Humans help family members and friends under circumstances where they may not help strangers. However, they also help complete strangers through both direct actions, such as helping someone who has stumbled, and indirect actions, such as giving to charity. Ben-Ami Bartal et al. have now explored the biological basis of such socially selective helping by testing whether rats help strangers, and if so, under what circumstances.

In the experiments a free rat was exposed to another rat trapped inside a plastic tube with an outward-facing door for 12 one-hour sessions. When tested with a cagemate trapped inside the tube, most free rats learned within a few days to release the trapped rat by opening the door. Ben-Ami Bartal et al. then exposed the free rats to strangers they had never met or seen before. Remarkably the rats consistently released the trapped stranger, acting toward strangers just as they had acted toward familiar cagemates. This result suggested that individual familiarity is not required for helping to occur.

To test the limits of rat benevolence, Ben-Ami Bartal et al. tested free rats (always white albino rats) with trapped rats from a different outbred strain (black-hooded rats). The rats helped cagemates of a different strain but not strangers of a different strain. These results could be explained by a requirement for strain familiarity or individual familiarity. To distinguish between these possibilities, albino rats were housed for 2 weeks with a rat of a different strain, and then re-housed with another albino rat before being tested with a trapped rat belonging to a different strain. Consistent with a requirement for strain but not individual familiarity, the free rats now helped stranger rats from the different, but now familiar, strain.

To explore if there is any role for genetics or relatedness in socially selective helping, Ben-Ami Bartal et al. tested whether rats will help strangers of their own strain based on genetic relatedness alone. To do this albino pups were transferred to litters of a different strain on the day they were born, and never saw or interacted with another albino rat until testing. Remarkably, the albino rats helped strangers from the different strain that they were raised with, but they did not help strangers of their own strain because this strain was unfamiliar to them. The fact that the motivation to help other rats has its origins in social interactions rather than genetics provides the flexibility that is needed to navigate their way through social environments that often change unexpectedly.

Pro-social behavior comprises actions that improve the well-being of others (Eisenberg et al., 1989) and is found widely in the animal world (Owens and Owens, 1984; Wilkinson, 1984; Lee, 1987; Heinrich and Marzluff, 1995; Warneken and Tomasello, 2006; Nowbahari et al., 2009; Yamamoto et al., 2012; Baden et al., 2013; Clay and de Waal, 2013; Hatchwell et al., 2013). Pro-sociality within a group promotes individual survival and reproduction (Hamilton, 1984; Preston and de Waal, 2002; Decety and Svetlova, 2012). On the other hand, acting pro-socially towards individuals from other groups may not be adaptive, as other groups often compete for valuable and limited resources. Thus animals can be motivated to act pro-socially or aggressively depending on the social context.

In humans, pro-social behavior is modulated by the degree of affiliation and is extended preferentially towards in-group members and less often toward unaffiliated others (Hornstein, 1978; Cialdini et al., 1997; Preston and de Waal, 2002; Levine et al., 2005; Sturmer et al., 2006; Lamm et al., 2010; Echols and Correll, 2012). Yet humans can and often do act pro-socially towards strangers (Batson et al., 2005). This human capacity to help unfamiliar individuals is often viewed as a cognitively complex behavior that depends on high cognitive capacities and cultural transmission (Levine et al., 2001).

Rodents have emerged as a valuable model system for social behavior and communication (Decety and Svetlova, 2012; Mogil, 2012; Panksepp and Panksepp, 2013; Preston, 2013). Rodents manifest emotional contagion (Langford et al., 2006; Chen et al., 2009; Jeon et al., 2010; Knapska et al., 2010; Panksepp and Lahvis, 2011; Akyazi and Eraslan, 2014; Atsak et al., 2011), cooperation (Rutte and Taborsky, 2007; Viana et al., 2010; Tsoory et al., 2012), and helping (Ben-Ami Bartal et al., 2011; Church, 1959; Rice and Gainer, 1962). We previously found that Sprague-Dawley (SD) rats learn to release SD cagemates trapped in a restrainer (Ben-Ami Bartal et al., 2011). Here, we set out to investigate how previous social experience acquired during development and adulthood influences helping behavior. First, we tested whether rats will help unfamiliar individuals, strangers. Rats showed helping behavior equally towards cagemates and strangers, if the strangers were of their own strain. However, rats did not help strangers of an unfamiliar strain, suggesting that helping in rats may be innately biased towards the helper’s own strain. Yet, further experiments demonstrated that a short period of pair-housing with a rat of the unfamiliar strain was sufficient to motivate helping for that individual. Moreover, rats that had previously lived with a rat of a different strain were as motivated to help strangers of that strain as they were to help strangers of their own strain. This finding demonstrates that rats choose to help others depending on the social context, and extend pro-social motivation beyond individual identity, to groups defined by strain. Finally, we sought to determine if genetic relatedness is at all capable of influencing pro-social motivation towards an unfamiliar rat. We found that rats that were fostered from birth with another strain did not help strangers of their own strain as adults. Fostered rats only acted pro-socially towards rats of the foster strain, demonstrating that genetic relatedness alone is not capable of producing pro-social motivation.

