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• W3010132017 abstract "•Independently of sex and familiarity, rats avoid actions harming a conspecific•Prior experience with footshocks increases harm aversion•Rats show large individual variability in harm aversion•Anterior cingulate cortex deactivation abolishes harm aversion 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 AbstracteyJraWQiOiI4ZjUxYWNhY2IzYjhiNjNlNzFlYmIzYWFmYTU5NmZmYyIsImFsZyI6IlJTMjU2In0.eyJzdWIiOiI3OWEzMDhkNTIyNWY3NmZlNDE2ZDZlZTYxMTlhY2I1MyIsImtpZCI6IjhmNTFhY2FjYjNiOGI2M2U3MWViYjNhYWZhNTk2ZmZjIiwiZXhwIjoxNjQyNDUyNzMyfQ.LzoxU_UZdGfhlm5vj0L05sir6b64uvwu9d_UoymHzCbAhpf5Jq4DHnNo6QyKPTs7zPd42ylOpiVAArLcCqMNZi209ha2Znn1uFqDw1V-hEfXoFjKeDMqWUv65mzQVFjNtAJwDF1OR2PO0oyMrFSsYUsV9MzdfYgDwCFGkPdK2ZoSMDy_8HBEWKfmf1JTJTBmK-A85j0M7AfGMKjXPwYfDZ6W_ePPWBz-AWSS8JVVA5dYQnZXmgUpUWYrrrNNPiXPZw2CfBtm7btAXnHXWGIGkmHHnSzahc1KiqhBzGYJbLnvgOKrl1aNz2wYSuWP7Yvpp6aHIGgv69PhxXOVxYfYqA(mp4, (23.38 MB) Download video 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. Learning to avoid actions that harm others is an important aspect of human development [1Wilson D.S. Altruism in everyday life.Does Altruism Exist?: Culture, Genes, and the Welfare of Others. Yale University Press, 2015: 117-129Google Scholar], and callousness to others’ harm is a hallmark of antisocial psychiatric disorders, including psychopathy and conduct disorder with reduced empathy [2Blair R.J.R. The neurobiology of psychopathic traits in youths.Nat. Rev. Neurosci. 2013; 14: 786-799Crossref PubMed Scopus (331) Google Scholar]. What could motivate humans and other animals to refrain from harming others? An influential theory posits that vicarious emotions (i.e., emotions felt by a witness, in the stead of the witnessed individual), including emotional contagion and empathy, trigger harm aversion [3Smith A. Theory of Moral Sentiments. Cambridge, 1759Crossref Google Scholar]. Put simply, harming other people is unpleasant, because we vicariously share the pain we inflict. Accordingly, it has been argued that psychiatric disorders characterized by antisocial behavior [2Blair R.J.R. The neurobiology of psychopathic traits in youths.Nat. Rev. Neurosci. 2013; 14: 786-799Crossref PubMed Scopus (331) Google Scholar, 4Blair R.J.R. Budhani S. Colledge E. Scott S. Deafness to fear in boys with psychopathic tendencies.J. Child Psychol. Psychiatry. 2005; 46: 327-336Crossref PubMed Scopus (132) Google Scholar] might stem from malfunctioning or biased vicarious emotions [5Meffert H. Gazzola V. den Boer J.A. Bartels A.A.J. Keysers C. Reduced spontaneous but relatively normal deliberate vicarious representations in psychopathy.Brain. 2013; 136: 2550-2562Crossref PubMed Scopus (167) Google Scholar, 6Keysers C. Gazzola V. Dissociating the ability and propensity for empathy.Trends Cogn. Sci. 2014; 18: 163-166Abstract Full Text Full Text PDF PubMed Scopus (82) Google Scholar]. An increasing number of studies show that rodents display affective reactions to the distress of conspecifics [7Jeon D. Kim S. Chetana M. Jo D. Ruley H.E. Lin S.-Y.Y. Rabah D. Kinet J.-P.P. Shin H.-S.S. Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC.Nat. Neurosci. 2010; 13: 482-488Crossref PubMed Scopus (370) Google Scholar, 8Kim E.J. Kim E.S. Covey E. Kim J.J. Social transmission of fear in rats: the role of 22-kHz ultrasonic distress vocalization.PLoS ONE. 2010; 5: e15077Crossref PubMed Scopus (137) Google Scholar, 9Atsak P. Orre M. Bakker P. Cerliani L. Roozendaal B. Gazzola V. Moita M. Keysers C. Experience modulates vicarious freezing in rats: a model for empathy.PLoS ONE. 2011; 6: e21855Crossref PubMed Scopus (116) Google Scholar, 10Li Z. Lu Y.F. Li C.L. Wang Y. Sun W. He T. Chen X.F. Wang X.L. Chen J. Social interaction with a cagemate in pain facilitates subsequent spinal nociception via activation of the medial prefrontal cortex in rats.Pain. 2014; 155: 1253-1261Abstract Full Text Full Text PDF PubMed Scopus (50) Google Scholar, 11Meyza K.Z. Bartal I.B. Monfils M.H. Panksepp J.B. Knapska E. The roots of empathy: through the lens of rodent models.Neurosci. Biobehav. Rev. 2017; 76: 216-234Crossref PubMed Scopus (74) Google Scholar, 12Burkett J.P. Andari E. Johnson Z.V. Curry D.C. de Waal F.B. Young L.J. Oxytocin-dependent consolation behavior in rodents.Science. 