Low empathy-like behaviour in male mice associates with impaired sociability, emotional memory, physiological stress reactivity and variations in neurobiological regulations

Abstract

Deficits in empathy have been proposed to constitute a hallmark of several psychiatric disturbances like conduct disorder, antisocial and narcissistic personality disorders. Limited sensitivity to punishment, shallow or deficient affect and reduced physiological reactivity to environmental stressors have been often reported to co-occur with limited empathy and contribute to the onset of antisocial phenotypes. Empathy in its simplest form (i.e. emotional contagion) is addressed in preclinical models through the evaluation of the social transmission of emotional states: mice exposed to a painful stimulus display a higher response if in the presence of a familiar individual experiencing a higher degree of discomfort, than in isolation. In the present study, we investigated whether a reduction of emotional contagion can be considered a predictor of reduced sociality, sensitivity to punishment and physiological stress reactivity. To this aim, we first evaluated emotional contagion in a group of Balb/cJ mice and then discretised their values in four quartiles. The upper (i.e. Emotional Contagion Prone, ECP) and the lower (i.e. Emotional Contagion Resistant, ECR) quartiles constituted the experimental groups. Our results indicate that mice in the lower quartile are characterized by reduced sociability, impaired memory of negative events and dampened hypothalamic-pituitary-adrenocortical reactivity to external stressors. Furthermore, in the absence of changes in oxytocin receptor density, we show that these mice exhibit elevated concentrations of oxytocin and vasopressin and reduced density of BDNF receptors in behaviourally-relevant brain areas. Thus, not only do present results translate to the preclinical investigation of psychiatric disturbances, but also they can contribute to the study of emotional contagion in terms of its adaptive significance.

Understanding others: Emotion recognition in humans and other animals

“…Witnessing the pain of another was sufficient to increase the individual response to the same experience. Relevantly, modulation of pain sensitivity, later confirmed by other studies, was found to be regulated by the degree of relatedness between the interacting individuals …”

“…Despite the diversity in the modalities to express and/or perceive emotions, humans and other animals seem to share many homologies in their responses to other's emotions. Some of these responses, such as emotion contagion, can be similarly observed in all the species we described, from humans to mice . Similarly, the ability to perceive and use salient information from conspecifics emotional states is shared from primates to rodents .…”

“…Finally, genetic factors have been strongly implicated in social cognition deficits associated with several psychiatric conditions . Similarly, recent evidence indicates that genetic factors might modulate emotion‐processing behaviors in mice as well (eg, see). Thus, a better understanding of the contribution of genetic factors to emotion recognition abilities could also facilitate the identification of at‐risk subpopulations and the development of targeted medical approaches based on the genetic background of each individual.…”

Observational fear behavior in rodents as a model for empathy

“…It has been well known that different inbred mouse strains show different emotional responses to social stress, and such differences have been attributed to genetic differences of the strains . We previously surveyed multiple inbred mouse strains and found that the vicarious freezing response was highly variable among different strains.…”

“…It has been well known that different inbred mouse strains show different emotional responses to social stress, and such differences have been attributed to genetic differences of the strains. 67,68 We previously surveyed multiple inbred mouse strains and found that the vicarious freezing response was highly variable among different strains. Importantly, the variability in observational fear was not significantly associated with the strain-specific differences in other behaviors such as conditioned fear, locomotor activity, anxiety, or 3-chamber sociability, suggesting that observational fear-specific genetic variations exist in inbred strains of mice.…”