In each hour-long session, a free rat of the SD strain was placed in an arena containing another rat trapped inside a centrally located restrainer. (A rodent stock, colloquially referred to as an outbred strain, is a colony of conspecifics derived from a small group of founder animals. Individuals are not genetically identical. Here we refer to stocks as strains.) The door to the restrainer could only be opened from the outside and thus only by the free rat. Door-opening by the free rat led to the trapped rat’s release from the restrainer. If a free rat failed to open the door within 40 min, the experimenter opened it halfway, allowing the trapped rat to exit the restrainer. Only door-openings resulting from the free rat’s action, during the first 40 min of each session, were counted as such. Regardless of which rat opened the restrainer door and whether that occurred before or after halfway opening, both rats remained in the arena for the entire hour of every session. All rats were males and all free rats were from the SD strain. Sessions were repeated for 12 days.

To determine whether rats help unfamiliar individuals, free SD rats were placed with trapped SD rats that were either strangers (n = 12, SD stranger condition) or cagemates (n = 8, SD cagemate condition) in the helping behavior test described above. Cagemates were pair-housed for 2 weeks prior to the experiment. Strangers were SD males from a different cohort, born in the same week but on a different day as the test rats. On each day of testing, a different stranger, to whom the free rat had no prior exposure, was trapped in the restrainer. Most rats in both SD cagemate (6/8, 75%) and SD stranger (10/12, 83%) conditions acted pro-socially, learning to release the trapped rat, and becoming openers (Figure 1; see Methods for opener definition). Rats in the two conditions were similarly active as measured by velocity (two-tailed Student’s t test, p>0.05), spent similar amount of time near the trapped rat (two-tailed Student’s t test, p>0.05), and began to open the door on around the same day (4.0 ± 1.1 days for trapped cagemates; 3.7 ± 0.8 for trapped strangers, mean ± SEM). Thus, rats were as motivated to help strangers as they were to help cagemates, showing that individual familiarity is not required for pro-social behavior in rats.

Figure 1

Download asset Open asset

The results above indicate that rats are motivated to help unfamiliar rats of their own strain. To determine if rats extend help to rats from a different strain, free SD rats were tested in the helping behavior test with trapped rats of the black-caped Long-Evans (LE) strain, which were either cagemates (n = 7, LE cagemate condition) or strangers (n = 16, LE stranger condition). SD rats did not release LE strangers with only a minority becoming openers (4/16, 25% openers; Figure 2; Video 1). In contrast, most SD rats in the LE cagemate condition became openers (5/7, 71%; χ2, p=0.04), learning to open the restrainer on average on day 3.8 ± 1.7 (mean ± SEM, Figure 2). Thus, rats help strangers of their own strain but not strangers of a different strain, suggestive of an in-strain bias for pro-social behavior. Moreover, short-term, paired-housing with a rat from a different strain is sufficient to motivate helping for that individual rat.

Figure 2

Download asset Open asset

Video 1

Download asset

We then examined whether SD rats that were familiar with one LE individual would be motivated to help LE strangers. SD rats were pair-housed with an LE cagemate for 2 weeks, then re-housed with an SD rat, and a week later, tested in the helping behavior test with trapped LE strangers (n = 12, LE familiar condition; Figure 2). In contrast to SD rats with no exposure to the LE strain, most SD rats familiar with one LE individual became openers for LE strangers (8/12, 67%; χ2, p=0.03). They learned to open the door on average on day 4.0 ± 1.0 despite a lack of individual familiarity with the trapped LE rat (Figure 2). This experiment shows that social experience with one individual rat of a different strain is sufficient to motivate helping towards unfamiliar members of that strain. This provides further evidence that individual familiarity is not required for helping.

Finally, to determine if helping behavior is at all influenced by the strain of the trapped rat (SD, LE), or if strain bias in helping is entirely due to strain familiarity (familiar, unfamiliar), SD rats were fostered and raised with LE rats from birth, in an environment that effectively prevented exposure to others of their own strain (fostered conditions, Figure 3). If rats are innately motivated to help rats of their own strain, then SD rats raised exclusively with LE rats (fostered) should act pro-socially towards other SDs. In contrast, if strain familiarity is the only determinant of pro-social behavior, these rats should not help their own kind. At 2 months of age, fostered rats were tested with trapped rats that were SD strangers (n = 8, fostered+SD) or LE strangers (n = 8, fostered+LE). Fostered SD rats did not help trapped SD strangers (Figure 4; Video 2). Only 1 of 8 fostered SD rats (12.5%) became an opener, establishing that rats are not innately motivated to help their own strain. In contrast, fostered rats did help LE strangers (5/8, 62.5%; χ2, p=0.04) as expected from the pro-social influence of strain familiarity. Thus, strain familiarity, even to one’s own strain, is required for the expression of helping behavior.

