Experience modulates vicarious freezing in rats: a model for empathy
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The study of the neural basis of emotional empathy has received a surge of interest in recent years but mostly employing human neuroimaging. A simpler animal model would pave the way for systematic single cell recordings and invasive manipulations of the brain regions implicated in empathy. Recent evidence has been put forward for the existence of empathy in rodents. In this study, we describe a potential model of empathy in female rats, in which we studied interactions between two rats: a witness observes a demonstrator experiencing a series of footshocks. By comparing the reaction of witnesses with or without previous footshock experience, we examine the role of prior experience as a modulator of empathy. We show that witnesses having previously experienced footshocks, but not naïve ones, display vicarious freezing behavior upon witnessing a cage-mate experiencing footshocks. Strikingly, the demonstrator's behavior was in turn modulated by the behavior of the witness: demonstrators froze more following footshocks if their witness froze more. Previous experiments have shown that rats emit ultrasonic vocalizations (USVs) when receiving footshocks. Thus, the role of USV in triggering vicarious freezing in our paradigm is examined. We found that experienced witness-demonstrator pairs emitted more USVs than naïve witness-demonstrator pairs, but the number of USVs was correlated with freezing in demonstrators, not in witnesses. Furthermore, playing back the USVs, recorded from witness-demonstrator pairs during the empathy test, did not induce vicarious freezing behavior in experienced witnesses. Thus, our findings confirm that vicarious freezing can be triggered in rats, and moreover it can be modulated by prior experience. Additionally, our result suggests that vicarious freezing is not triggered by USVs per se and it influences back onto the behavior of the demonstrator that had elicited the vicarious freezing in witnesses, introducing a paradigm to study empathy as a social loop.
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In rats and mice, emotional contagion of others' distress brought about by foot shocks increased if the rats and mice had experienced foot shocks in the past.
“In rats and mice, the emotional contagion of others' distress brought about by foot shocks increased if the rats and mice had experienced the foot shocks in the past (Atsak et al., 2011; Sanders et al., 2013).”
From Helping behavior in prairie voles: a model of empathy and the importance of oxytocin (2022) · cites this paper as Atsak et al., 2011
In the imminent threat paradigm, observers respond to the demonstrators' fear with freezing and decreased heart rate, both indicating high fear levels.
“It has been shown that in the imminent threat paradigm the observers respond to the demonstrators' fear with freezing 152,158 and decreased heart rate, 159 both of which indicate high fear levels.”
From Ecological validity of social interaction tests in rats and mice (2019) · cites this paper as [158]
Vicarious freezing is significantly enhanced by prior experience with footshock.
“Comparing the reaction of witnesses with or without previous footshock experience, it has been shown that vicarious freezing is significantly enhanced by prior experience.158”
From Ecological validity of social interaction tests in rats and mice (2019) · cites this paper as [158]
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Cites
Action recognition in the premotor cortex
Gallese, V., Fadiga, L., Fogassi, L., & Rizzolatti, G. (1996) · Brain · doi:10.1093/brain/119.2.593 · Cited by 4,968 · see citing works
Empathy: its ultimate and proximate bases
Preston, S. D., & de Waal, F. B. M. (2002) · Behavioral and Brain Sciences · doi:10.1017/s0140525x02000018 · Cited by 4,126 · see citing works
Baron-Cohen, S., & Wheelwright, S. (2004) · Journal of Autism and Developmental Disorders · doi:10.1023/b:jadd.0000022607.19833.00 · Cited by 4,093 · see citing works
Empathy for Pain Involves the Affective but not Sensory Components of Pain
Singer, T., Seymour, B., O'Doherty, J., Kaube, H., Dolan, R. J., & Frith, C. D. (2004) · Science · doi:10.1126/science.1093535 · Cited by 3,929 · see citing works
Putting the Altruism Back into Altruism: The Evolution of Empathy
