Empathy and Pro-Social Behavior in Rats
Inbal Ben-Ami Bartal, et al.
Science 334, 1427 (2011);
DOI: 10.1126/science.1210789

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REPORTS
fluctuations in population density provide important information to guide decisions on disease
control strategies, international aid and humanitarian responses, and assessments of economic
development.
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Empathy and Pro-Social
Behavior in Rats
Inbal Ben-Ami Bartal,1 Jean Decety,1,2,4 Peggy Mason3,4
Whereas human pro-social behavior is often driven by empathic concern for another, it is unclear
whether nonprimate mammals experience a similar motivational state. To test for empathicallymotivated pro-social behavior in rodents, we placed a free rat in an arena with a cagemate trapped in a
restrainer. After several sessions, the free rat learned to intentionally and quickly open the restrainerand free the cagemate. Rats did not open empty or object-containing restrainers. They freed cagemateseven when social contact was prevented. When liberating a cagemate was pitted against chocolate
contained within a second restrainer, rats opened both restrainers and typically shared the chocolate.
Thus, rats behave pro-socially in response to a conspecific’s distress, providing strong evidence forbiological roots of empathically motivated helping behavior.
ro-social behavior refers to actions that are
intended to benefit another. One common
motivator of pro-social behavior in humans is empathic concern: an other-oriented
emotional response elicited by and congruent
with the perceived welfare of an individual inP

1
Department of Psychology, University of Chicago, Chicago,
IL, USA. 2Department of Psychiatry and Behavioral Neuroscience, University of Chicago, Chicago, IL, USA. 3Departmentof Neurobiology, University of Chicago, Chicago, IL, USA.
4
Committee on Neurobiology, University of Chicago, Chicago,
IL, USA.

distress (1, 2). Sharing another’s distress via
emotional contagion can result in overwhelming
fear and immobility unless one’s own distressis down-regulated, thus allowing empathicallydriven pro-social behavior (3, 4). Building on
observations of emotional contagion in rodents(5–10), we sought to determine whether rats
are capable of empathically motivated helping
behavior. We tested whether the presence of atrapped cagemate induces a pro-social motivational state in rats, leading them to open the restrainer door and liberate the cagemate.

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Acknowledgments: This study was supported by the Billand Melinda Gates Foundation. A.J.T. is supported by a grantfrom the Bill and Melinda Gates Foundation (49446).
A.J.T., M.J.F., and B.T.G. are also supported by the Researchand Policy for Infectious Disease Dynamics (RAPIDD) programof the Science and Technology Directorate, Department ofHomeland Security and the Fogarty International Center, NIH.
All DMSP OLS imagery is available from the Space Physics
Interactive Data Resource (http://spidr.ngdc.noaa.gov/spidr/).

Supporting Online Materialwww.sciencemag.org/cgi/content/full/334/6061/1424/DC1
Materials and Methods
SOM Text
Figs. S1 to S3Tables S1 to S4
References (28–40)
1 July 2011; accepted 21 October 201110.1126/science.1210554

Rats were housed in pairs for 2 weeks before
the start of testing. In each session, a rat (the freerat) was placed in an arena with a centrally located restrainer in which a cagemate was trapped(trapped condition, n = 30 rats, 6 females). The
free rat could liberate the trapped rat by applying
enough force to tip over the restrainer door (Fig.
1A). If a free rat failed to open the door, the experimenter opened it halfway, allowing the trapped
rat to escape and preventing learned helplessness.
Rats remained in the arena together for the final
third of the session. Door-opening only counted
as such if the free rat opened the door before
the experimenter opened it halfway. Sessions
were repeated for 12 days. Control conditions
included testing a free rat with an empty restrainer (empty condition, n = 20 rats, 6 females)or toy rat–containing restrainer (object condition,n = 8 males). As an additional control, for thenumber of rats present, we tested a free rat with anempty restrainer and an unrestrained cagemate
located across a perforated divide (2+empty
condition, n = 12 males). Free rats’ heads weremarked and their movements were recorded witha top-mounted camera for offline analysis (11).
Free rats circled the restrainer, digging at it andbiting it, and contacted the trapped rat throughholes in the restrainer (Fig. 1B and movie S1).
They learned to open the door and liberate thetrapped cagemate within a mean of 6.9 T 2.9 days.
Free rats spent more time near the restrainer in