Figure 3

Download asset Open asset

Figure 4

Download asset Open asset

Video 2

Download asset

The finding that fostered rats did not help SD strangers indicates that a rat’s familiarity with himself is insufficient to motivate helping for individuals of his strain. Instead, social interaction with another rat, such as that occurring while two rats live together, is critical to shaping pro-social motivation. Moreover, since rats tested with strangers from unfamiliar strains did not become openers across the days of testing, the exposure and interactions afforded by testing sessions appear insufficient to produce pro-social motivation.

Fostered rats were noticeably more anxious than naturally reared rats. In open-field testing conducted prior to the experiment, fostered rats spent more time in the corners of the arena than rats in other conditions (33.1 ± 2.7 s/min for fostered rats; 25.0 ± 1.9 s/min for naturally reared rats; files with open field data for SD cagemate and SD strangers were corrupted and therefore not included; two-tailed Student’s t test, p<0.02; Figure 5A). Moreover, fostered rats that opened the restrainer began to do so significantly later (day 8.0 ± 1.1 for fostered rats; 4.5 ± 0.5 for all other rats; two-tailed Student’s t test, p<0.01; Figures 1–2, 4B). Fostered rats were tested for an extra day, confirming that opening behavior persisted. These data suggest that fostering rats in a different-strain environment is associated with increased anxiety. A same-strain, cross-fostering control condition is needed to distinguish whether strain, fostering, or both drive this effect.

Figure 5

Download asset Open asset

Across all conditions, the free rat’s familiarity with the strain of the trapped rat is the common determinant of whether helping behavior occurred (Figure 6A). Most rats in familiar strain conditions became openers (33/47, 74%) whereas only 21% (5/24) of rats in unfamiliar strain conditions did (χ2, p<0.001). Rats tested with a familiar strain experienced opening the restrainer door as rewarding, as they typically opened it on consecutive days (Figure 6B–C). In contrast, rats tested with unfamiliar strains rarely opened on consecutive days, suggesting that opening was not rewarding for these animals. As open field performance and alarm calls were not different for familiar and unfamiliar strain conditions (Figure 5C), it is unlikely that trait anxiety or the trapped rat’s distress accounts for the results.

Figure 6

Download asset Open asset

When tested with familiar strains, helping behavior was demonstrated equally for strangers and cagemates. Yet, the underlying affective response might differ in these conditions. In support of this idea, rats displayed a different movement pattern when tested with a trapped cagemate or stranger. Rats tested with a trapped cagemate were significantly more active prior to door-opening than rats tested with a stranger (MMA, p<0.05, Figure 7A). However, there was no difference in the distance from the restrainer in these conditions (Figure 7B). These results demonstrate that rats were equally motivated to help, but not equally aroused by, a trapped cagemate and stranger.

Figure 7

Download asset Open asset

Door-opening behavior overlapped greatly, but not completely, with strain familiarity. Across all conditions, rats who became openers demonstrated an affiliative behavioral pattern. Prior to door-opening, openers spent more time around the closed restrainer than did non-openers (two-tailed Student’s t test, p<0.01; Figure 8A; Video 1). Following the trapped rat’s exit from the restrainer, significantly less fights were observed for openers than for non-openers (two-tailed Student’s t test, p<0.01; Figure 8A). Baseline anxiety level was assessed by the time spent in the corners of the arena during open-field testing. Only for openers, baseline anxiety was positively correlated with the first day of opening (Figure 8B), suggesting that anxiety negatively impacts successful helping in the presence of pro-social motivation. Rats were less active before door-opening compared to after door-opening (repeated measures ANOVA, main effect, p<0.001; Figure 8C). Pairwise comparisons found that this effect was due to significantly reduced activity in non-openers prior to door opening, which was not the case for openers (pairwise comparisons, p<0.05; Figure 8C). This difference may result from either non-openers’ greater anxiety or reduced interest in the trapped rat.

Figure 8

Download asset Open asset

This study demonstrates that helping another rat, by releasing it from a restrainer, is flexibly applied to select others based on previous social experience. It is neither the individual identity nor the particular strain of the rat in need that motivates helping. Rather, it is the prior social experience of the free rat with any member of the trapped rat’s strain that determines the target group for helping. Thus, rats help another rat from a given strain (same or different) only if they have previously lived with a member of that strain.

Rats pick up sensory cues from their cagemates that are retained and utilized to discriminate between strangers that share those cues and those that do not. This information then plays a key role in eliciting pro-social behavior, and could potentially be used for other behavioral decisions as well, when encountering an unfamiliar individual, effectively forming group categories. The experiments delineated above are not informative of the sensory modalities participating in the classification of strangers as similar or different to the cagemate. Previous research points to the importance of vision, olfaction and audition for affective communication between mice (Langford et al., 2006; Jeon et al., 2010). It is possible that helping behavior in rats similarly relies on visual, olfactory, auditory, and also tactile cues as the clear and perforated restrainer allows for full sensory communication between the free and trapped rats.

