Experience Modulates Vicarious Freezing in Rats: A Model for Empathy

Abstract

The study of the neural basis of emotional empathy has received a surge of interest in recent years but mostly employing human neuroimaging. A simpler animal model would pave the way for systematic single cell recordings and invasive manipulations of the brain regions implicated in empathy. Recent evidence has been put forward for the existence of empathy in rodents. In this study, we describe a potential model of empathy in female rats, in which we studied interactions between two rats: a witness observes a demonstrator experiencing a series of footshocks. By comparing the reaction of witnesses with or without previous footshock experience, we examine the role of prior experience as a modulator of empathy. We show that witnesses having previously experienced footshocks, but not naïve ones, display vicarious freezing behavior upon witnessing a cage-mate experiencing footshocks. Strikingly, the demonstrator's behavior was in turn modulated by the behavior of the witness: demonstrators froze more following footshocks if their witness froze more. Previous experiments have shown that rats emit ultrasonic vocalizations (USVs) when receiving footshocks. Thus, the role of USV in triggering vicarious freezing in our paradigm is examined. We found that experienced witness-demonstrator pairs emitted more USVs than naïve witness-demonstrator pairs, but the number of USVs was correlated with freezing in demonstrators, not in witnesses. Furthermore, playing back the USVs, recorded from witness-demonstrator pairs during the empathy test, did not induce vicarious freezing behavior in experienced witnesses. Thus, our findings confirm that vicarious freezing can be triggered in rats, and moreover it can be modulated by prior experience. Additionally, our result suggests that vicarious freezing is not triggered by USVs per se and it influences back onto the behavior of the demonstrator that had elicited the vicarious freezing in witnesses, introducing a paradigm to study empathy as a social loop.

Rudimentary empathy in macaques’ social decision-making

“…Our finding of similar, and correlated behavioral responses to the direct experience of an aversive stimulus and to the observation of its impact upon a peer would appear consistent with simulation theories of empathy (7)(8)(9)21). Empathic-like responses have already been reported in others animal studies (2,5,7,(53)(54)(55)(56). Such behavioral responses are usually either contagious, modulated by past experience, and/or dependent on the partner identity.…”

“…social neuroscience | emotions | social gaze | eye blink | prosocial A nimal sociality encompasses a broad range of behaviors presumed to influence social bonds and promote group cohesion (1)(2)(3)(4)(5). Although higher forms of altruism, such as costly care of unknown individuals or donations to charity, may require uniquely human mentalizing abilities, evidence supports an evolutionary continuity in the motivational and affective mechanisms that regulate attachment and affiliation (6)(7)(8)(9).…”

“…In nonhuman primates, the ubiquitous social play, grooming behavior, and their hormonal correlates suggest an ability to conceive what is pleasant or unpleasant for others (10)(11)(12). Pioneering experimental studies have shown that macaques can perceive and seek to alleviate their peers' distress (13,14) and more recent studies have attributed even to rodents the possibility of empathy and its promotion of helping behavior (2)(3)(4). Empathy is understood to refer to vicarious experiences of the affective states of others and is believed to improve adaptive social behaviors.…”

Observational Fear Learning

“…This suggests that factors modulating the appraisal of another's distress may influence the strength of observational fear learning and expression. Accordingly, recent research in rats demonstrated that witnessing cage mates receive foot shocks led to higher levels of freezing behavior if observers had experienced foot shocks in the past (Atsak et al, 2010), suggesting that prior experience with an aversive event may enhance empathetic responses that facilitate vicarious fear learning. In another study, mice showed most robust social fear learning when they observed familiar conspecifics (e.g., littermates and mating partners), as compared with unrelated conspecifics (Jeon et al, 2010).…”

Reply: Spontaneous versus deliberate vicarious representations: different routes to empathy in psychopathy and autism

“…(Engen and Singer, 2013). Even rodents show signs of spontaneous vicarious emotions for the distress of others, but only when they have previous experience with the particular stressor and have shared a cage with the object of their empathy (Atsak et al, 2011). This suggests that spontaneous empathy does not have a single 'magnitude', but can be influenced by many different contextual factors and by previous experience in a way that might be subject-specific.…”