de Waal, F. B. M. (2008) · Annual Review of Psychology · doi:10.1146/annurev.psych.59.103006.093625 · Cited by 2,483 · see citing works
Both of Us Disgusted in My Insula
Wicker, B., Keysers, C., Plailly, J., Royet, J.-P., Gallese, V., & Rizzolatti, G. (2003) · Neuron · doi:10.1016/s0896-6273(03)00679-2 · Cited by 2,185 · see citing works
Self-citationParietal Lobe: From Action Organization to Intention Understanding
Fogassi, L., Ferrari, P. F., Gesierich, B., Rozzi, S., Chersi, F., & Rizzolatti, G. (2005) · Science · doi:10.1126/science.1106138 · Cited by 1,990 · see citing works
The social neuroscience of empathy
Singer, T., & Lamm, C. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04418.x · Cited by 1,981 · see citing works
Neural mechanisms of empathy in humans: a relay from neural systems for imitation to limbic areas
Carr, L., Iacoboni, M., Dubeau, M.-C., Mazziotta, J. C., & Lenzi, G. L. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0935845100 · Cited by 1,978 · see citing works
Hearing Sounds, Understanding Actions: Action Representation in Mirror Neurons
Kohler, E., Keysers, C., Umiltà, M. A., Fogassi, L., Gallese, V., & Rizzolatti, G. (2002) · Science · doi:10.1126/science.1070311 · Cited by 1,801 · see citing works
Self-citationEmpathic neural responses are modulated by the perceived fairness of others
Singer, T., Seymour, B., O'Doherty, J. P., Stephan, K. E., Dolan, R. J., & Frith, C. D. (2006) · Nature · doi:10.1038/nature04271 · Cited by 1,726 · cited 2× · see citing works
“While this conclusion may seem trivial, it actually brakes new grounds in the context of empathy research: most current models of empathy for pain or distress in human neuroscience used prerecorded stimuli [2,4,9,10,11,72,73,74] or used live interactions but prevented participants from viewing the reactions of their p…”
The empathic brain: how, when and why?
de Vignemont, F., & Singer, T. (2006) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2006.08.008 · Cited by 1,716 · see citing works
Sex differences in empathy and related capacities.
Eisenberg, N., & Lennon, R. (1983) · Psychological Bulletin · doi:10.1037/0033-2909.94.1.100 · Cited by 1,310 · see citing works
How do we perceive the pain of others? A window into the neural processes involved in empathy
Jackson, P. L., Meltzoff, A. N., & Decety, J. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2004.09.006 · Cited by 1,257 · see citing works
Umiltà, M. A., Kohler, E., Gallese, V., Fogassi, L., Fadiga, L., Keysers, C., & Rizzolatti, G. (2001) · Neuron · doi:10.1016/s0896-6273(01)00337-3 · Cited by 1,192 · see citing works
Self-citationSingle-Neuron Responses in Humans during Execution and Observation of Actions
Mukamel, R., Ekstrom, A. D., Kaplan, J., Iacoboni, M., & Fried, I. (2010) · Current Biology · doi:10.1016/j.cub.2010.02.045 · Cited by 1,178 · see citing works
Sex differences in the brain: implications for explaining autism
Baron-Cohen, S., Knickmeyer, R. C., & Belmonte, M. K. (2005) · Science · doi:10.1126/science.1115455 · Cited by 1,145 · see citing works
Human empathy through the lens of social neuroscience.
Decety, J., & Lamm, C. (2006) · The Scientific World JOURNAL · doi:10.1100/tsw.2006.221 · Cited by 1,051 · cited 2× · see citing works
“While this conclusion may seem trivial, it actually brakes new grounds in the context of empathy research: most current models of empathy for pain or distress in human neuroscience used prerecorded stimuli [2,4,9,10,11,72,73,74] or used live interactions but prevented participants from viewing the reactions of their p…”
InfluentialA Social-Neuroscience Perspective on Empathy
Jean Decety, A., & Jackson, P. L. (2006) · Current Directions in Psychological Science · doi:10.1111/j.0963-7214.2006.00406.x · Cited by 909 · see citing works
Social Modulation of Pain as Evidence for Empathy in Mice
Langford, D. J., Crager, S. E., Shehzad, Z., Smith, S. B., Sotocinal, S. G., Levenstadt, J. S., Chanda, M. L., Levitin, D. J., & Mogil, J. S. (2006) · Science · doi:10.1126/science.1128322 · Cited by 865 · see citing works
Keysers, C. (2004) · doi:10.1016/s0896-6273(04)00156-4 · Cited by 806 · see citing works
Self-citationSomatosensation in social perception
Keysers, C., Kaas, J. H., & Gazzola, V. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2833 · Cited by 787 · see citing works
Self-citationSex differences in empathy and related behaviors.
