Beta oscillations in frontal cortex and striatum represent post-processing of successful behavior

Abstract

Beta band (13-30 Hz) oscillations in sensorimotor cortex are associated with motor performance, but the nature of this relationship is not clear. Recently, excessive beta activity in cortico-basal ganglia circuits has been recognized as a hallmark of Parkinson's disease. Renewed interest in beta oscillations has since led to the suggestion that they might reflect the preservation of the current output or state of a given brain region. To investigate the potential role of beta activity in the brain, we recorded local field potentials in the frontal cortex and striatum of monkeys as they performed single and sequential arm movement tasks. To facilitate these experiments, we developed novel methods for recording simultaneously from independently moveable electrodes implanted chronically at over 100 sites in cortical and subcortical areas of the monkey brain. We found that, across tasks, beta oscillations occurred in brief, spatially localized bursts that were most prominent following task performance. Across brain regions, post-performance bursts were differentially modulated by the preceding task. In motor cortex they tracked the number of movements just performed. In contrast, striatal and prefrontal burst rates were proportional to the number of visual cues, or to a combination of the cues and movements, respectively, and were higher following correct, rewarded, trials than unrewarded errors. Pairs of striatal-prefrontal sites exhibited increased cross-covariance and coherence during post-trial beta bursts, suggesting that these bursts might be involved in communication or coordination across brain regions. Based on our results, we propose that beta oscillations may represent post-performance reinforcement of the network dynamics that led to the desired behavioral outcome obtained immediately prior.