Activity of striatal neurons reflects social action and own reward

Abstract

Social interactions provide agents with the opportunity to earn higher benefits than when acting alone and contribute to evolutionary stable strategies. A basic requirement for engaging in beneficial social interactions is to recognize the actor whose movement results in reward. Despite the recent interest in the neural basis of social interactions, the neurophysiological mechanisms identifying the actor in social reward situations are unknown. A brain structure well suited for exploring this issue is the striatum, which plays a role in movement, reward, and goal-directed behavior. In humans, the striatum is involved in social processes related to reward inequity, donations to charity, and observational learning. We studied the neurophysiology of social action for reward in rhesus monkeys performing a reward-giving task. The behavioral data showed that the animals distinguished between their own and the conspecific's reward and knew which individual acted. Striatal neurons coded primarily own reward but rarely other's reward. Importantly, the activations occurred preferentially, and in approximately similar fractions, when either the own or the conspecific's action was followed by own reward. Other striatal neurons showed social action coding without reward. Some of the social action coding disappeared when the conspecific's role was simulated by a computer, confirming a social rather than observational relationship. These findings demonstrate a role of striatal neurons in identifying the social actor and own reward in a social setting. These processes may provide basic building blocks underlying the brain's function in social interactions.

Fig. 1.

Reward-giving task and behavioral results. (A) Experimental setup. Two monkeys sat opposite each other at a horizontal computer touch screen, each holding a resting key. On each trial, light gray and black backgrounds indicated actor and conspecific roles to the respective animals. (B) Task sequence: shape of conditioned cue predicted absence (square) or presence (circle) of reward for each animal (yellow for left, purple for right animal). Appearance of a subsequent blue go signal was followed by key release, stimulus touch and reward for actor, and 1 s later for conspecific. (C) The four reward conditions used: reward for neither, own reward only, conspecific's reward only, and reward for both. (D) Mean reaction times for the four reward conditions (from go signal to stimulus touch) between the two animals. Error bars show SEM. (E) Eye fixation density between onset of conditioned stimuli and go signal. (F) Eye fixation density on conspecific's face and spout after reward delivery to conspecific.

Fig. 2.

Coding of reward and actor in striatal neurons. (A and B) Activations coding own reward irrespective of actor. (A) Single neuron (activation after feedback onset). (B) Population; n = 20 activations showing increased activity with own reward presence (red-green) compared with no own reward (purple-blue). Activity was normalized to maximum firing rate of individual neurons irrespective of trial type and is shown as impulse density. (C and D) Coding of own action and own reward: higher activations with own compared with conspecific's action in single neuron (C; activation after cue onset) and population (D; n = 28). (E and F) Coding of conspecific's action for own reward in single neuron (E; activations after feedback onset) and population (F; n = 15). Interrupted axes underneath B, D, and F indicate noncontinuous analysis periods and are labeled in F.

Fig. 3.

Sensitivity to actor in striatal neurons not coding reward and neuronal ROC. (A and B) Coding of own action (solid lines) compared with conspecific's action (dashed lines) in single neuron (A) and population (B; n = 57). Overlapping solid lines suggest lack of reward coding. (C and D) Coding of conspecific's action (dashed lines) rather than own action (solid lines) in single neuron (C) and population (D; n = 23). Overlapping dashed lines suggest lack of reward coding. (E) Neuronal ROC values for own reward vs. actor. Reward ROC varies between 0 and 1 for no reward vs. own reward and actor ROC varies between 0 and 1 for own action vs. conspecific’s action. (F) Same as E but for conspecific's reward vs. actor. Gray bars indicate 95% bootstrap CI. Number of members on each group for G and H (permutation test, P < 0.05): green rhomboids (n = 73), own reward and not actor; yellow squares (n = 11), conspecific's reward and not actor; turquoise triangles (n = 23), own and conspecific's reward and not actor; purple triangles (n = 61), own reward and actor; dark blue crosses (n = 3), conspecific's reward and actor; blue stars (n = 118), not reward but actor; pink triangles (n = 45), all categories; red dots (n = 122), all insignificant.

Fig. 4.

Decrease of neuronal distinction between own and conspecific's action during computer control test. (A) Higher activation with own action compared with conspecific's action (Left) decreased when conspecific was replaced by computer (Center). The difference recovered with reinstatement of conspecific (Right). Data are from a single striatal neuron. (B) Same as A, but higher activation with conspecific's action. (C) Kolmogorov-Smirnov statistics (D) for influence of computer opponent on actor specific neuronal responses. Empty bars, decreased difference own vs. conspecific's action with computer (9 activations); filled bars, maintained difference own vs. conspecific's action with computer (13 activations). (D and E) Simple action relationships fail to explain neuronal sensitivity for social action (D, average of 58 activations coding own social action; E, 36 activations coding conspecific's social action). Solid bars represent population activity during action of recorded monkey (normalized to maximum firing rate of individual neurons irrespective of trial type). Dashed bars represent activity in recorded monkey during conspecific's action. Response inhibition refers to absence of movements of recorded monkey. In No response inhibition trials, the recorded animal performed movements without being required. In D, neuronal activity was high in own trials but low in conspecific's trials irrespective of own inhibition. In E, neuronal activity was low in own trials but high in conspecific trials irrespective of own movement. Error bars show SEM.