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As with any method, there are limitations tothe use of nighttime satellite imagery; the exact
association between brightness and population
density varies between locations and is affected byenvironmental (15) and economic factors (25–27).
Additionally, images must be selected carefully
to avoid contamination from solar and lunar illumination and cloud cover (SOM part 1).
Measuring the drivers of seasonal variability
in transmission rates, particularly in areas withsparse disease surveillance and strong epidemic
nonlinearities (2), is critical for improving thedesign of epidemiological control measures. It
is now possible to improve outbreak response
strategies based on fluctuations in population
density and disease transmission, as we haveshown for a recent measles outbreak in Niamey.
This would be particularly useful in areas withrepetitive seasonal fluctuations in density wheretargeted campaigns could maximize the numberof individuals present during vaccinations. It isalso possible that this method could be adapted
for near–real-time analyses, as images are uploaded
from the satellite within ~48 hours (although theusability of individual images is sensitive to environmental conditions).
The advantages of understanding changes in
population density are broadly applicable. This information can aid in estimating population changes
caused by large-scale human movements—i.e.,
displacement due to conflict (17) or recurring
movements such as the Hajj. Measurements of1427

the arena center [P < 0.001, mixed model analysis (MMA), Fig. 1C] and showed greater movement speed (hereafter termed activity, P < 0.001,
MMA, Fig. 1D) than did control rats. Before
learning to open the restrainer door, free rats inthe trapped condition stayed significantly more
active in the second half of sessions relative tothe first half than did rats in control conditions[P < 0.001, MMA, protected least significant
difference (PLSD) test, Fig. 1E]. Thus, rats were
motivated to move and act specifically in thepresence of a trapped cagemate.
In the trapped condition, the proportion of ratsthat opened the door increased (Fig. 2A), and thelatency to door-opening decreased (Fig. 2B andmovie S2) across sessions, which is evidence oflearning. Significantly more rats in the trapped[23 out of 30 (23/30)] than control (5/40) conditions were classified as “openers” by the end of
the experiment (P < 0.001, c-square test), opening the door within minutes of placement in thearena (11). A sharp increase in the free rat’s activity was observed at the time of door-opening(Fig. 2C), suggesting that the liberation of atrapped cagemate is a salient event.
Initially, rats in the trapped condition opened
the door in any of three ways: tipping the door
over from the side or top or pushing it up with
their heads. However, on days 6 to 12, they consistently opened the door with their heads (Fig.
2D). Furthermore, whereas rats initially froze
after the door fell over, later on they did notfreeze (Fig. 2E), demonstrating that door-opening
was the expected outcome of a deliberate, goaldirected action.
Ultrasonic (~23 kHz) vocalizations were collected from multiple testing arenas with a batdetector and were analyzed to determine whether
rats emitted alarm calls. Significantly more alarm
calls were recorded during the trapped condition(13%) than during the empty and object conditions [3 to 5%, P < 0.05 analysis of variance(ANOVA), PLSD < 0.05, Fig. 2F] in randomly
sampled files from all days of testing. Alarm calls
occurred more frequently (20 to 27%) on days
1 to 3, when door-opening was rare. In 90% of
files containing alarm calls on day 1, the trapped
rat was identified as the source; in the remaining
samples, we were not able to identify the caller.
These data suggest that trapped rats were indeed
stressed.
A greater proportion of female rats (6/6) thanmale rats (17/24) in the trapped condition became
door-openers (P < 0.05, c-square), which is consistent with suggestions that females are more
empathic than males (7, 12, 13). Further, female
rats in the trapped condition opened the restrainer
door at a shorter latency than males on days 7 to
12 (P < 0.01, MMA, Fig. 3A). Female rats werealso more active than males in the trapped condition (P < 0.001, ANOVA) but not in the empty
condition (Fig. 3B).
To examine whether individual differences inboldness influenced door-opening, we tested thelatency for approach to the ledge of a half-opened