2016; 351: 375-378Crossref PubMed Scopus (275) Google Scholar, 13de Waal F.B.M. Preston S.D. Mammalian empathy: behavioural manifestations and neural basis.Nat. Rev. Neurosci. 2017; 18: 498-509Crossref PubMed Scopus (273) Google Scholar, 14Ferretti V. Maltese F. Contarini G. Nigro M. Bonavia A. Huang H. Gigliucci V. Morelli G. Scheggia D. Managò F. et al.Oxytocin signaling in the central amygdala modulates emotion discrimination in mice.Curr. Biol. 2019; 29: 1938-1953.e6Abstract Full Text Full Text PDF PubMed Scopus (47) Google Scholar, 15Scheggia D. Managò F. Maltese F. Bruni S. Nigro M. Dautan D. Latuske P. Contarini G. Gomez-Gonzalo M. Requie L.M. et al.Somatostatin interneurons in the prefrontal cortex control affective state discrimination in mice.Nat. Neurosci. 2020; 23: 47-60Crossref PubMed Scopus (37) Google Scholar, 16Han Y. Bruls R. Soyman E. Thomas R.M. Pentaraki V. Jelinek N. Heinemans M. Bassez I. Verschooren S. Pruis I. et al.Bidirectional cingulate-dependent danger information transfer across rats.PLoS Biol. 2019; (Published online December 5, 2019)https://doi.org/10.1371/journal.pbio.3000524Crossref Scopus (7) Google Scholar]. These reactions are observed as increased freezing and modulation of pain sensitivity of the witness while attending to the other conspecific in pain [7Jeon D. Kim S. Chetana M. Jo D. Ruley H.E. Lin S.-Y.Y. Rabah D. Kinet J.-P.P. Shin H.-S.S. Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC.Nat. Neurosci. 2010; 13: 482-488Crossref PubMed Scopus (370) Google Scholar, 8Kim E.J. Kim E.S. Covey E. Kim J.J. Social transmission of fear in rats: the role of 22-kHz ultrasonic distress vocalization.PLoS ONE. 2010; 5: e15077Crossref PubMed Scopus (137) Google Scholar, 9Atsak P. Orre M. Bakker P. Cerliani L. Roozendaal B. Gazzola V. Moita M. Keysers C. Experience modulates vicarious freezing in rats: a model for empathy.PLoS ONE. 2011; 6: e21855Crossref PubMed Scopus (116) Google Scholar, 10Li Z. Lu Y.F. Li C.L. Wang Y. Sun W. He T. Chen X.F. Wang X.L. Chen J. Social interaction with a cagemate in pain facilitates subsequent spinal nociception via activation of the medial prefrontal cortex in rats.Pain. 2014; 155: 1253-1261Abstract Full Text Full Text PDF PubMed Scopus (50) Google Scholar, 11Meyza K.Z. Bartal I.B. Monfils M.H. Panksepp J.B. Knapska E. The roots of empathy: through the lens of rodent models.Neurosci. Biobehav. Rev. 2017; 76: 216-234Crossref PubMed Scopus (74) Google Scholar, 13de Waal F.B.M. Preston S.D. Mammalian empathy: behavioural manifestations and neural basis.Nat. Rev. Neurosci. 2017; 18: 498-509Crossref PubMed Scopus (273) Google Scholar] or when the witness is re-exposed to cues associated with the other’s pain [17Bruchey A.K. Jones C.E. Monfils M.-H. Fear conditioning by-proxy: social transmission of fear during memory retrieval.Behav. Brain Res. 2010; 214: 80-84Crossref PubMed Scopus (74) Google Scholar, 18Jones C.E. Riha P.D. Gore A.C. Monfils M.-H. Social transmission of Pavlovian fear: fear-conditioning by-proxy in related female rats.Anim. Cogn. 2014; 17: 827-834Crossref PubMed Scopus (51) Google Scholar]. Recent studies in rats identified emotional mirror neurons in the anterior cingulate cortex (ACC; area 24 in particular) [19Sakaguchi T. Iwasaki S. Okada M. Okamoto K. Ikegaya Y. Ethanol facilitates socially evoked memory recall in mice by recruiting pain-sensitive anterior cingulate cortical neurons.Nat. Commun. 