The present study effectively demonstrates that strain identity is meaningless without social experience during development. Fostered rats raised without social interactions with their own strain were not motivated to help strangers of their strain, compelling evidence against an innate bias for pro-social behavior towards one’s own kind. This finding is congruent with studies showing that neither kinship nor perceived similarity is needed to motivate pro-social behavior in primates (Batson et al., 2005; Horner et al., 2011; Baden et al., 2013). In nature, social animals typically live with related others, and thus a pro-social bias favoring familiar others would also favor genetically similar others. Yet, relying on social experience rather than genetic similarity for guiding pro-social behavior has an added value in that it allows animals to flexibly adapt to different circumstances (Dugatkin, 2002). Assigning an affective meaning to a group category following social experience would be an efficient mechanism for appropriately extending pro-social behavior towards unknown individuals belonging to that same group.

While door-opening has an obvious pro-social outcome, a variety of motivations could contribute to this behavior. We have previously excluded the possibilities that door-opening depends on reward from either motor mastery or social contact (Ben-Ami Bartal et al., 2011). In addition it is unlikely that rats were motivated to open the restrainer by aggressive or anti-social motivations (Myer and White, 1965) because conflict between the free and trapped rats was minimal for opener pairs. As non-openers tested with an unfamiliar strain were not less active before door-opening than openers tested with a familiar strain (Figure 8C), differences in general arousal cannot account for the observed results. Given the greater interest in the trapped rat shown by openers and the lack of aggressive interactions between opener pairs, the authors favor the interpretation that rats open the restrainer door in order to terminate the trapped rat’s distress.

While we did not see any difference in helping behavior expressed toward strangers and cagemates, the underlying affective responses may have differed. Indeed, movement velocity was greater for rats tested with cagemates compared to those tested with strangers, indicative of different motivational states or magnitudes. Nonetheless, rats were sufficiently motivated to help strangers. This result is consistent with previous demonstrations of helping behavior expressed toward strangers in other animals, including humans (Warneken and Tomasello, 2006; Batson et al., 2007; Loggia et al., 2008; Custance and Mayer, 2012; Tan and Hare, 2013). While emotional contagion has been demonstrated for both individually familiar and unfamiliar mouse pairs (Chen et al., 2009; Jeon et al., 2010), it may be facilitated by individual familiarity (Langford et al., 2006; Jeon et al., 2010). Work in dogs and primates further supports a familiarity effect for emotional contagion (Palagi et al., 2009; Campbell and de Waal, 2011; Silva et al., 2012).

Empathy, the capacity to share and recognize the emotional states of another (Decety, 2011), often motivates approach and pro-social behavior and caring in humans (Eisenberg and Miller, 1987). The empathic response involves activation of common neural networks for processing one’s own and another’s distress (Decety et al., 2012). Some forms of empathy are primarily dependent on subcortical neural structures that are phylogenetically conserved across mammalian species (Decety and Svetlova, 2012). Emotional contagion, a fundamental component of empathy resulting when the emotion of one individual evokes a matching emotional state in another individual (Preston and de Waal, 2002), has been demonstrated in rodents (Chen et al., 2009; Langford et al., 2006). Thus, rodents, and mammals in general, may share a mechanism for mobilizing pro-social motivation in response to the distress of another individual. We would argue that a rodent form of empathy, as defined above, is the main motivation for the helping behavior observed in our studies. Moreover, the absence of door-opening for rats of unfamiliar strains likely reflects a reduced empathic arousal of the free rats in these conditions.

Rats that are not familiar with a different strain do not act pro-socially towards others of that strain. The selectivity with which rats engage in helping behavior is further evidence that releasing a trapped rat is an intentional social behavior, congruent with an empathic drive to help some rats, but not others. Yet, social experience can modify this behavior. We conclude that through social interactions, rats form affective bonds that elicit empathy and motivate helping. This motivation to help is extended to strangers of familiar strains, showing that rats form groups based on social experience. As is the case for humans (Xu et al., 2009; Mathur et al., 2010), rats base the bias for pro-social behavior on group membership. And as for humans, a diverse social experience was effective in mitigating such bias (Chiao et al., 2008; Elfenbein and Ambady, 2003; Madsen et al., 2007; Telzer et al., 2013; Zuo and Han, 2013). Moreover, we have demonstrated that for rats, genetic similarity does not influence pro-social motivation. Rather, groups are socially defined. Whereas social bias is hard to overcome through cognitive effort (Dovidio et al., 2002; Johnson et al., 2002; Amodio et al., 2004; Correll et al., 2007), our results support the existence of at least one mechanism for altering group membership that does not require complex cognition.

