Dopaminergic signaling supports auditory social learning

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.

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Fig: Yoking food reward to an observer facilitates social learning. (A) Replication of Fig. 1 from Paraouty et al. Experimental Design. Left: Naïve observer gerbil (black) was separated from a performing same-sex demonstrator gerbil (brown) by a transparent divider. The demonstrator was previously trained by the experimenters (see “Methods” section for details). Right: Following 5 days of exposure, the practice phase began during which the naïve observer gerbil was permitted to practice the task on its own. (B) Mean ± standard error of the mean (SEM) of the number of Go and Nogo trials performed by the demonstrators (5 males; age = 122.6 ± 4.7 days during the 5 days of exposure (brown), and by the naïve observer gerbils (age = 101.4 ± 4.1) during the practice sessions (black). (C) Mean ± SEM d′ values of the demonstrators during the 5 days of exposure (brown) and of the naïve observer gerbils during the practice sessions (black). The performance sensitivity, d′ was calculated once the observers performed > 15 Nogo trials. (D) Experimental Design. Left: Yoked reward observer gerbil (orange) was separated from a performing demonstrator gerbil (brown) by a transparent divider. A food tray was also present in the observer’s compartment, and the food reward of the demonstrator animal was yoked to that of the observer. Right: Practice session, similar to A (right). (E) similar to B, with demonstrators (4 males; age = 130 ± 4.2) and yoked reward observers (age = 96.8 ± 5.3). (F) Similar to C for the yoked reward observers. For comparison purposes, the observers’ results from 1B and 1C are replicated on Figures (E) and (F), respectively.

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.

Paraouty, N., Rizzuto, C.R. & Sanes, D.H. Dopaminergic signaling supports auditory social learning. Sci Rep 11, 13117 (2021). https://doi.org/10.1038/s41598-021-92524-1

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