Hoffman, M. L. (1977) · Psychological Bulletin · doi:10.1037/0033-2909.84.4.712 · Cited by 755 · see citing works
Empathy and the somatotopic auditory mirror system in humans
Gazzola, V., Aziz-Zadeh, L., & Keysers, C. (2006) · Current Biology · doi:10.1016/j.cub.2006.07.072 · Cited by 752 · see citing works
Self-citationPain-related neurons in the human cingulate cortex
Hutchison, W. D., Davis, K. D., Lozano, A. M., Tasker, R. R., & Dostrovsky, J. O. (1999) · Nature Neuroscience · doi:10.1038/8065 · Cited by 681 · see citing works
Observational fear learning involves affective pain system and Cav1.2 Ca2+ channels in ACC
Jeon, D., Kim, S., Chetana, M., Jo, D., Ruley, H. E., Lin, S.-Y., Rabah, D., Kinet, J.-P., & Shin, H.-S. (2010) · Nature Neuroscience · doi:10.1038/nn.2504 · Cited by 651 · see citing works
Lahav, A., Saltzman, E. L., & Schlaug, G. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4822-06.2007 · Cited by 649 · see citing works
Demystifying social cognition: a Hebbian perspective
Keysers, C., & Perrett, D. I. (2004) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2004.09.005 · Cited by 592 · see citing works
Self-citationEmpathy for positive and negative emotions in the gustatory cortex
Jabbi, M., Swart, M., & Keysers, C. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.10.032 · Cited by 590 · see citing works
Self-citationVicarious responses to pain in anterior cingulate cortex: Is empathy a multisensory issue?
Morrison, I., Lloyd, D., Di Pellegrino, G., & Roberts, N. (2004) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/cabn.4.2.270 · Cited by 490 · see citing works
Sex differences in human neonatal social perception
Connellan, J., Baron‐Cohen, S., Wheelwright, S. J., Bátki, A., & Ahluwalia, J. S. (2000) · Infant Behavior and Development · doi:10.1016/s0163-6383(00)00032-1 · Cited by 479 · see citing works
Expanding the mirror: vicarious activity for actions, emotions, and sensations
Keysers, C., & Gazzola, V. (2009) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2009.10.006 · Cited by 472 · see citing works
Self-citationBlanchard, R. J., Blanchard, D. C., Agullana, R., & Weiss, S. M. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90423-l · Cited by 461 · see citing works
Estrous cycle influences the response of female rats in the elevated plus-maze test
Marcondes, F. K., Miguel, K. J., Melo, L. L., & Spadari-Bratfisch, R. C. (2001) · Physiology & Behavior · doi:10.1016/s0031-9384(01)00593-5 · Cited by 449 · see citing works
Frye, C. A., Petralia, S. M., & Rhodes, M. E. (2000) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(00)00392-0 · Cited by 438 · see citing works
Audiovisual mirror neurons and action recognition
Keysers, C., Kohler, E., Umilt�, M. A., Nanetti, L., Fogassi, L., & Gallese, V. (2003) · Experimental Brain Research · doi:10.1007/s00221-003-1603-5 · Cited by 420 · see citing works
Self-citationEvidence for mirror systems in emotions
Bastiaansen, J. A., Thioux, M., & Keysers, C. (2009) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0058 · Cited by 414 · see citing works
Self-citationTowards a unifying neural theory of social cognition
Keysers, C., & Gazzola, V. (2006) · Progress in Brain Research · doi:10.1016/s0079-6123(06)56021-2 · Cited by 367 · see citing works
Self-citationPanksepp, J., & Burgdorf, J. (2000) · Behavioural Brain Research · doi:10.1016/s0166-4328(00)00238-2 · Cited by 362 · see citing works
Jabbi, M., Bastiaansen, J., & Keysers, C. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002939 · Cited by 362 · see citing works
Self-citationMirror Neurons Differentially Encode the Peripersonal and Extrapersonal Space of Monkeys
Caggiano, V., Fogassi, L., Rizzolatti, G., Thier, P., & Casile, A. (2009) · Science · doi:10.1126/science.1166818 · Cited by 361 · see citing works
Aversive Learning Enhances Perceptual and Cortical Discrimination of Indiscriminable Odor Cues
Li, W., Howard, J. D., Parrish, T. B., & Gottfried, J. A. (2008) · Science · doi:10.1126/science.1152837 · Cited by 351 · see citing works
Rozzi, S., Ferrari, P. F., Bonini, L., Rizzolatti, G., & Fogassi, L. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06395.x · Cited by 343 · see citing works
Infant Rodent Ultrasounds ? A Gate to the Understanding of Sound Communication
Ehret, G. (2005) · Behavior Genetics · doi:10.1007/s10519-004-0853-8 · Cited by 325 · see citing works
Sex differences in response to children's toys in nonhuman primates (Cercopithecus aethiops sabaeus)
Alexander, G. M., & Hines, M. (2002) · Evolution and Human Behavior · doi:10.1016/s1090-5138(02)00107-1 · Cited by 291 · see citing works
Emotional reactions of rats to the pain of others.
