Distinct populations of neurons respond to emotional valence and arousal in the human subthalamic nucleus

Significance The involvement of the subthalamic nucleus (STN) in affective processing has been suggested with the appearance of neuropsychiatric side effects of deep brain stimulation in Parkinson’s disease (PD), but direct evidence has been lacking. In our study, we recorded single-neuron activity from the STN during affective picture presentation to PD patients intraoperatively. We discovered two spatially distinct populations of “affective” neurons responding to the emotional dimensions of the stimuli: valence (pleasantness-unpleasantness) and arousal (intensity). As previously believed, neural circuits underlying these two affective dimensions are functionally segregated. Here we observed separated emotional processing even at the single neuron level. These results extend our knowledge regarding the emotional role of the STN and the neural basis of emotions. Both animal studies and studies using deep brain stimulation in humans have demonstrated the involvement of the subthalamic nucleus (STN) in motivational and emotional processes; however, participation of this nucleus in processing human emotion has not been investigated directly at the single-neuron level. We analyzed the relationship between the neuronal firing from intraoperative microrecordings from the STN during affective picture presentation in patients with Parkinson’s disease (PD) and the affective ratings of emotional valence and arousal performed subsequently. We observed that 17% of neurons responded to emotional valence and arousal of visual stimuli according to individual ratings. The activity of some neurons was related to emotional valence, whereas different neurons responded to arousal. In addition, 14% of neurons responded to visual stimuli. Our results suggest the existence of neurons involved in processing or transmission of visual and emotional information in the human STN, and provide evidence of separate processing of the affective dimensions of valence and arousal at the level of single neurons as well.