Pallidal spiking activity reflects learning dynamics and predicts performance

Eitan Schechtman*, Maria Imelda Noblejas, Aviv D. Mizrahi, Omer Dauber, Hagai Bergman

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

19 Scopus citations

Abstract

The basal ganglia (BG) network has been divided into interacting actor and critic components, modulating the probabilities of different state-action combinations through learning. Most models of learning and decision making in the BG focus on the roles of the striatum and its dopaminergic inputs, commonly overlooking the complexities and interactions of BG downstream nuclei. In this study, we aimed to reveal the learning-related activity of the external segment of the globus pallidus (GPe), a downstream structure whose computational role has remained relatively unexplored. Recording from monkeys engaged in a deterministic three-choice reversal learning task, we found that changes in GPe discharge rates predicted subsequent behavioral shifts on a trial-by-trial basis. Furthermore, the activity following the shift encoded whether it resulted in reward or not. The frequent changes in stimulus-outcome contingencies (i.e., reversals) allowed us to examine the learning-related neural activity and show that GPe discharge rates closely matched across-trial learning dynamics. Additionally, firing rates exhibited a linear decrease in sequences of correct responses, possibly reflecting a gradual shift from goal-directed execution to automaticity. Thus, modulations in GPe spiking activity are highest for attentiondemanding aspects of behavior (i.e., switching choices) and decrease as attentional demands decline (i.e., as performance becomes automatic). These findings are contrasted with results from striatal tonically active neurons, which show none of these task-related modulations. Our results demonstrate that GPe, commonly studied in motor contexts, takes part in cognitive functions, in which movement plays a marginal role.

Original languageAmerican English
Pages (from-to)E6281-E6289
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue number41
DOIs
StatePublished - 11 Oct 2016

Bibliographical note

Funding Information:
The authors thank the anonymous referees for extremely helpful remarks and acknowledge the contributions of Sharon Freeman, Zvi Israel, Anatoly Shapochnikov, and Hila Gabbay to this project. This work was supported by research grants from the European Research Council, the Israel Science Foundation, the United States-Israel Binational Science Foundation, the German-Israeli Foundation for Scientific Research and Development, the Adelis Foundation, the Rosetrees Trust, and the Vorst Foundation. E.S. is a fellow of the Harry and Silvia Hoffman leadership program and the Adams Fellowship Program of the Israel Academy of Sciences.

Keywords

  • Actor-critic model
  • Attention
  • Basal ganglia
  • Globus pallidus
  • Learning

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