Church, R. M. (1959) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0043531 · Cited by 285 · see citing works
Stimulus-driven modulation of motor-evoked potentials during observation of others' pain
Avenanti, A., Paluello, I. M., Bufalari, I., & Aglioti, S. M. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2006.03.010 · Cited by 254 · see citing works
Principles of Rat Communication: Quantitative Parameters of Ultrasonic Calls in Rats
Brudzynski, S. M. (2005) · Behavior Genetics · doi:10.1007/s10519-004-0858-3 · Cited by 242 · see citing works
Brudzyński, S. M. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.03.004 · Cited by 229 · see citing works
Social Transmission of Fear in Rats: The Role of 22-kHz Ultrasonic Distress Vocalization
Kim, E. J., Kim, E. S., Covey, E., & Kim, J. J. (2010) · PLoS ONE · doi:10.1371/journal.pone.0015077 · Cited by 216 · see citing works
Grueneberg Ganglion Cells Mediate Alarm Pheromone Detection in Mice
Brechbühl, J., Klaey‐Tassone, M., & Broillet, M.-C. (2008) · Science · doi:10.1126/science.1160770 · Cited by 213 · see citing works
Empathy is moderated by genetic background in mice
Chen, Q., Panksepp, J. B., & Lahvis, G. P. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004387 · Cited by 211 · see citing works
Cheng, Y., Chou, K., Jean Decety, A., Chen, I.-Y., Hung, D. L., Tzeng, O. J. L., & Lin, C. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.10.026 · Cited by 193 · see citing works
Inferior frontal gyrus activity triggers anterior insula response to emotional facial expressions.
Jabbi, M., & Keysers, C. (2008) · Emotion · doi:10.1037/a0014194 · Cited by 190 · see citing works
Self-citationWöhr, M., Borta, A., & Schwarting, R. K. W. (2005) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.07.004 · Cited by 175 · see citing works
Partner's Stress Status Influences Social Buffering Effects in Rats.
Kiyokawa, Y., Kikusui, T., Takeuchi, Y., & Mori, Y. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.4.798 · Cited by 167 · see citing works
Gender Differences in the Mu Rhythm of the Human Mirror-Neuron System
Cheng, Y., Lee, P., Yang, C.-Y., Lin, C., Hung, D. L., & Jean Decety, A. (2008) · PLoS ONE · doi:10.1371/journal.pone.0002113 · Cited by 160 · see citing works
Behavioural responses of laboratory rats to playback of 22 kHz ultrasonic calls
Brudzyński, S. M., & Chiu, E. M. C. (1995) · Physiology & Behavior · doi:10.1016/0031-9384(95)00003-2 · Cited by 159 · see citing works
Social modulation of learning in ratsPreprint
Knapska, E., Mikosz, M., Werka, T., & Maren, S. (2009) · Learning & Memory · doi:10.1101/lm.1670910 · Cited by 158 · see citing works
Hiroi, R., & Neumaier, J. F. (2005) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.07.021 · Cited by 151 · see citing works
Between-subject transfer of emotional information evokes specific pattern of amygdala activation
Knapska, E., Nikolaev, E., Boguszewski, P. M., Walasek, G., Błaszczyk, J. W., Kaczmarek, L., & Werka, T. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511302103 · Cited by 149 · see citing works
Observational Learning and Social Facilitation in the Rat
Zentall, T. R., & Levine, J. M. (1972) · Science · doi:10.1126/science.178.4066.1220 · Cited by 143 · see citing works
Neural Correlates of Competing Fear Behaviors Evoked by an Innately Aversive Stimulus
Mongeau, R., Miller, G. A., Chiang, E., & Anderson, D. J. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-09-03855.2003 · Cited by 142 · see citing works