2018; 9: 3526Crossref PubMed Scopus (26) Google Scholar, 20Carrillo M. Han Y. Migliorati F. Liu M. Gazzola V. Keysers C. Emotional mirror neurons in the rat’s anterior cingulate cortex.Curr. Biol. 2019; 29: 1301-1312.e6Abstract Full Text Full Text PDF PubMed Scopus (63) Google Scholar], which respond to the observer experiencing pain and to witnessing a conspecific’s distress. Reducing activity in the ACC reduces emotional contagion [7Jeon D. Kim S. Chetana M. Jo D. Ruley H.E. Lin S.-Y.Y. Rabah D. Kinet J.-P.P. Shin H.-S.S. Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC.Nat. Neurosci. 2010; 13: 482-488Crossref PubMed Scopus (370) Google Scholar, 20Carrillo M. Han Y. Migliorati F. Liu M. Gazzola V. Keysers C. Emotional mirror neurons in the rat’s anterior cingulate cortex.Curr. Biol. 2019; 29: 1301-1312.e6Abstract Full Text Full Text PDF PubMed Scopus (63) Google Scholar]. However, 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 thus remains unclear. Inspired by classic studies, here, we refine a paradigm to study instrumental harm aversion in rats. A rat called the “actor” can press one of two levers for sucrose pellets. After a baseline phase revealing the rat’s preference for one of the levers, we pair this preferred lever with a shock to a second rat (“victim”), located in an adjacent compartment (Figure 1). We then measure how much actors switch away from the preferred lever as a behavioral index of harm aversion. We show that (1) male and female Sprague-Dawley rats switch significantly away from the shock-delivering lever, (2) this effect is stronger in shock-pre-exposed actors, and (3) deactivating the ACC reduces this effect. By altering the timing of shock delivery, we show that contingency between lever pressing and shock delivery is essential. By varying the reward value of the levers, we show rats switch from an easier to a harder lever and from one that provides two pellets to one that provides one pellet to prevent harm to another. However, rats were unwilling to switch from a lever that provides three pellets to one that provides one pellet. We additionally report and explore substantial individual differences in switching across rats. We first compare the behavior of rats in three main conditions: ContingentHarm; NoHarm; and RandomHarm (Table 1). In all three conditions, an actor was trained to press one of two levers for one sucrose pellet in the actor compartment (Figures 1A–1F). One lever required ∼60 cN (∼60 g) of force to be pressed, although the other required ∼30 cN (∼30 g), with the harder-to-press side randomized across animals. After initial training alone, all actors were exposed to 4 footshocks (exposure; Figures 1E and 1F) in the adjacent victim’s compartment to maximize emotional contagion [9Atsak P. Orre M. Bakker P. Cerliani L. Roozendaal B. Gazzola V. Moita M. Keysers C. Experience modulates vicarious freezing in rats: a model for empathy.PLoS ONE. 2011; 6: e21855Crossref PubMed Scopus (116) Google Scholar, 19Sakaguchi T. Iwasaki S. Okada M. Okamoto K. Ikegaya Y. Ethanol facilitates socially evoked memory recall in mice by recruiting pain-sensitive anterior cingulate cortical neurons.Nat. Commun. 