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Encoding of Probabilistic Rewarding and Aversive Events by Pallidal and Nigral Neurons

¹Department of Physiology, The Hebrew University–Hadassah Medical School; and ²The Interdisciplinary Center for Neural Computation and ³Eric Roland Center for Neurodegenerative Diseases, The Hebrew University, Jerusalem, Israel

Submitted 14 July 2008; accepted in final form 1 December 2008

Previous studies have rarely tested whether the activity of high-frequency discharge (HFD) neurons of the basal ganglia (BG) is modulated by expectation, delivery, and omission of aversive events. Therefore the full value domain encoded by the BG network is still unknown. We studied the activity of HFD neurons of the globus pallidus external segment (GPe, n = 310), internal segment (GPi, n = 149), and substantia nigra pars reticulata (SNr, n = 145) in two monkeys during a classical conditioning task with cues predicting the probability of food, neutral, or airpuff outcomes. The responses of BG HFD neurons were long-lasting and diverse with coincident increases and decreases in discharge rate. The population responses to reward-related events were larger than the responses to aversive and neutral-related events. The latter responses were similar, except for the responses to actual airpuff delivery. The fraction of responding cells was larger for reward-related events, with better discrimination between rewarding and aversive trials in the responses with an increase rather than a decrease in discharge rate. GPe and GPi single units were more strongly modulated and better reflected the probability of reward- than aversive-related events. SNr neurons were less biased toward the encoding of the rewarding events, especially during the outcome epoch. Finally, the latency of SNr responses to all predictive cues was shorter than the latency of pallidal responses. These results suggest preferential activation of the BG HFD neurons by rewarding compared with aversive events.