1. 1. Akyazi I
   2. Eraslan E

   (2014) Transmission of stress between cagemates: a study in rats

   Physiology & Behavior 123:114–118.

   https://doi.org/10.1016/j.physbeh.2013.10.006

   • Google Scholar
2. 1. Amodio DM
   2. Harmon-Jones E
   3. Devine PG
   4. Curtin JJ
   5. Hartley SL
   6. Covert AE

   (2004) Neural signals for the detection of unintentional race bias

   Psychological Science 15:88–93.

   https://doi.org/10.1111/j.0963-7214.2004.01502003.x

   • Google Scholar
3. 1. Atsak P
   2. Orre M
   3. Bakker P
   4. Cerliani L
   5. Roozendaal B
   6. Gazzola V
   7. Moita M
   8. Keysers C

   (2011) Experience modulates vicarious freezing in rats: a model for empathy

   PLOS ONE 6:e21855.

   https://doi.org/10.1371/journal.pone.0021855

   • Google Scholar
4. 1. Baden AL
   2. Wright PC
   3. Louis EE Jr
   4. Bradley BJ

   (2013) Communal nesting, kinship, and maternal success in a social primate

   Behavioral Ecology and Sociobiology 67:1939–1950.

   https://doi.org/10.1007/s00265-013-1601-y

   • Google Scholar
5. 1. Batson CD
   2. Lishner DA
   3. Cook J
   4. Sawyer S

   (2005) Similarity and nurturance: two possible sources of empathy for strangers

   Basic and Applied Social Psychology 27:15–25.

   https://doi.org/10.1207/s15324834basp2701_2

   • Google Scholar
6. 1. Batson CD
   2. Eklund JH
   3. Chermok VL
   4. Hoyt JL
   5. Ortiz BG

   (2007) An additional antecedent of empathic concern: valuing the welfare of the person in need

   Journal of Personality and Social Psychology 93:65–74.

   https://doi.org/10.1037/0022-3514.93.1.65

   • Google Scholar
7. 1. Ben-Ami Bartal I
   2. Decety J
   3. Mason P

   (2011) Empathy and pro-social behavior in rats

   Science 334:1427–1430.

   https://doi.org/10.1126/science.1210789

   • Google Scholar
8. 1. Campbell MW
   2. de Waal FB

   (2011) Ingroup-outgroup bias in contagious yawning by chimpanzees supports link to empathy

   PLOS ONE 6:e18283.

   https://doi.org/10.1371/journal.pone.0018283

   • Google Scholar
9. 1. Champagne FA
   2. Francis DD
   3. Mar A
   4. Meaney MJ

   (2003) Variations in maternal care in the rat as a mediating influence for the effects of environment on development

   Physiology & Behavior 79:359–371.

   https://doi.org/10.1016/S0031-9384(03)00149-5

   • Google Scholar
10. 1. Chen Q
    2. Panksepp JB
    3. Lahvis GP

    (2009) Empathy is moderated by genetic background in mice

    PLOS ONE 4:e4387.

    https://doi.org/10.1371/journal.pone.0004387

    • Google Scholar
11. 1. Chiao JY
    2. Iidaka T
    3. Gordon HL
    4. Nogawa J
    5. Bar M
    6. Aminoff E
    7. Sadato N
    8. Ambady N

    (2008) Cultural specificity in amygdala response to fear faces

    Journal of Cognitive Neuroscience 20:2167–2174.

    https://doi.org/10.1162/jocn.2008.20151

    • Google Scholar
12. 1. Church RM

    (1959) Emotional reactions of rats to the pain of others

    Journal of Comparative and Physiological Psychology 52:132–134.

    https://doi.org/10.1037/h0043531

    • Google Scholar
13. 1. Cialdini RB
    2. Brown SL
    3. Lewis BP
    4. Luce C
    5. Neuberg SL

    (1997) Reinterpreting the empathy–altruism relationship: when one into one equals oneness

    Journal of Personality and Social Psychology 73:481–494.

    https://doi.org/10.1037/0022-3514.73.3.481

    • Google Scholar
14. 1. Clay Z
    2. de Waal FB

    (2013) Bonobos respond to distress in others: consolation across the age spectrum

    PLOS ONE 8:e55206.

    https://doi.org/10.1371/journal.pone.0055206

    • Google Scholar
15. 1. Correll J
    2. Park B
    3. Judd CM
    4. Wittenbrink B
    5. Sadler MS
    6. Keesee T

    (2007) Across the thin blue line: police officers and racial bias in the decision to shoot

    Journal of Personality and Social Psychology 92:1006–1023.

    https://doi.org/10.1037/0022-3514.92.6.1006

    • Google Scholar
16. 1. Custance D
    2. Mayer J

    (2012) Empathic-like responding by domestic dogs (Canis familiaris) to distress in humans: an exploratory study

    Animal Cognition 15:851–859.

