Towards a unified theory of emotional contagion in rodents-A meta-analysis.

Here we leverage 80 years of emotional contagion research in rodents and perform the first meta-analysis on this topic. Using 457 effect sizes, we show that, while both rats and mice are capable of emotional contagion, there are differences in how various factors modulate empathy in these species: 1) only mice show strain-specific differences in emotional contagion response; 2) although rats and mice have equivalent contagion response to familiar and unfamiliar individuals, our results show that familiarity length is negatively correlated with level of contagion in rats only; 3) prior experience with emotional stimuli almost doubles fear contagion response in rats while no changes are detected in pre-exposed mice; 4) both mice and rats tested alone show comparable reduced contagion compared to animals tested in a group; 5) emotional contagion is reduced in animals from both species missing one sensory modality compared to situations where all sensory modalities are recruited during emotional contagion. Lastly, we report similar patterns of brain activation during emotional contagion in rats and mice.

Harm to Others Acts as a Negative Reinforcer in Rats.

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.

Towards an animal model of callousness.

Callous-unemotional traits - the insensitivity to other's welfare and well-being - are characterized by a lack of empathy. They are characteristic of psychopathy and can be found in other anti-social disorders, such as conduct disorder. Because of the increasing prevalence of anti-social disorders and the rising societal costs of violence and aggression, it is of great importance to elucidate the psychological and physiological mechanisms underlying callousness in the search for pharmacological treatments. One promising avenue is to create a relevant animal model to explore the neural bases of callousness. Here, we review recent advances in rodent models of pro-social choice that could be applied to probe the absence of pro-sociality as a proxy of callous behavior, and provide future directions for the exploration of the neural substrates of callousness.

A Social Reinforcement Learning Hypothesis of Mutual Reward Preferences in Rats.

Although the use of neuroimaging techniques has revealed much about the neural correlates of social decision making (SDM) in humans, it remains poorly understood how social stimuli are represented, and how social decisions are implemented at the neural level in humans and in other species. To address this issue, the establishment of novel animal paradigms allowing a broad spectrum of neurobiological causal manipulations and neurophysiological recordings provides an exciting tool to investigate the neural implementation of social valuation in the brain. Here, we discuss the potential of a rodent model, Rattus norvegicus, for the understanding of SDM and its neural underpinnings. Particularly, we consider recent data collected in a rodent prosocial choice task within a social reinforcement framework and discuss factors that could drive SDM in rodents.

Basolateral amygdala lesions abolish mutual reward preferences in rats.

In a recent study, we demonstrated that rats prefer mutual rewards in a Prosocial Choice Task. Here, employing the same task, we show that the integrity of basolateral amygdala was necessary for the expression of mutual reward preferences. Actor rats received bilateral excitotoxic (n=12) or sham lesions (n=10) targeting the basolateral amygdala and were subsequently tested in a Prosocial Choice Task where they could decide between rewarding ("Both Reward") or not rewarding a partner rat ("Own Reward"), either choice yielding identical reward to the actors themselves. To manipulate the social context and control for secondary reinforcement sources, actor rats were paired with either a partner rat (partner condition) or with an inanimate rat toy (toy condition). Sham-operated animals revealed a significant preference for the Both-Reward-option in the partner condition, but not in the toy condition. Amygdala-lesioned animals exhibited significantly lower Both-Reward preferences than the sham group in the partner but not in the toy condition, suggesting that basolateral amygdala was required for the expression of mutual reward preferences. Critically, in a reward magnitude discrimination task in the same experimental setup, both sham-operated and amygdala-lesioned animals preferred large over small rewards, suggesting that amygdala lesion effects were restricted to decision making in social contexts, leaving self-oriented behavior unaffected.

Effort increases sensitivity to reward and loss magnitude in the human brain.

It is ecologically adaptive that the amount of effort invested to achieve a reward increases the relevance of the resulting outcome. Here, we investigated the effect of effort on activity in reward and loss processing brain areas by using functional magnetic resonance imaging. In total, 28 subjects were endowed with monetary rewards of randomly varying magnitude after performing arithmetic calculations that were either difficult (high effort), easy (low effort) or already solved (no effort). Subsequently, a forced donation took place, where a varying part of the endowment was transferred to a charity organization, causing a loss for the subject. Results show that reward magnitude positively modulates activity in reward-processing brain areas (subgenual anterior cingulate cortex and nucleus accumbens) only in the high effort condition. Furthermore, anterior insular activity was positively modulated by loss magnitude only after high effort. The results strongly suggest an increasing relevance of outcomes with increasing previous effort.

Rats prefer mutual rewards in a prosocial choice task.

Pro-sociality, i.e., the preference for outcomes that produce benefits for other individuals, is ubiquitous in humans. Recently, cross-species comparisons of social behavior have offered important new insights into the evolution of pro-sociality. Here, we present a rodent analog of the Pro-social Choice Task that controls strategic components, de-confounds other-regarding choice motives from the animals' natural tendencies to maximize own food access and directly tests the effect of social context on choice allocation. We trained pairs of rats-an actor and a partner rat-in a double T-maze task where actors decided between two alternatives only differing in the reward delivered to the partner. The "own reward" choice yielded a reward only accessible to the actor whereas the "both reward" choice produced an additional reward for a partner (partner condition) or an inanimate toy (toy Condition), located in an adjacent compartment. We found that actors chose "both reward" at levels above chance and more often in the partner than in the toy condition. Moreover, we show that this choice pattern adapts to the current social context and that the observed behavior is stable over time.