Computational mechanisms dealing with gains and losses in reinforcement learning

Social dominance is a powerful modulator of behavior in animals that form hierarchical societies, such as monkeys. Social rank significantly affects priority over food so that subordinate monkeys often suppress reaching it when with dominant conspecifics. This behavior requires integrating reward and social rank information to determine motor behavior, but its underlying neural mechanisms are still elusive. The caudate nucleus (CD) of the basal ganglia is known to play a pivotal role in representing reward expectation and translating it to actions. To investigate whether CD activities also encode social rank, we recorded from the CD as monkeys reached for food in a naturalistic setting designed to evoke dominant and subordinate behaviors. A monkey and a human competitor were seated side-by-side facing a round table, on which food pellets were placed at various locations and retrieved by monkey or human. When food was placed between competitors, human behavior was either competitive (actively retrieving the food) or passive, alternating across blocks. During competitive blocks, monkeys exhibited subordinate behavior and suppressed hand movements; otherwise, monkeys exhibited dominant behavior and readily retrieved the food. Analyzing recorded activities, we found a group of CD neurons with activities primarily related to reward expectation, as described in previous studies. We further found another group of CD neurons that had higher activity when the animal was in a dominant state; their activities had significant preference to trials of the non-competitive block, irrespective of the location of food placement, and were not modulated by reward expectation as tested in a control, non-social experiment. These results suggest that the neurons of the second group signal a state of lower social inhibition the dominant state. With these activities, the CD can contribute to determining a final motor behavior based on both reward expectation and social rank information.