Pallidal spiking activity reflects learning dynamics and predicts performance.
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 attention-demanding 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.
Edmond and Lily Safra Centre for Brain Sciences, The Hebrew University of Jerusalem, Safra Campus, Jerusalem, Israel 9190401; eitan.schechtman@mail.huji.ac.il.
Eitan
0000-0002-8127-012X
E
Schechtman
Department of Neurobiology, Institute of Medical Research-Israel Canada, Hadassah Medical School, The Hebrew University of Jerusalem, Jerusalem, Israel 9112001.
Maria Imelda
MI
Noblejas
Department of Neurobiology, Institute of Medical Research-Israel Canada, Hadassah Medical School, The Hebrew University of Jerusalem, Jerusalem, Israel 9112001.
Aviv D
AD
Mizrahi
Department of Neurobiology, Institute of Medical Research-Israel Canada, Hadassah Medical School, The Hebrew University of Jerusalem, Jerusalem, Israel 9112001.
Omer
O
Dauber
Edmond and Lily Safra Centre for Brain Sciences, The Hebrew University of Jerusalem, Safra Campus, Jerusalem, Israel 9190401; Department of Neurobiology, Institute of Medical Research-Israel Canada, Hadassah Medical School, The Hebrew University of Jerusalem, Jerusalem, Israel 9112001.
Hagai
H
Bergman
D000200:Action Potentials; D000818:Animals; D001522:Behavior, Animal; D002522:Chlorocebus aethiops; D003342:Corpus Striatum / Q000502:physiology; D005260:Female; D005917:Globus Pallidus / Q000502:physiology*; D007858:Learning / Q000502:physiology*; D009434:Neural Pathways; D012201:Reward
actor–critic model; attention; basal ganglia; globus pallidus; learning
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