Modulation of relative aversive and safety learning by D2-expressing neurons of the anterior paraventricular nucleus of the thalamus

Abstract

Associative learning provides a means to assign appropriate value signals to experiences that animals can later use to make appropriate value-based choices. By generalizing from prior aversive experiences and comparing them with a current experience, animals can learn the relative aversive (“better or worse than”) value or relative positive safety value between experiences. Yet, how such relative value signals are acquired during learning remains poorly known. The paraventricular nucleus of the thalamus (PVT) is critical for the control of salience and valence signals. It is therefore well placed to be involved in learning relative aversive value and learned safety. Using newly developed conditioned place-preference tasks, we uncover specific behavioral signatures associated with learning relative aversive value and learned safety, as well as related value-based choices. We then show that neurons expressing dopamine D2 receptor (D2+) in the anterior PVT (aPVT) are preferentially recruited by both relative aversive value learning and learned safety. Using pharmacogenetic strategies, we demonstrate that aPVT D2+, but not D2−, neurons are required for learning relative—but not absolute—aversive value. Finally, we show that aPVT D2+, but not D2−, neurons contribute to the encoding of learned safety. Overall, our findings reveal a novel role of aPVT D2+ neurons in computing relative aversive/safety value signals between experiences during learning to promote appropriate value-based choices.