    https://doi.org/10.1007/s10071-012-0510-1

    • Google Scholar
17. 1. Decety J

    (2011) The neuroevolution of empathy

    Annals of the New York Academy of Sciences 1231:35–45.

    https://doi.org/10.1111/j.1749-6632.2011.06027.x

    • Google Scholar
18. 1. Decety J
    2. Svetlova M

    (2012) Putting together phylogenetic and ontogenetic perspectives on empathy

    Developmental Cognitive Neuroscience 2:1–24.

    https://doi.org/10.1016/j.dcn.2011.05.003

    • Google Scholar
19. 1. Decety J
    2. Norman GJ
    3. Berntson GG
    4. Cacioppo JT

    (2012) A neurobehavioral evolutionary perspective on the mechanisms underlying empathy

    Progress in Neurobiology 98:38–48.

    https://doi.org/10.1016/j.pneurobio.2012.05.001

    • Google Scholar
20. 1. Dovidio JF
    2. Gaertner SL
    3. Kawakami K
    4. Hodson G

    (2002) Why can’t we just get along? Interpersonal biases and interracial distrust

    Cultural Diversity & Ethnic Minority Psychology 8:88–102.

    https://doi.org/10.1037/1099-9809.8.2.88

    • Google Scholar
21. 1. Dugatkin LA

    (2002) Animal cooperation among unrelated individuals

    Naturwissenschaften 89:533–541.

    https://doi.org/10.1007/s00114-002-0379-y

    • Google Scholar
22. Book

    1. Echols S
    2. Correll J

    (2012)

    It’s more than skin deep: empathy and helping behavior across social groups

    In: Decety J, editors. Empathy: from bench to bedside. Cambridge: MIT Press. pp. 55–71.

    • Google Scholar
23. 1. Eisenberg N
    2. Miller PA

    (1987) The relation of empathy to prosocial and related behaviors

    Psychological Bulletin 101:91–119.

    https://doi.org/10.1037/0033-2909.101.1.91

    • Google Scholar
24. 1. Eisenberg N
    2. Fabes RA
    3. Miller PA
    4. Fultz J
    5. Shell R
    6. Mathy RM
    7. Reno RR

    (1989) Relation of sympathy and personal distress to prosocial behavior: a multimethod study

    Journal of Personality and Social Psychology 57:55–66.

    https://doi.org/10.1037/0022-3514.57.1.55

    • Google Scholar
25. 1. Elfenbein HA
    2. Ambady N

    (2003) When familiarity breeds accuracy: cultural exposure and facial emotion recognition

    Journal of Personality and Social Psychology 85:276–290.

    https://doi.org/10.1037/0022-3514.85.2.276

    • Google Scholar
26. 1. Hamilton DW

    (1984) The genetical evolution of social behavior I

    Journal of Theoretical Biology 7:1–16.

    https://doi.org/10.1016/0022-5193(64)90038-4

    • Google Scholar
27. 1. Hatchwell BJ
    2. Sharp SP
    3. Beckerman AP
    4. Meade J

    (2013) Ecological and demographic correlates of helping behaviour in a cooperatively breeding bird

    Journal of Animal Ecology 82:486–494.

    https://doi.org/10.1111/1365-2656.12017

    • Google Scholar
28. 1. Heinrich B
    2. Marzluff J

    (1995)

    Why ravens share

    American Scientist 83:342–349.

    • Google Scholar
29. 1. Horner V
    2. Carter JD
    3. Suchak M
    4. de Waal FB

    (2011) Spontaneous prosocial choice by chimpanzees

    Proceedings of the National Academy of Sciences of the United States of America 108:13847–13851.

    https://doi.org/10.1073/pnas.1111088108

    • Google Scholar
30. Book

    1. Hornstein HA

    (1978)

    Promotive tension and prosocial behavior: a Lewinian analysis

    In: Wispé L, editors. Altruism, sympathy, and helping: psychological and sociological principles. New York: Academic. pp. 177–207.

    • Google Scholar
31. 1. Jeon D
    2. Kim S
    3. Chetana M
    4. Jo D
    5. Ruley HE
    6. Lin SY
    7. Rabah D
    8. Kinet JP
    9. Shin HS

    (2010) Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC

    Nature Neuroscience 13:482–488.

    https://doi.org/10.1038/nn.2504

    • Google Scholar
32. 1. Johnson JD
    2. Simmons CH
    3. Jordan A
    4. MacLean L
    5. Taddei J
    6. Thomas D

    (2002) Rodney King and O. J. revisited: the impact of race and defendant empathy induction on judicial decisions

    Journal of Applied Social Psychology 32:1208–1223.

    https://doi.org/10.1111/j.1559-1816.2002.tb01432.x

    • Google Scholar
33. 1. Knapska E
    2. Mikosz M
    3. Werka T
    4. Maren S

    (2010) Social modulation of learning in rats

    Learning & Memory 17:35–42.

