Movement Disorder Patients with Depression have Altered Corticostriatal Alpha-Beta Power Response to Reward and Loss

Depression is a common comorbidity in movement disorders such as Parkinson’s disease (PD) and essential tremor (ET). Altered reward signaling contributes to core depression symptoms such as anhedonia, but the specific neural activity patterns underlying these processes and how they manifest in comorbid movement disorders are incompletely understood. Fourteen PD patients and 16 ET patients (22 male, 8 female) participated while undergoing deep brain stimulation surgery. Subjects completed a working memory task and received visual feedback about response accuracy while signals were recorded from traversed structures (caudate and/or dorsolateral prefrontal cortex (DLPFC)). Preoperative Beck Depression Inventory-II (BDI-II) scores of ≥14 indicated elevated depression symptoms. Using cluster-based permutation testing, we identified time and frequency ranges in which oscillatory power significantly differed during reward versus loss feedback. We then used two-way ANOVAs and linear mixed effects models to assess how these power changes differed based on movement disorder and depression severity. Caudate and DLPFC alpha-beta (8-30 Hz) power increased during reward feedback. In both regions, this increase was attenuated in depressed subjects [caudate difference=-0.22, 95% CI=-0.32 to -0.13; DLPFC difference=-0.10, 95% CI=-0.16 to -0.045]. BDI-II score was a negative predictor of reward- and loss-related corticostriatal alpha-beta power [caudate estimate=-0.014, 95% CI=-0.020 to -0.0078; DLPFC estimate=-0.0075, 95% CI=-0.012 to -0.0029]. Specific to PD, depressed patients had greater decreases in DLPFC alpha-beta power following loss feedback than non-depressed patients [difference=-0.10, 95% CI=-0.17 to -0.027]. Our findings suggest that altered corticostriatal alpha-beta power may contribute to reward dysfunction in depression in patients with movement disorders. Significance statement Depression is prevalent in both the general population and patients with movement disorders such as Parkinson’s disease (PD) and essential tremor (ET). Imaging studies have suggested that patients with depression have altered reward processing, but our understanding of the neural activity underlying this effect and its manifestation in comorbid neurological disorders is limited. Using intracranial EEG recordings in movement disorder patients, we show that depression symptom severity predicts altered corticostriatal alpha-beta oscillatory power (8-30 Hz) reward signaling and that depressed PD patients show heightened alpha-beta power response to loss feedback. Our findings implicate alpha-beta power attenuation within corticostriatal circuits as a potential therapeutic target for guiding novel treatment development for treatment-resistant depression and the comorbid depression symptoms of movement disorders.