2018; 9: 3526Crossref PubMed Scopus (26) Google Scholar, 21Allsop S.A. Wichmann R. Mills F. Burgos-Robles A. Chang C.J. Felix-Ortiz A.C. Vienne A. Beyeler A. Izadmehr E.M. Glober G. et al.Corticoamygdala transfer of socially derived information gates observational learning.Cell. 2018; 173: 1329-1342.e18Abstract Full Text Full Text PDF PubMed Scopus (100) Google Scholar]. Actors were then placed back into their actor compartment and performed 24 trials of lever pressing with their cage mate in the victim compartment (baseline).Table 1Core Experimental ConditionsContingentHarmNoHarmRandomHarmn = 24 (12♂, 12♀)Nn= 14, all ♂n = 8, all ♂Shock to ActorShock to VictimShock to ActorShock to VictimShock to ActorShock to VictimExposureyes/yes/yes/BaselinenonononononoShocknoyesnononoyesFoodnonononononoFor each experimental condition (columns), the table specifies who got electrical shocks during the exposure, baseline, and shock sessions (yes) and who did not (no). A “/” indicates that the victim was not present during the exposure session. Sample size (n) reflects the number of actors included in the behavioral analyses. ♂, male; ♀, female. Open table in a new tab For each experimental condition (columns), the table specifies who got electrical shocks during the exposure, baseline, and shock sessions (yes) and who did not (no). A “/” indicates that the victim was not present during the exposure session. Sample size (n) reflects the number of actors included in the behavioral analyses. ♂, male; ♀, female. These 24 trials started with 4 forced trials (2 for each lever; pseudo-randomized) to force actors to sample both options, followed by 20 free choice trials to measure baseline lever preference (Figure 1E). In the ContingentHarm condition, on the 3 days following baseline (Shock1, Shock2, and Shock3 sessions; Figure 1E), the actor performed 24 trials of the same task each day (4 forced + 20 free choice), similar to baseline trials, except that pressing the lever preferred during baseline triggered a footshock (0.8 mA; 1 s) to the victim in the adjacent compartment. In this condition, we had two groups: male (ContingentHarm ♂) and female pairs (ContingentHarm ♀). We compared this condition against a NoHarm control condition, in which pressing either lever never delivered a shock to the victim to control for spontaneous changes in preference. Finally, we created a RandomHarm control condition, in which the victim is exposed to the same shocks that triggered strong switching in the ContingentHarm condition but were administered independently of the choices of the actor. For this RandomHarm condition, we identified the 8 actors from the ContingentHarm condition (from all 24 animals) that showed the strongest switching away from the shock lever. For each, we recorded the sequence of shock and no-shock trials to the victim. In the RandomHarm condition, each victim then received the sequence of shocks from one of the switchers from the ContingentHarm condition, independently of what lever was pressed by the actor. Crucially, to break the action-outcome contingency, shocks were delayed randomly by 3–8 s after actors exited the food receptacle, i.e., before the start of the following trial. At the group level, we compared preference changes from baseline to shock sessions across conditions. A 4-group(ContingentHarm♂, ContingentHarm♀, NoHarm♂, RandomHarm♂) × 4-session(baseline, Shock1, Shock2, Shock3) repeated-measures ANOVA revealed a significant effect of session (F(3,123) = 7.34; p < 0.001; η2 = 0.15; BFincl = 433) and session × group interaction (F(9,123) = 1.93; p = 0.05; η2 = 0.12; BFincl = 3). We first concentrate on male actors, for which we have three groups (ContingentHarm♂, NoHarm♂, and RandomHarms♂), which showed similar preferences at baseline (i.e., comparable preference for the future shock lever; ANOVA; F(2,31) = 1.29; p = 0.289; BFincl = 0.46). From baseline to all shock sessions, ContingentHarm male actors showed the expected decrease in shock lever pressing, with their preference for the shock lever lower than the NoHarm and RandomHarm control groups in all shock sessions (even if regressing out differences in baseline preference; Figure 2A). Actors in the male ContingentHarm group thus shifted significantly away from a lever that causes shocks to a conspecific, and this was not simply due to the distress of the