Fear conditioning by-proxy: Social transmission of fear during memory retrieval
Bruchey, A. K., Jones, C. E., & Monfils, M.-H. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2010.04.047 · Cited by 128 · see citing works
Testing Simulation Theory with Cross-Modal Multivariate Classification of fMRI Data
Etzel, J. A., Gazzola, V., & Keysers, C. (2008) · PLoS ONE · doi:10.1371/journal.pone.0003690 · Cited by 116 · see citing works
Self-citationBreeding for 50-kHz Positive Affective Vocalization in Rats
Burgdorf, J. S., Panksepp, J., Brudzyński, S. M., Kroes, R. A., & Moskal, J. R. (2005) · Behavior Genetics · doi:10.1007/s10519-004-0856-5 · Cited by 115 · see citing works
Sex differences in social interaction in rats: role of the immediate-early gene Zif268
Stack, A., Carrier, N., Dietz, D., Hollis, F., Sorenson, J., & Kabbaj, M. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.163 · Cited by 113 · see citing works
Gender-specific effects of social housing in rats after chronic mild stress exposure
Westenbroek, C. (2003) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/s0278-5846(02)00310-x · Cited by 102 · see citing works
Watanabe, S., & Ono, K. (1986) · Behavioural Processes · doi:10.1016/0376-6357(86)90089-6 · Cited by 90 · see citing works
Westenbroek, C., Snijders, T. A. B., den Boer, J. A., Gerrits, M., Fokkema, D. S., & Horst, G. J. T. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.01.004 · Cited by 76 · see citing works
Social modulation of associative fear learning by pheromone communicationPreprint
Bredy, T. W., & Barad, M. (2008) · Learning & Memory · doi:10.1101/lm.1226009 · Cited by 69 · see citing works
Sex-specific social regulation of inflammatory responses and sickness behaviors
Yee, J. R., & Prendergast, B. J. (2010) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2010.03.006 · Cited by 65 · see citing works
Aversive and attractive marking of toxic and safe foods by Norway rats
Galef, B. G., & Beck, M. (1985) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(85)91645-0 · Cited by 60 · see citing works
Direct and Indirect Behavioral Pathways to the Social Transmission of Food Avoidancea
Galef, B. G. (1985) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1985.tb27074.x · Cited by 59 · see citing works
Social cognition in premotor and parietal cortex
Fujii, N., Hihara, S., & Iriki, A. (2008) · Social Neuroscience · doi:10.1080/17470910701434610 · Cited by 53 · see citing works
Asymmetrical stimulus generalization following differential fear conditioning
Bang, S. J., Allen, T. A., Jones, L. K., Boguszewski, P. M., & Brown, T. H. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.02.009 · Cited by 45 · see citing works
Female fear: Influence of estrus cycle on behavioral response and neuronal activation
Chen, W., Shields, J. A., Huang, W., & King, J. A. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.01.019 · Cited by 42 · see citing works
Single-unit responses to 22kHz ultrasonic vocalizations in rat perirhinal cortex
Allen, T. A., Furtak, S. C., & Brown, T. H. (2007) · Behavioural Brain Research · doi:10.1016/j.bbr.2007.03.009 · Cited by 42 · see citing works
Social Transmission of Avoidance Behavior under Situational Change in Learned and Unlearned Rats
Masuda, A., & Aou, S. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006794 · Cited by 33 · see citing works
Observation and discrimination learning in the rat: Specific and nonspecific effects.
