Social reward monitoring and valuation in the macaque brain

Abstract

Behaviors are influenced by rewards to both oneself and others, but the neurons and neural connections that monitor and evaluate rewards in social contexts are unknown. To address this issue, we devised a social Pavlovian conditioning procedure for pairs of monkeys. Despite being constant in amount and probability, the subjective value of forthcoming self-rewards, as indexed by licking and choice behaviors, decreased as partner-reward probability increased. This value modulation was absent when the conspecific partner was replaced by a physical object. Medial prefrontal cortex neurons selectively monitored self-reward and partner-reward information, whereas midbrain dopaminergic neurons integrated this information into a subjective value. Recordings of local field potentials revealed that responses to reward-predictive stimuli in medial prefrontal cortex started before those in dopaminergic midbrain nuclei and that neural information flowed predominantly in a medial prefrontal cortex-to-midbrain direction. These findings delineate a dedicated pathway for subjective reward evaluation in social environments.

Representation of distinct reward variables for self and other in primate lateral hypothalamus

“…This finding indicates that the value of one's own reward is subjectively lowered by a higher incidence of rewards to conspecifics. Note that, in our behavioral procedure, the order of outcome revelation and the context of resource limitation were both critical factors for the emergence of subjective value modulation, as reported previously (18).…”

“…What might be the impact of partner's reward contexts on LH activity? We previously reported that subjective value modulation, as indexed by the licking movement, was absent in the M2variable block when the partner monkey was replaced with a water-collecting bottle (18). We also reported that the subjective value modulation, as indexed by the licking and choice behaviors, was significantly attenuated or absent in the M2-variable block when the partner monkey was present in front of M1 but was deprived of access to a reward (18).…”

“…We previously showed that the MPFC, a hub of social brain networks (20), contains both self-type cells and partner-type cells in the reward domain (18). Therefore, it is tempting to hypothesize that the LH is functionally coordinated with the MPFC.…”

“…To address these issues, we introduced a Pavlovian conditioning procedure extended to a self-and-other context using pairs of monkeys (18) and recorded neural activity from one monkey in each pair. In this procedure, we incorporated aspects of social comparison (19) and resource limitation by manipulating reward probabilities for self and other.…”

Autonomic arousal tracks outcome salience not valence in monkeys making social decisions

“…In this behavioral paradigm, neurons in the rostral anterior cingulate gyrus (ACCg) code the chosen social outcome 7 and neurons in the amygdala code the value of juice amount similarly regardless of whether it is delivered to the self or the other monkey, but not when it is delivered to a jar in the nonsocial control condition 8 . In a similar paradigm, researchers found neurons in the dorsal convexity of the medial prefrontal cortex that selectively coded reward for either the actor monkey or a partner monkey 9 .…”