1428

Fig. 1. (A) Top views of the trapped and 2+empty conditions and side views of the restrainer and door.
(B) The locations (0.5 frames per second) of representative free rats with respect to the restrainer (red box)
are plotted for each condition on day 1 of testing. (C) Rats in the trapped condition spent more time(mean T SEM) in the arena center (>5 cm away from the wall) than did rats in control conditions. (D) The
velocity (mean T SEM) of rats in the trapped condition was greater than that of control rats throughout thesession. (E) The ratio of the average activity during the second half of sessions relative to the average
activity during the first half (mean T SEM) was greater for rats in the trapped condition on days 1 to 6 thanfor rats in control conditions.

Fig. 2. (A) The proportion of rats in the trapped condition that opened the door increased across the daysof testing. (B) Only rats in the trapped condition opened the door at decreasing latencies across days oftesting. (C) Rats in the trapped condition showed a sharp increase in activity when the restrainer door was
opened (time 0). (D) Across days, free rats in the trapped condition developed a consistent opening style,lifting the door up with their heads. (E) As rats learned to open the door, they stopped freezing in response
to door-opening. (F) More alarm calls were recorded in the trapped condition (n = 67 sample files) than inempty (n = 64) or object (n = 67) conditions.

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Downloaded from www.sciencemag.org on January 17, 2012REPORTScage before the experiment (11). Animals who
became openers had lower approach latencies
than nonopeners (P < 0.01, t test), suggesting thatsuccessful opening behavior correlates with boldness scores (fig. S1). This demonstrates that individual trait differences may factor into theexpression of pro-social behavior.
To determine whether anticipation of social
interaction is necessary to motivate door-opening,
we tested rats in a modified setup in which thetrapped animal could only exit into a separate
arena (separated condition, Fig. 4, A and B). Rats
(12 pairs) were first exposed to the trapped condition (12 days); three rats did not open the dooron any of the last 3 days and were not tested
further. Next, rats were placed in the separated

setup with a restrainer that was either empty (separated empty) or contained a cagemate (separated
cagemate) for 29 days of testing. Finally, conditions were reversed so that rats previously inthe separated cagemate condition were tested in
the separated empty condition and vice versa,
for 27 days. Thus, all nine rats were tested incounterbalanced order with both an empty and afull restrainer. Rats placed in the separated cagemate condition either continued or returned to
opening the door at short latency as they had in
the trapped condition. In contrast, when rats wereplaced in the separated empty condition, they
stopped opening the door of the empty restrainer(P < 0.001, MMA, PLSD, Fig. 4, A and B). Thus,
rats opened the door of a cagemate-containing

Fig. 3. (A) Females in thetrapped, but not empty,
condition opened the doorat consistently shorter latencies than did males ondays 7 to 12. (B) Activity
was greater for females
than males in the trapped,
but not empty, condition.

Fig. 4. (A and B) Rats opened the door for a trapped cagemate even when nosocial interaction was possible between the two animals after door-opening. Dooropening was extinguished when the restrainer was empty but either resumed (A) or
persisted (B) when the restrainer contained a cagemate, regardless of the order ofwww.sciencemag.org

