cortical activity phase led that in the basal ganglia in those oscillatory activities with frequencies <30 Hz. In contrast, STN and GPi phase led cortex in the 70-85 Hz band. The temporal differences in the way in which cortical activity led or lagged behind that in STN/GPi were similar, around 20 ms, regardless of the overall direction of information flow and frequency band. We conclude that the basal ganglia may receive multiple cortical inputs at frequencies <30 Hz and, in the presence of dopaminergic activity, produce a high frequency drive back to the cerebral cortex, in particular the supplementary motor area (SMA).

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We investigate the extent to which functional circuits coupling cortical and subthalamic activity are multiple and segregated by frequency in untreated Parkinson's disease (PD). To this end, we recorded EEG and local field potentials (LFPs) from macroelectrodes inserted into the subthalamic nucleus area (SA) in nine awake patients following functional neurosurgery for PD. Patients were studied after overnight withdrawal of medication. Coherence between EEG and SA LFPs was apparent in the theta (3-7 Hz), alpha (8-13 Hz), lower beta (14-20 Hz) and upper beta (21-32 Hz) bands, although activity in the alpha and upper beta bands dominated. Theta coherence predominantly involved mesial and lateral areas, alpha and lower beta coherence the mesial and ipsilateral motor areas, and upper beta coherence the midline cortex. SA LFPs led EEG in the theta band. In contrast, EEG led the depth LFP in the lower and upper beta bands. SA LFP activity in the alpha band could either lead or lag EEG. Thus there are several functional sub-loops between the subthalamic area and cerebral cortical motor regions, distinguished by their frequency, cortical topography and temporal relationships. Tuning to distinct frequencies may provide a means of marking and segregating related processing, over and above any anatomical segregation of processing streams.

The speed with which one reacts to an imperative signal depends on the extent to which preceding cues predict that command. When reliable warning cues are available, the processing of the imperative stimulus can be favoured and responses partially pre-prepared, leading to shorter reaction times. Here we seek evidence for involvement of the human basal ganglia in the exploitation of behaviourally relevant predictive cues. To this end, local field potentials (LFPs) were recorded in the region of the subthalamic nuclei of parkinsonian patients during the performance of a pre-cued reaction task in which the cue either predicted or failed to predict the demands of the imperative signal. We demonstrate that LFP activity in the beta frequency band ( approximately 20 Hz) is modulated by the behavioural relevance of the external cue. The findings suggest that, first, the subthalamic nucleus is involved in mediating or facilitating the response advantage derived from predictive cues in humans and, secondly, variations in synchronous neuronal activity in the beta band may contribute to this function in the subthalamic nucleus.