Abstract

Explicit rewards are commonly used to reinforce a behavior, a form of learning that engages the dopaminergic neuromodulatory system. In contrast, skill acquisition can display dramatic improvements from a social learning experience, even though the observer receives no explicit reward. Here, we test whether a dopaminergic signal contributes to social learning in naïve gerbils that are exposed to, and learn from, a skilled demonstrator performing an auditory discrimination task. Following five exposure sessions, naïve observer gerbils were allowed to practice the auditory task and their performance was assessed across days. We first tested the effect of an explicit food reward in the observer’s compartment that was yoked to the demonstrator’s performance during exposure sessions. Naïve observer gerbils with the yoked reward learned the discrimination task significantly faster, as compared to unrewarded observers. The effect of this explicit reward was abolished by administration of a D1/D5 dopamine receptor antagonist during the exposure sessions. Similarly, the D1/D5 antagonist reduced the rate of learning in unrewarded observers. To test whether a dopaminergic signal was sufficient to enhance social learning, we administered a D1/D5 receptor agonist during the exposure sessions in which no reward was present and found that the rate of learning occurred significantly faster. Finally, a quantitative analysis of vocalizations during the exposure sessions suggests one behavioral strategy that contributes to social learning. Together, these results are consistent with a dopamine-dependent reward signal during social learning.

Highlights

  • Explicit rewards are commonly used to reinforce a behavior, a form of learning that engages the dopaminergic neuromodulatory system

  • As described p­ reviously[46], demonstrator gerbils were first trained by an experimenter to perform a Go-Nogo amplitude modulation (AM) rate discrimination task

  • Dopamine signaling plays a broad role in learning that results in acquisition of explicit r­ ewards[49], suggesting that it may play a general role in social forms of learning that do not yield an immediate reward

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Summary

Introduction

Explicit rewards are commonly used to reinforce a behavior, a form of learning that engages the dopaminergic neuromodulatory system. We test whether a dopaminergic signal contributes to social learning in naïve gerbils that are exposed to, and learn from, a skilled demonstrator performing an auditory discrimination task. Naïve observer gerbils with the yoked reward learned the discrimination task significantly faster, as compared to unrewarded observers The effect of this explicit reward was abolished by administration of a D1/D5 dopamine receptor antagonist during the exposure sessions. To test whether a dopaminergic signal was sufficient to enhance social learning, we administered a D1/D5 receptor agonist during the exposure sessions in which no reward was present and found that the rate of learning occurred significantly faster. To test the hypothesis that social learning engages a dopamine-dependent reward signal that facilitates the subsequent acquisition of an auditory task, we used pharmacological loss- and gain-of-function manipulations of D1/D5 dopamine receptors in naïve observer gerbils during exposure sessions. The results suggest that dopaminergic signaling is both necessary and sufficient to facilitate socially-mediated task acquisition and one important social cue is the demonstrators’ vocalizations at trial initiation

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