victim (which was matched, i.e., no significant differences in the amount of freezing and ultrasonic vocalizations (USVs), across ContingentHarm and RandomHarm groups; Figure S1) but to the contingency between the actions of the actor and the reactions of the victim. Male and females did not differ in their change in preference across sessions (Figure 2B; session × gender: F(3,63) = 0.21; p = 0.89; η2 = 0.01; BFincl = 0.20), with both showing a significant main effect of session when analyzed individually (female: F(3,30) = 5.9, p < 0.003, BFincl = 14.5; Male: F(3,33) = 7.8, p < 0.001, BFincl = 64). For all subsequent analyses looking at the change of preference across sessions, we thus pool males and females into one single ContingentHarm condition (n = 24 actors). The Bayes factor for including a main effect of gender, however, was anecdotal (BFincl = 0.44). To prevent harm to their victim, actors could stop pressing any lever instead of switching to the no-shock lever. Across our three groups, all animals performed all their baseline trials. In the ContingentHarm shock sessions, six animals failed to press any lever within the 400 s allowed (missing 1, 1, 2, 10, 20, and 32 out of the 60 free choice trials over the 3 shock sessions, respectively). In contrast, all animals in the NoHarm condition performed all their 60 free choices over all sessions, and only one in the RandomHarm condition missed one trial. This illustrates witnessing contingent shocks to another rat can motivate agents to stop pressing levers altogether. However, given that, over all ContingentHarm animals, 95% of free trials were performed, we concentrate on the shift away from the shock lever as our dependent measure. To quantify switching at the individual level, we computed a switching index (SI),SI=Sbaseline−SshockSbaseline+Sshock, where Sbaseline is the proportion of shock lever presses during baseline and Sshock the average proportion of shock lever presses over all shock sessions (see STAR Methods). Positive SIs reflect switching away from the shock lever and SI = 1 maximum possible switch given an individual’s baseline preference (Figure 3D). In the ContingentHarm condition, some animals showed substantial preference changes in shock sessions, and others remained indifferent. A permutation test revealed n = 9 actors (i.e., 38%) in the ContingentHarm condition (n = 4 males and n = 5 females) showed a significant switch (at p < 0.05; green solid circles in Figure 3A; hereafter referred to as “switchers”). A binomial test showed that 9 out of 24 switchers are not explained by chance (binomial; n = 24; alpha = 0.05; p = 10−6). These switchers found across males and females showed a decrease between 25% and 80% from baseline. Switching rates were within chance level in the NoHarm (n = 1 significant switcher; blue colored in circle; binomial; p = 0.36) and absent in the RandomHarm condition (n = 0 significant switchers). A χ2 square test revealed the ContingentHarm condition had more switchers than the NoHarm condition (χ2 = 4.20; p = 0.04) and the RandomHarm condition (χ2 = 4.17; p = 0.04). Figure 3B shows the lever choices session per session for each ContingentHarm actor and the distribution of changes across sessions. For switchers, most changes in lever choice occurred in the first shock session, with little change occurring in the subsequent sessions. To explore what may determine these differences in switching in the ContingentHarm condition, we extracted a number of variables from the behavior of the actors and victims and examined which could predict the SI (Table 2; Figure S2). To limit multiple comparisons, we focused on a limited number of variables that are meant to assess distress, attention, the ability to press the levers, and behavioral flexibility. Behavioral flexibility was