Harm to Others Acts as a Negative Reinforcer in Rats.

Julen Hernandez-Lallement,Cindy M Pinhal,Valeria Gazzola,Efe Soyman,Christian Keysers,Augustine Triumph Attah

doi:10.1016/j.cub.2020.01.017

Abstract

Empathy, the ability to share another individual's emotional state and/or experience, has been suggested to be a source of prosocial motivation by attributing negative value to actions that harm others. The neural underpinnings and evolution of such harm aversion remain poorly understood. Here, we characterize an animal model of harm aversion in which a rat can choose between two levers providing equal amounts of food but one additionally delivering a footshock to a neighboring rat. We find that independently of sex and familiarity, rats reduce their usage of the preferred lever when it causes harm to a conspecific, displaying an individually varying degree of harm aversion. Prior experience with pain increases this effect. In additional experiments, we show that rats reduce the usage of the harm-inducing lever when it delivers twice, but not thrice, the number of pellets than the no-harm lever, setting boundaries on the magnitude of harm aversion. Finally, we show that pharmacological deactivation of the anterior cingulate cortex, a region we have shown to be essential for emotional contagion, reduces harm aversion while leaving behavioral flexibility unaffected. This model of harm aversion might help shed light onto the neural basis of psychiatric disorders characterized by reduced harm aversion, including psychopathy and conduct disorders with reduced empathy, and provides an assay for the development of pharmacological treatments of such disorders. VIDEO ABSTRACT.

Highlights

Learning to avoid actions that harm others is an important aspect of human development [1], and callousness to others’ harm is a hallmark of antisocial psychiatric disorders, including psychopathy and conduct disorder with reduced empathy [2]
We characterize an animal model of harm aversion in which a rat can choose between two levers providing equal amounts of food but one delivering a footshock to a neighboring rat
We find that independently of sex and familiarity, rats reduce their usage of the preferred lever when it causes harm to a conspecific, displaying an individually varying degree of harm aversion

Summary

Introduction

Learning to avoid actions that harm others is an important aspect of human development [1], and callousness to others’ harm is a hallmark of antisocial psychiatric disorders, including psychopathy and conduct disorder with reduced empathy [2]. An increasing number of studies show that rodents display affective reactions to the distress of conspecifics [7,8,9,10,11,12,13,14,15,16] These reactions are observed as increased freezing and modulation of pain sensitivity of the witness while attending to the other conspecific in pain [7,8,9,10,11, 13] or when the witness is re-exposed to cues associated with the other’s pain [17, 18]. Reducing activity in the ACC reduces emotional contagion [7, 20] In these paradigms, the observing rat is not the cause of the witnessed pain, and whether vicarious activity in area 24 is associated with harm aversion remains unclear

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