    https://doi.org/10.1101/lm.1670910

    • Google Scholar
34. 1. Lamm C
    2. Meltzoff AN
    3. Decety J

    (2010) How do we empathize with someone who is not like us? A functional magnetic resonance imaging study

    Journal of Cognitive Neuroscience 22:362–376.

    https://doi.org/10.1162/jocn.2009.21186

    • Google Scholar
35. 1. Langford DJ
    2. Crager SE
    3. Shehzad Z
    4. Smith SB
    5. Sotocinal SG
    6. Levenstadt JS
    7. Chanda ML
    8. Levitin DJ
    9. Mogil JS

    (2006) Social modulation of pain as evidence for empathy in mice

    Science 312:1967–1970.

    https://doi.org/10.1126/science.1128322

    • Google Scholar
36. 1. Lee PC

    (1987) Allomothering among African elephants

    Animal Behaviour 35:278–291.

    https://doi.org/10.1016/S0003-3472(87)80234-8

    • Google Scholar
37. 1. Levine RA
    2. Norenzayan A
    3. Philbrick K

    (2001) Cross-cultural differences in helping strangers

    Journal of Cross-Cultural Psychology 32:543–560.

    https://doi.org/10.1177/0022022101032005002

    • Google Scholar
38. 1. Levine M
    2. Prosser A
    3. Evans D
    4. Reicher S

    (2005) Identity and emergency intervention: how social group membership and inclusiveness of group boundaries shape helping behavior

    Personality & Social Psychology Bulletin 31:443–453.

    https://doi.org/10.1177/0146167204271651

    • Google Scholar
39. 1. Loggia ML
    2. Mogil JS
    3. Bushnell MC

    (2008) Empathy hurts: compassion for another increases both sensory and affective components of pain perception

    Pain 136:168–176.

    https://doi.org/10.1016/j.pain.2007.07.017

    • Google Scholar
40. 1. Madsen EA
    2. Tunney RJ
    3. Fieldman G
    4. Plotkin HC
    5. Dunbar RI
    6. Richardson JM
    7. McFarland D

    (2007) Kinship and altruism: a cross-cultural experimental study

    British Journal of Psychology 98:339–359.

    https://doi.org/10.1348/000712606X129213

    • Google Scholar
41. 1. Mathur VA
    2. Harada T
    3. Lipke T
    4. Chiao JY

    (2010) Neural basis of extraordinary empathy and altruistic motivation

    NeuroImage 51:1468–1475.

    https://doi.org/10.1016/j.neuroimage.2010.03.025

    • Google Scholar
42. 1. Mogil JS

    (2012) The surprising empathic abilities of rodents

    Trends in Cognitive Sciences 3:143–144.

    https://doi.org/10.1016/j.tics.2011.12.012

    • Google Scholar
43. 1. Myer JS
    2. White RT

    (1965) Aggressive motivation in the rat

    Animal Behaviour 13:430–433.

    https://doi.org/10.1016/0003-3472(65)90102-8

    • Google Scholar
44. 1. Nowbahari E
    2. Scohier A
    3. Durand J
    4. Hollis K

    (2009) Ants, Cataglyphis cursor, use precisely directed rescue behavior to free entrapped relatives

    PLOS ONE 4:e6573.

    https://doi.org/10.1371/journal.pone.0006573

    • Google Scholar
45. 1. Owens DD
    2. Owens MJ

    (1984) Helping behaviour in brown Hyenas

    Nature 308:843–845.

    https://doi.org/10.1038/308843a0

    • Google Scholar
46. 1. Palagi E
    2. Leone A
    3. Mancini G
    4. Ferrari PF

    (2009) Contagious yawning in gelada baboons as a possible expression of empathy

    Proceedings of the National Academy of Sciences of the United States of America 106:19262–19267.

    https://doi.org/10.1073/pnas.0910891106

    • Google Scholar
47. 1. Panksepp J
    2. Panksepp JB

    (2013) Toward a cross-species understanding of empathy

    Trends in Neurosciences 36:489–496.

    https://doi.org/10.1016/j.tins.2013.04.009

    • Google Scholar
48. 1. Panksepp JB
    2. Lahvis GP

    (2011) Rodent empathy and affective neuroscience

    Neuroscience & Biobehavioral Reviews 35:1864–1875.

    https://doi.org/10.1016/j.neubiorev.2011.05.013

    • Google Scholar
49. 1. Preston SD

    (2013) The Origins of altruism in offspring care

    Psychological Bulletin 139:1305–1341.

    https://doi.org/10.1037/a0031755

    • Google Scholar
50. 1. Preston SD
    2. de Waal FBM

    (2002)

    Empathy: Its ultimate and proximate bases

    The Behavioral and Brain Sciences 25:1–20.

