An integrated framework for the role of oxytocin in multistage social decision-making

Abstract

<p class="first" id="P1">Interest in the effects of oxytocin on social behavior has persisted even as an overarching theory describing these effects has remained largely elusive. Some of the earliest studies on the effects of oxytocin on social decision-making indicated that oxytocin might enhance prosocial actions directed towards others. This led to development of the prosocial hypothesis, which stipulates that oxytocin specifically enhances prosocial choices. However, further work indicated that oxytocin administration could elicit antisocial behaviors as well in certain social situations, highlighting the importance of context-dependent effects. At least two prominent hypotheses have been used to explain these seemingly contradictory findings. The social salience hypothesis indicates that the effects of oxytocin can be conceptualized as a general increase in the salience of social stimuli in the environment. Distinctly, the approach/withdrawal hypothesis stipulates that oxytocin enhances approach behaviors and decreases withdrawal behaviors. These phenomenologically motivated hypotheses regarding the effects of oxytocin on social behavior have created controversies in the field. In this review, we present a multistage framework of social decision-making designed to unify these disparate theories in a process common to all social decisions. We conceptualize this process as involving multiple distinct computational steps, including sensory input, sensory perception, valuation, decision formulation, and behavioral output. Iteratively, these steps generate social behaviors, and oxytocin could be acting on any of these steps to exert its effects. In support of this framework, we examine both behavioral and neural evidence across rodents, non-human primates, and humans, determining at what point in our multistage framework oxytocin could be eliciting its socially relevant effects. Finally, we postulate based on our framework that the prosocial, social salience, and approach/withdrawal hypotheses may not be mutually exclusive and could explain the influence of oxytocin on social behavior to different extents depending on context. </p><p id="P2"> <div class="figure-container so-text-align-c"> <img alt="" class="figure" src="/document_file/f1e80e62-e733-483b-b352-2e2c4ba194b8/PubMedCentral/image/nihms932964u1.jpg"/> </div> </p>