Abstract
Pain can be socially transferred between familiar rats due to empathic responses. To validate rat model of empathy for pain, effects of pain expressions in a cagemate demonstrator (CD) in pain on empathic pain responses in a naïve cagemate observer (CO) after 30 min priming dyadic social interactions (PDSI) were evaluated. The CD rats were prepared with four pain models: bee venom (BV), formalin, complete Freund's adjuvant (CFA), and spared nerve injury (SNI). Both BV and formalin tests are characterized by displayable and eye-identifiable spontaneous pain-related behaviors (SPRB) immediately after treatment, while CFA and SNI models are characterized by delayed occurrence of evoked pain hypersensitivity but with less eye-identifiable SPRB. After 30 min PDSI with a CD immediately after BV and formalin, respectively, the empathic mechanical pain hypersensitivity (EMPH) could be identified at both hind paws in CO rats. The BV—or formalin-induced EMPH in CO rats lasted for 4–5 h until full recovery. However, EMPH failed to develop in CO after socially interacting with a CD immediately after CFA, or 2 h after BV when SPRB completely disappeared. The CO's EMPH was partially relieved when socially interacting with an analgecized CD whose SPRB had been significantly suppressed. Moreover, repeated exposures to a CD in pain could enhance EMPH in CO. Finally, social transfer of pain hypersensitivity was also identified in CO who was being co-housed in pairs with a conspecific treated with CFA or SNI. The results suggest that development of EMPH in CO rats would be determined not only by extent of familiarity but also by visually identifiable pain expressions in the social partners during short period of PDSI. However, the visually unidentifiable pain can also be transferred to naïve cagemate when being co-housed in pairs with a distressed conspecific. In summary, the vicariously social contagion of pain between familiar rats is dependent upon not only expressions of pain in social partners but also the time that dyads spent in social communications. The rat model of empathy for pain is a highly stable, reproducible and valid model for studying the neural mechanisms of empathy in lower animals.
Highlights
The time that cagemate observer (CO) rats spent on allo-grooming and allo-licking toward the dyadic cagemate demonstrator (CD) during 30 min social interaction was significantly longer than Cagemate control (CC) rats [Figure 2E, CO [bee venom (BV)] vs. CC, F(2, 15) = 16.40, P < 0.0001, n = 6 for each group, One way analysis of variance (ANOVA) with Turkey’s correction]
Similar to our previous results (Li et al, 2014; Lü et al, 2017), the empathic mechanical pain hypersensitivity (EMPH) displaying as distinct reductions in the paw withdrawal mechanical threshold (PWMT) were identified on the bilateral hind paws in CO rats after 30 min dyadic social interactions with the BV- and formalintreated CD rats (Figures 3D,E, vs. PWMTbaseline, ∗/#P < 0.05, ∗∗/##P < 0.01, ∗∗∗/###P < 0.001, n = 8 for both CO [BV] and CO [Formalin], one way repeat measures ANOVA with Greenhouse-Geisser Correction)
The results showed that 80% of the CO rats (8/10) developed the EMPH (40% minimal reduction in the PWMT as standard) after socially interacting with the BV- and formalin-treated CD rats, only 40% (4/10) or 20% (2/10) of the CO rats showed distinct reduction in the PWMT after priming social interactions with the CD rats treated with complete Freund’s adjuvant (CFA) or 2 h after BV.[2 sided P = 0.17, CO [BV/Formalin] vs. CO [CFA]; 2 sided P = 0.024, CO [BV] vs. CO [Post-BV 2 h], Fisher’s two-tailed test]
Summary
Pain can be socially transferred between familiar conspecifics in rodents due to empathic responses (Martin et al, 2014; Mogil, 2015; Chen, 2018). From the point of evolutionary view, empathy can be defined as an evolutionary behavior of social animals and humans associated with prosocial reciprocity, altruism, and morality by the ability and capacity to feel, recognize, understand, and share the emotional states of others (Preston and de Waal, 2002; de Waal, 2008; Bernhardt and Singer, 2012; Decety et al, 2016; de Waal and Preston, 2017; Chen, 2018) In humans, both directly felt pain and empathy for pain has been demonstrated to be processed by a common core neural network mainly involving the anterior cingulate cortex (ACC) and anterior insular cortex (Rainville et al, 1997; Singer et al, 2004; Lamm et al, 2011). Besides the roles of familiarity in production of empathy for pain, the roles of other factors such as the extent of pain expressions in the social demonstrators require to be further examined
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