SCIENCE

restrainer but not of an empty restrainer, indicating that the expectation of social contact is notnecessary for eliciting pro-social behavior.
In order to examine the relative value of liberating a trapped cagemate, we tested a cohort ofrats in a cagemate versus chocolate paradigm.
When given a choice, these non–food-deprived
rats ate an average of >7 chocolate chips and norat chow, indicating that they found chocolate
highly palatable. The free rat was placed in anarena with two restrainers, one containing thetrapped cagemate and the other containing fivechocolate chips (chocolate cagemate condition,
Fig. 4, C and D). As a control, one restrainer was
empty while the other contained chocolate (chocolate empty condition). For rats in the chocolate cagemate condition, there was no differencein the door-opening latencies for the two restrainers during days 6 to 12 (Fig. 4C). In contrast, rats in the chocolate empty condition opened
the chocolate-containing restrainer more quickly
than the empty one (P < 0.01, t test, Fig. 4D).
These results show that the value of freeing a
trapped cagemate is on par with that of accessing chocolate chips. Like rats in the trapped
condition, rats needed several days (5.8 T 2.1) tolearn to open the chocolate restrainer, which isevidence that door-opening was neither easy nor
instinctual.
Although free rats in the chocolate cagemate condition could potentially eat all fiveDownloaded from www.sciencemag.org on January 17, 2012REPORTS

testing [n = 4 rats, (A); n = 5, (B)]. (C) On days 6 to 12, the latencies at which rats
opened a restrainer containing a trapped cagemate and one containing chocolate
chips were not different. (D) Rats in the chocolate empty condition opened theempty restrainer at significantly longer latencies than the chocolate restrainer.
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9 DECEMBER 20111429

chocolate chips, they shared them in half of alltrials (52%) and in 61% of trials on days 6 to
12. Rats in the chocolate empty condition ate
virtually all the chips (4.8 T 0.7), whereas freerats in the chocolate cagemate condition ate
fewer chips (3.5 T 1.5, P < 0.01, t test), whichallowed trapped rats to eat the remaining chips(1.5 T 1.4).
Our study demonstrates that rats behave
pro-socially when they perceive a conspecificexperiencing nonpainful psychological restraint
stress (14, 15), acting to end that distress throughdeliberate action. In contrast to previous work
(5, 9, 16, 17), the present study shows pro-social
behavior accomplished by the deliberate actionof a rat. Moreover, this behavior occurred in
the absence of training or social reward, andeven when in competition with highly palatablefood.
Our observations could have alternative
explanations. Rats may have acted to stop thealarm calls of the trapped rats (18). Yet alarm
calls occurred too infrequently to support this
explanation. Alternatively, rats may have been
attracted to the trapped cagemate by curiosity.
However, door-opening in the separated cagemate condition persisted for over a month, atime period over which curiosity extinguishes(19). Finally, door-opening could be a coincidental effect of high activity levels. This is unlikely because once rats learned to open the door,
they did so at short latency, using a consistentstyle, and were unsurprised by door-opening.
Additionally, door-opening is not easy, rendering accidental openings unlikely. Thus, the mostparsimonious interpretation of the observed helping behavior is that rats free their cagemate inorder to end distress, either their own or that of1430

the trapped rat, that is associated with the circumstances of the trapped cagemate. This emotional motivation, arguably the rodent homologof empathy, appears to drive the pro-social behavior observed in the present study.
The presence of empathy in nonhuman animals is gaining support in the scientific community (20–26), although skeptics remain (27).
In the current study, the free rat was not simply
empathically sensitive to another rat’s distress
but acted intentionally to liberate a trapped conspecific. The ability to understand and actively
respond to the affective state of a conspecific is
crucial for an animal’s successful navigation in
the social arena (4) and ultimately benefits groupsurvival.
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Acknowledgments: This research was supported by
grants from the National Institute on Drug Abuse(DA022978 and DA022429) to P.M. and from NSF(BCS-0718480) to J.D. The assistance of I. Boni, A. Brimmer,
U. Fonio, K. Hellman, A. Logli, J. Peralta, K. Ragsdale,
D. Rodgers, M. Sales, J. Wang, A. Weiss, and K. Yuan is
gratefully acknowledged.

Supporting Online Materialwww.sciencemag.org/cgi/content/full/334/6061/1427/DC1
Materials and Methods
Fig. S1
Table S1
Reference (28)7 July 2011; accepted 18 October 201110.1126/science.1210789

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