Objective: To identify subcortical neural biomarkers of happiness and reward evaluation through sensing-enabled deep brain stimulation (DBS) in people with Parkinson’s Disease (PwPD).

Background: Integrating risk and reward into expected value (EV) is critical in healthy decision-making, and assessing outcomes via reward prediction errors (RPE) centrally impacts one’s happiness [1]. However, the ability to assess potential rewards and integrate outcomes is altered in PD. Treatment with DBS affords the opportunity to both stimulate and record neural activity from value processing centers in the basal ganglia. Despite evidence of the involvement of the subthalamic nucleus (STN) and globus pallidum (GP) in value assessment [2], their role as well as the effects of DBS on risk and reward outcome evaluation remain unclear.

Method: 20 PwPD with bilateral (n=15) or unilateral (n=5) sensing-enabled Medtronic Percept DBS (10 STN and 10 GP) completed the Rutledge forced choice gambling task in clinic while on dopaminergic medication. Participants chose between a fixed value or a gamble with 50/50 probability of success. Per-trial happiness was estimated with a combination of EV and RPE [1]. Subcortical neural recordings of local field potentials (LFP) were acquired with a wireless Percept tablet. Participants completed six blocks of 30 trials alternating DBS on and off per block, counterbalanced across people.  Baseline-corrected average theta (3-7Hz) and high beta (13-30Hz) power was calculated from LFP data 0.5 to 1.5 seconds after result outcome.

Results: STN theta power following the result of a gamble was significantly higher in trials with higher vs. lower happiness (p=0.02). DBS significantly altered this relationship (p<0.001). This effect was not seen in the GP (p=0.69), showing spatial selectivity of this finding. Furthermore, STN high beta power following a gamble result decreased with increasing unsigned RPE (uRPE) (p=0.02), but this was not seen in the GP (p=0.24).

Conclusion: STN but not GP theta power increases when one is happy with a result, revealing a biomarker in PwPD that tracks momentary happiness. This relationship disappears when DBS is turned on. High beta power in the STN inversely tracks uRPE, which supports the role of a beta biomarker in evaluating surprising outcomes. Together, this work reveals an important role for theta and beta power in the STN during happiness and reward evaluation.

References: [1] Rutledge, Robb B., et al. “A computational and neural model of momentary subjective well-being.” Proceedings of the National Academy of Sciences 111.33 (2014): 12252-12257.
[2] Hoy, Colin W., et al. “Beta and theta oscillations track effort and previous reward in the human basal ganglia and prefrontal cortex during decision making.” Proceedings of the National Academy of Sciences 121.31 (2024): e2322869121.

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MDS Abstracts - https://www.mdsabstracts.org/abstract/theta-and-beta-oscillations-track-happiness-and-surprise-in-the-subthalamic-nucleus-after-reward-outcome/