assessed in two ways: (1) how much the preference for the lever that will later be paired with shocks changed from step 3c of the training session to baseline (Figure 1E) and (2) how much actors switched lever preferences after the shock session for food reward. The latter was measured after the end of the third shock session by turning off shock delivery, identifying which lever was less preferred, and baiting that lever with 3 pellets, in contrast to one pellet delivered by pressing the preferred lever (food session; Figures 1E and 1F; Table 1). We computed individual food indices (FIs) (Figures 3C and 3D), which quantified the change of lever choice from the last shock session across the three successive food sessions. ContingentHarm animals did not show significant differences in FI from the NoHarm and RandomHarm animals (Figure 3C), and switchers and non-switcher animals showed comparable FI in the ContingentHarm condition (Figure 3C), suggesting that non-switchers switch as much as switchers for rewards, but not for shocks to others.Table 2Behavioral Correlates of SwitchingtauLower 95% CIUpper 95% CIBF10p2Difference in log time spent in the food hopper (Shock–NoShock in session Shock1)−0.55−0.75−0.1846.46aSignificant either based on BF (using 3 and 1/3 as critical values) or based on p < 0.05 threshold0.001aSignificant either based on BF (using 3 and 1/3 as critical values) or based on p < 0.05 thresholdDifference in log latency to enter food hopper (Shock–NoShock in Shock1)0.460.120.6614.32aSignificant either based on BF (using 3 and 1/3 as critical values) or based on p < 0.05 threshold0.004aSignificant either based on BF (using 3 and 1/3 as critical values) or based on p < 0.05 thresholdIncrease victim time spent close to divider (Shock–NoShock in Shock1)−0.40−0.61−0.109.28aSignificant either based on BF (using 3 and 1/3 as critical values) or based on p < 0.05 threshold0.006aSignificant either based on BF (using 3 and 1/3 as critical values) or based on p < 0.05 thresholdIncrease in average trial duration (Shock1–baseline)0.390.080.607.57aSignificant either based on BF (using 3 and 1/3 as critical values) or based on p < 0.05 threshold0.008aSignificant either based on BF (using 3 and 1/3 as critical values) or based on p < 0.05 thresholdChange in lever preference for food (food index)−0.30−0.530.001.860.045aSignificant either based on BF (using 3 and 1/3 as critical values) or based on p < 0.05 thresholdSpontaneous changes in shock lever preference (last training–baseline)−0.26−0.490.031.110.082Difference in weight (actor–victim)−0.23−0.460.060.850.118Increase in actor freezing (Shock1–baseline)0.16−0.120.400.460.295Increase in victim freezing (Shock1–baseline)0.14−0.140.390.410.333Weight actor−0.11−0.360.160.340.456Weight victim0.05−0.220.300.28aSignificant either based on BF (using 3 and 1/3 as critical values) or based on p < 0.05 threshold0.747Increase actor time spent close to divider (shock–NoShock in Shock1)0.05−0.220.300.28aSignificant either based on BF (using 3 and 1/3 as critical values) or based on p < 0.05 threshold0.747Squeak loudness (power shock–NoShock in Shock1)−0.05−0.300.220.28aSignificant either based on BF (using 3 and 1/3 as critical values) or based on p < 0.05 threshold0.747Increase in 22 kHz USV (Shock1–baseline)0.00−0.260.260.26aSignificant either based on BF (using 3 and 1/3 as critical values) or based on p < 0.05 threshold0.980Variables ranked based on decreasing evidence of correlation (BF10) using the rank order correlation Kendall Tau. The horizontal lines separate variables based on whether there is (1) evidence for the presence of an association (top cases, BF10 > 3), (2) inconclusive evidence (middle, 0.33 < BF10 < 3), or (3) evidence for the absence of an association (BF10 < 0.33, bottom). See also Figure S2. BF10, Bayes factor