Neural mechanisms of observational learning

Abstract

Individuals can learn by interacting with the environment and experiencing a difference between predicted and obtained outcomes (prediction error). However, many species also learn by observing the actions and outcomes of others. In contrast to individual learning, observational learning cannot be based on directly experienced outcome prediction errors. Accordingly, the behavioral and neural mechanisms of learning through observation remain elusive. Here we propose that human observational learning can be explained by two previously uncharacterized forms of prediction error, observational action prediction errors (the actual minus the predicted choice of others) and observational outcome prediction errors (the actual minus predicted outcome received by others). In a functional MRI experiment, we found that brain activity in the dorsolateral prefrontal cortex and the ventromedial prefrontal cortex respectively corresponded to these two distinct observational learning signals.

Fig. 1.

Experimental design and behavioral results. (A) After a variable ITI, participants were first given the opportunity to observe the confederate player being presented with two abstract fractal stimuli to choose from. After another variable ITI, participants were then presented with the same stimuli, and the trial proceeded in the same manner. When the fixation cross was circled, participants made their choice using the index finger (for left stimulus) and middle finger (for right stimulus) on the response pad. (B) The proportion of correct choices increased with increasing amounts of social information. (C) There was a monotonic increase in the proportion of correct choices as a function of the observability of the other player's behavior and outcomes. Learning from the actions and outcomes of the other player resulted in significantly more correct choices than action only observable and individual learning conditions.

Fig. 2.

Activity in the ventral striatum correlating with individual outcome prediction error. (A) Coronal section showing significant voxels correlating with individual outcome prediction errors (P < 0.05, whole-brain correction). (B) Time course of activity in the ventral striatum binned according to sign of individual outcome prediction error. (C) Linear regression of activity in the ventral striatum against individual outcome prediction errors as expected by the model (red circular markers, P < 0.001, R² = 0.888). To demonstrate that social and nonsocial learning are integrated at the neural level, the gray triangular markers show the regression with expected outcome prediction errors when social information is removed from the model on social learning trials (P = 0.917, R² = 0.001).

Fig. 3.

Activity in the DLPFC correlating with observational action prediction error. (A) Coronal section showing significant voxels correlating with action prediction errors (P < 0.05, SVC for frontal lobe). (B) Time course of activity in DLPFC at the time of the other player's choice, binned according to magnitude of action prediction error. (C) Linear regression of activity in DLPFC with action prediction errors expected by the model (red circular markers, P < 0.001, R² = 0.773).

Fig. 4.

Activity in VMPFC and ventral striatum corresponding to observational outcome prediction errors during the outcome of the other player. (A) Coronal section showing significant voxels correlating with observational outcome prediction errors in VMPFC [P < 0.05, SVC for 30 mm around coordinates of reported peak in O'Doherty et al. (38)]. (B) Time course of activity in VMPFC during the outcome of the other player, binned according to sign of observed outcome prediction errror. (C) Linear regression of activity in VMPFC at the time of the other player's outcome with expected observational outcome prediction errors (red circular markers, P < 0.002, R² = 0.719). (D) Coronal section showing significant voxels correlating with inverse observational outcome prediction errors in ventral striatum (P < 0.003, SVC). (E) Time course of activity in ventral striatum during the outcome of the other player, binned according to sign of observational prediction errors. (F) Linear regression of activity in ventral striatum at the time of the other player's outcome with expected observational prediction errors (red circular markers, P < 0.03, R² = −0.552).