Anticipating social incentives recruits alpha-beta oscillations in the human substantia nigra and invigorates behavior across the life span

A B S T R A C T Anticipating social and non-social incentives recruits shared brain structures and promotes behavior. However, little is known about possible age-related behavioral changes, and how the human substantia nigra (SN) signals positive and negative social information. Therefore, we recorded intracranial electroencephalography (iEEG) from the SN of Parkinson's Disease (PD) patients ( n = 12, intraoperative, OFF medication) in combination with a social incentive delay task including photos of neutral, positive or negative human gestures and mimics as feedback. We also tested a group of non-operated PD patients ( n = 24, ON and OFF medication), and a sample of healthy young ( n = 51) and older ( n = 52) adults with behavioral readouts only. Behaviorally, the anticipation of both positive and negative social feedback equally accelerated response times in contrast to neutral social feedback in healthy young and older adults. Although this effect was not significant in the group of operated PD patients - most likely due to the small sample size - iEEG recordings in their SN showed a significant increase in alpha -beta power (9-20 Hz) from 300 to 600 ms after cue onset again for both positive and negative cues. Finally, in non-operated PD patients, the behavioral effect was not modulated by medication status (ON vs OFF medication) suggesting that other processes than dopaminergic neuromodulation play a role in driving invigoration by social incentives. Together, our findings provide novel and direct evidence for a role of the SN in processing positive and negative social information via specific oscillatory mechanisms in the alpha-beta range, and they suggest that anticipating social value in simple cue-outcome associations is intact in healthy aging and PD.

Automated summary

The results from intracranial electroencephalography recordings show that anticipating both positive and negative social feedback accelerates response times in healthy young and older adults, while the effect in operated Parkinson's Disease (PD) patients may be influenced by small sample size. The behavioral effect in non-operated PD patients is not modulated by medication status, indicating that processes other than dopaminergic neuromodulation play a role in driving invigoration by social incentives.