Novelty-induced frontal-STN networks in Parkinson's disease

Cole, R. C.; Espinoza, A. I.; Singh, A.; Berger, J. I.; Cavanagh, J. F.; Greenlee, J. D.; Narayanan, N. S.

Evaluating and responding to new information requires cognitive control. Here, we studied novelty-response mechanisms in Parkinson's disease (PD). In PD patient-volunteers, we recorded from cortical circuits with scalp-based electroencephalography (EEG) and from subcortical circuits using intraoperative neurophysiology during surgeries for implantation of deep-brain stimulation (DBS) electrodes. We report three major results. First, novel auditory stimuli triggered midfrontal ~4-Hz rhythms, which were attenuated in PD patients but were not linked with cognitive function or novelty-associated slowing. Second, 32% of subthalamic nucleus (STN) neurons were response-modulated; nearly all (94%) of these were also modulated by novel stimuli. Finally, response-modulated STN neurons were coherent with midfrontal low-frequency activity. These findings link scalp-based measurements of neural activity with neuronal activity in the STN. Our results provide insight into midfrontal cognitive control mechanisms and how hyperdirect circuits evaluate new information.