Abstract

Individuals learn both from the outcomes of their own internally generated actions (“experiential learning”) and from the observation of the consequences of externally generated actions (“observational learning”). While neuroscience research has focused principally on the neural mechanisms by which brain structures such as the ventromedial prefrontal cortex (vmPFC) support experiential learning, relatively less is known regarding how learning proceeds through passive observation. We explored the necessity of the vmPFC for observational learning by testing a group of patients with damage to the vmPFC as well as demographically matched normal comparison and brain-damaged comparison groups—and a single patient with bilateral dorsal prefrontal damage—using several value-learning tasks that required learning from direct experience, observational learning, or both. We found a specific impairment in observational learning in patients with vmPFC damage manifest in the reduced influence of previously observed rewards on current choices, despite a relatively intact capacity for experiential learning. The current study provides evidence that the vmPFC plays a critical role in observational learning, suggests that there are dissociable neural circuits for experiential and observational learning, and offers an important new extension of how the vmPFC contributes to learning and memory.

Highlights

  • To make optimal decisions, individuals must learn the value of stimuli in an ever-changing environment and use this information to guide choice behavior

  • We considered the overall performance of the ventromedial prefrontal cortex (vmPFC) patient cohort in phase 4, where learning was dependent solely on the observation of reward outcomes associated with the actions of a computer player during WATCH trials, which was known to be playing in the same environment but whose choices were random

  • Our neuropsychological study investigated the contribution of the vmPFC to experiential and observational learning—a distinction operationalized here as the ability to update stimulus values based on the rewarding outcomes that follow either internally generated or externally generated actions

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Summary

Introduction

Individuals must learn the value of stimuli in an ever-changing environment and use this information to guide choice behavior. While much research has been conducted regarding the role of the ventromedial prefrontal cortex (vmPFC) in value-guided choices based on learning from the consequences of one’s own actions (Damasio et al 1990; Damasio 1994; Bechara et al 2000; Rolls 2004; Rangel et al 2008; Kable and Glimcher 2009; Rushworth et al 2011; Rudebeck and Murray 2011a), less is understood about the neural mechanisms by which individuals learn the value of stimuli in the environment through the passive observation of externally generated actions and their consequences. Our procedure has closer parallels with experimental paradigms used to investigate the differential contributions of the striatum and hippocampus to feedback-based and observational learning, respectively, in the memory literature (Poldrack et al 2001; Shohamy et al 2004)—and the “ghost” conditions used previously to examine the nonsocial components of observational learning—for example, where the observer passively watches a remotely controlled door being moved randomly either to the right or to the left by an experimenter to reveal a food reward (Hopper et al 2008; Hopper 2010)

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