in favor of the presence of a correlation; CI, confidence interval; P2, two tailed frequentist probability for Tau = 0; Tau, Kendall’s tau.a Significant either based on BF (using 3 and 1/3 as critical values) or based on p < 0.05 threshold Open table in a new tab Variables ranked based on decreasing evidence of correlation (BF10) using the rank order correlation Kendall Tau. The horizontal lines separate variables based on whether there is (1) evidence for the presence of an association (top cases, BF10 > 3), (2) inconclusive evidence (middle, 0.33 < BF10 < 3), or (3) evidence for the absence of an association (BF10 < 0.33, bottom). See also Figure S2. BF10, Bayes factor in favor of the presence of a correlation; CI, confidence interval; P2, two tailed frequentist probability for Tau = 0; Tau, Kendall’s tau. To relate all these measures to SI (which is not normally distributed over the entire group), we used Kendall’s Tau rank order correlation as the measure of association. Table 2 and Figure S2 show these variables ranked by the evidence (Bayes factor) for an association. Focusing on associations with a BF10 > 3 (dark red lines in Figure S2) shows that animals that switched more spent less time in the food hopper and took longer to enter the food hopper after trials in which the victim received a shock, leading to longer overall trial duration. Figure 3E illustrates that this effect is visible specifically in the Shock1 session, where switchers, but not non-switchers, delay their entry and accelerate their exit from the food hopper specifically on trials in which they delivered a shock to the other animal. This was confirmed by an ANOVA that revealed a session(baseline, Shock1, Shock2, Sochk3) × trial(shock lever, no-shock lever) × type(switchers, non-switchers) interaction (significantly for log latency F(3,36) = 5.9, p = 0.002, BFincl = 73 and a trend for log duration F(3,33) = 2.37, p = 0.08, BFincl = 2.7). A similar effect was not apparent in the NoHarm or RandomHarm conditions (Figure S3). As a result, switcher rats also took longer to perform trials (Figure 3E). This suggests witnessing the victim receive shocks interfered with the food-directed action of switchers, but not non-switchers. We also observed that dyads with more switching had victims that spent less time close to the divider. In contrast, variables that might have captured differences in distress signals (freezing, 22-kHz USV emissions, and loudness of pain squeaks) failed to reveal robust associations with switching (Table 2). The same was true for weight and our measures of behavioral flexibility, as measured by changes in lever choice across training and baseline or in response to food rewards. Prior experience with footshocks increases the sensitivity of rodents to witnessing footshocks in others [9Atsak P. Orre M. Bakker P. Cerliani L. Roozendaal B. Gazzola V. Moita M. Keysers C. Experience modulates vicarious freezing in rats: a model for empathy.PLoS ONE. 2011; 6: e21855Crossref PubMed Scopus (116) Google Scholar, 16Han Y. Bruls R. Soyman E. Thomas R.M. Pentaraki V. Jelinek N. Heinemans M. Bassez I. Verschooren S. Pruis I. et al.Bidirectional cingulate-dependent danger information transfer across rats.PLoS Biol. 2019; (Published online December 5, 2019)https://doi.org/10.1371/journal.pbio.3000524Crossref Scopus (7) Google Scholar, 19Sakaguchi T. Iwasaki S. Okada M. Okamoto K. Ikegaya Y. Ethanol facilitates socially evoked memory recall in mice by recruiting pain-sensitive anterior cingulate cortical neurons.Nat. Commun. 2018; 9: 3526Crossref PubMed Scopus (26) Google Scholar, 21Allsop S.A. Wichmann R. Mills F. Burgos-Robles A. Chang C.J. Felix-Ortiz A.C. Vienne A. Beyeler A. Izadmehr E.M. Glober G. et al.Corticoamygdala transfe" @default.
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