High beta power in the ventrolateral prefrontal cortex indexes human approach behavior: a case study.

Abstract

Deep brain stimulation (DBS) of the ventral capsule and ventral striatum (VC/VS) is an effective therapy for treatment resistant obsessive-compulsive disorder (trOCD). DBS initiation often produces acute improvements in mood and energy. These acute behavioral changes, which we refer to as "approach behaviors", include increased social engagement and talkativeness. We investigated the relationship between stimulation amplitude, spectral power in the ventrolateral prefrontal cortex (vlPFC), and speech rate in one male patient with trOCD implanted with bilateral VC/VS DBS leads and subdural electrodes adjacent to orbitofrontal cortex (OFC) and vlPFC. Several times over the first 17 weeks of therapy, we conducted experiments where we recorded data during epochs of high amplitude or zero/low amplitude stimulation. We found that both speech rate and vlPFC power in a high beta frequency band (31±1.5Hz, 1/f activity removed) increased during high amplitude as compared to low amplitude periods. Speech rate correlated with vlPFC high beta power. These effects were more consistent across time points in the left hemisphere than the right. At week 17, we performed an experiment where stimulation was held constant while the patient was asked to speak or remain silent. We showed that the presence or absence of speech was not sufficient to increase the vlPFC high beta power, suggesting stimulation is a key driver of the observed neurobehavioral phenomenon. Our results suggest vlPFC high beta power is a biomarker for approach behaviors associated with VC/VS DBS.Significance Statement In one patient receiving DBS of the ventral capsule and ventral striatum (VC/VS) for OCD, we leveraged a unique clinical opportunity to study the neurophysiological basis of approach behaviors using chronic intracranial recordings from prefrontal cortical regions. VC/VS DBS initiation often produces acute improvements in mood and energy associated with increased social engagement and talkativeness (approach behaviors). Our results suggest that vlPFC high beta activity (particularly in the left hemisphere) may index approach behaviors (quantified here by speech features). This neural signal is consistent with our previous non-invasive studies identifying predictors of mania in patients with bipolar disorder, and we hope to gather further evidence that it indexes a continuum from adaptive approach behavior to maladaptive manic symptoms.