    • Google Scholar
51. 1. Rice GE
    2. Gainer P

    (1962) ‘Altruism’ in the albino rat

    Journal of Comparative and Physiological Psychology 55:123–125.

    https://doi.org/10.1037/h0042276

    • Google Scholar
52. 1. Rutte C
    2. Taborsky M

    (2007) Generalized reciprocity in rats

    PLOS Biology 5:e196.

    https://doi.org/10.1371/journal.pbio.0050196

    • Google Scholar
53. 1. Silva K
    2. Bessa J
    3. de Sousa L

    (2012) Auditory contagious yawning in domestic dogs (Canis familiaris): first evidence for social modulation

    Animal Cognition 15:721–724.

    https://doi.org/10.1007/s10071-012-0473-2

    • Google Scholar
54. 1. Sturmer S
    2. Snyder M
    3. Kropp A
    4. Siem B

    (2006) Empathy-motivated helping: the moderating role of group membership

    Personality & Social Psychology Bulletin 32:943–956.

    https://doi.org/10.1177/0146167206287363

    • Google Scholar
55. 1. Tan J
    2. Hare B

    (2013) Bonobos share with strangers

    PLOS ONE 8:e51922.

    https://doi.org/10.1371/journal.pone.0051922

    • Google Scholar
56. 1. Telzer EH
    2. Humphreys KL
    3. Shapiro M
    4. Tottenham N

    (2013) Amygdala sensitivity to race is not present in childhood but emerges over adolescence

    Journal of Cognitive Neuroscience 25:234–244.

    https://doi.org/10.1523/JNEUROSCI.1272-13.2013

    • Google Scholar
57. 1. Tsoory MM
    2. Youdim MB
    3. Schuster R

    (2012) Social-cooperation differs from individual behavior in hypothalamic and striatal monoamine function: evidence from a laboratory rat model

    Behavioural Brain Research 232:252–263.

    https://doi.org/10.1016/j.bbr.2012.04.032

    • Google Scholar
58. 1. Viana DS
    2. Gordo I
    3. Sucena E
    4. Moita MAP

    (2010) Cognitive and motivational requirements for the emergence of cooperation in a rat social Game

    PLOS ONE 5:e8483.

    https://doi.org/10.1371/journal.pone.0008483

    • Google Scholar
59. 1. Warneken F
    2. Tomasello M

    (2006) Altruistic helping in human infants and young chimpanzees

    Science 311:1301–1303.

    https://doi.org/10.1126/science.1121448

    • Google Scholar
60. 1. Wilkinson GS

    (1984) Reciprocal food sharing in vampire bats

    Nature 308:181–184.

    https://doi.org/10.1038/308181a0

    • Google Scholar
61. 1. Xu X
    2. Zuo X
    3. Wang X
    4. Han S

    (2009) Do you feel my pain? Racial group membership modulates empathic neural responses

    The Journal of Neuroscience 29:8525–8529.

    https://doi.org/10.1523/JNEUROSCI.2418-09.2009

    • Google Scholar
62. 1. Yamamoto S
    2. Humle T
    3. Tanaka M

    (2012) Chimpanzees’ flexible targeted helping based on an understanding of conspecifics’ goals

    Proceedings of the National Academy of Sciences of the United States of America 109:3588–3592.

    https://doi.org/10.1073/pnas.1108517109

    • Google Scholar
63. 1. Zuo X
    2. Han S

    (2013) Cultural experiences reduce racial bias in neural responses to others’ suffering

    Culture and Brain 1:34–46.

    https://doi.org/10.1007/s40167-013-0002-4

    • Google Scholar

Author details

1. Inbal Ben-Ami Bartal

   Department of Neurobiology, University of Chicago, Chicago, United States

   Contribution

   IB-AB, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   No competing interests declared.

2. David A Rodgers

   Department of Neurobiology, University of Chicago, Chicago, United States

   Contribution

   DAR, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   Competing interests

   No competing interests declared.

3. Maria Sol Bernardez Sarria

   Department of Neurobiology, University of Chicago, Chicago, United States

   Contribution

   MSBS, Acquisition of data, Analysis and interpretation of data

   Competing interests

   No competing interests declared.

4. Jean Decety

   1. Department of Psychology, University of Chicago, Chicago, United States
   2. Department of Psychiatry and Behavioral Neuroscience, University of Chicago, Chicago, United States
   3. Committee on Neurobiology, University of Chicago, Chicago, United States

   Contribution

   JD, Contributed critically to the conceptual and theoretical framework for this work, Drafting or revising the article

   Competing interests

   No competing interests declared.

5. Peggy Mason

   1. Department of Neurobiology, University of Chicago, Chicago, United States
   2. Committee on Neurobiology, University of Chicago, Chicago, United States

   Contribution

   PM, Conception and design, Acquisition of data, Analysis and interpretation of data, Drafting or revising the article

   For correspondence

   pmason@uchicago.edu

   Competing interests

   PM: Reviewing editor, eLife.

• 14,268

  views

• 1,680

  downloads

• 189

  citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.