Kohn, B., & Dennis, M. (1972) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0032298 · Cited by 32 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- [57]Langford D 2006 Social modulation of pain as evidence for empathy in mice. Science 312 1967 1970 16809545
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Sorted by citations
Pro-social behavior in rats is modulated by social experience
Ben-Ami Bartal, I., Rodgers, D. A., Bernardez Sarria, M. S., Decety, J., & Mason, P. (2014) · eLife · doi:10.7554/elife.01385 · Cited by 286 · see citing works
Corticoamygdala Transfer of Socially Derived Information Gates Observational Learning
Allsop, 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. (2018) · Cell · doi:10.1016/j.cell.2018.04.004 · Cited by 288 · see citing works
Rats demonstrate helping behavior toward a soaked conspecific
Sato, N., Tan, L., Tate, K., & Okada, M. (2015) · Animal Cognition · doi:10.1007/s10071-015-0872-2 · Cited by 224 · see citing works
Oxytocin enhances observational fear in mice
Pisansky, M. T., Hanson, L. R., Gottesman, I. I., & Gewirtz, J. C. (2017) · Nature Communications · doi:10.1038/s41467-017-02279-5 · Cited by 167 · see citing works
Optogenetic insights on the relationship between anxiety-related behaviors and social deficits
Allsop, S. A., Vander Weele, C. M., Wichmann, R., & Tye, K. M. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00241 · Cited by 150 · see citing works
Ecological validity of social interaction tests in rats and mice
Kondrakiewicz, K., Kostecki, M., Szadzińska, W., & Knapska, E. (2019) · Genes, Brain and Behavior · doi:10.1111/gbb.12525 · Cited by 136 · see citing works
Hippocampal-amygdala memory circuits govern experience-dependent observational fear
Terranova, J. I., Yokose, J., Osanai, H., Marks, W. D., Yamamoto, J., Ogawa, S. K., & Kitamura, T. (2022) · Neuron · doi:10.1016/j.neuron.2022.01.019 · Cited by 117 · see citing works
Behavioral and mechanistic insight into rodent empathy
Sivaselvachandran, S., Acland, E. L., Abdallah, S., & Martin, L. J. (2018) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.06.007 · Cited by 114 · see citing works
The contagion of social defeat stress: Insights from rodent studies
Carnevali, L., Montano, N., Tobaldini, E., Thayer, J. F., & Sgoifo, A. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.01.011 · Cited by 100 · see citing works
Empathic Fear Responses in Mice Are Triggered by Recognition of a Shared Experience
Sanders, J., Mayford, M., & Jeste, D. (2013) · PLoS ONE · doi:10.1371/journal.pone.0074609 · Cited by 90 · see citing works
Silence resulting from the cessation of movement signals danger
Pereira, A. G., Cruz, A., Lima, S. Q., & Moita, M. A. (2012) · Current Biology · doi:10.1016/j.cub.2012.06.015 · Cited by 88 · see citing works
Self-citationDominance status predicts social fear transmission in laboratory rats
Jones, C. E., & Monfils, M.-H. (2016) · Animal Cognition · doi:10.1007/s10071-016-1013-2 · Cited by 81 · see citing works
Linking Social Cognition to Learning and Memory
Leblanc, H., & Ramirez, S. (2020) · The Journal of Neuroscience · doi:10.1523/jneurosci.1280-20.2020 · Cited by 69 · see citing works
When is emotional contagion adaptive?
Nakahashi, W., & Ohtsuki, H. (2015) · Journal of Theoretical Biology · doi:10.1016/j.jtbi.2015.06.014 · Cited by 66 · see citing works
Towards a unified theory of emotional contagion in rodents—A meta-analysis
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Kitano, K., Yamagishi, A., Horie, K., Nishimori, K., & Sato, N. (2022) · iScience · doi:10.1016/j.isci.2022.103991 · Cited by 31 · see citing works
A plea for cross-species social neuroscience
Keysers, C., & Gazzola, V. (2016) · Current topics in behavioral neurosciences · doi:10.1007/7854_2016_439 · Cited by 21 · see citing works
Wardwell, J., Watanasriyakul, W. T., Normann, M. C., Akinbo, O. I., McNeal, N., Ciosek, S., Cox, M., Holzapfel, N., Sujet, S., & Grippo, A. J. (2020) · Stress · doi:10.1080/10253890.2020.1724950 · Cited by 16 · see citing works
- Authors
- Atsak, P., Orre, M., Bakker, P., Cerliani, L., Roozendaal, B., Gazzola, V., Moita, M., & Keysers, C.
- Affiliations
- University Medical Center Groningen (NL)
- Netherlands Institute for Neuroscience (NL)
- Instituto Gulbenkian de Ciência (PT)
- Corresponding author
- Keysers, Christian
- ORCID
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2011-07-13
- Volume
- 6
- Issue
- 7
- Pages
- e21855
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3135600
- OpenAlex
- W2050986015
- Cited by
- 193
- References
- 80
- Citations by year
- 2026: 10 · 2025: 5 · 2024: 18 · 2023: 9 · 2022: 13 · 2021: 17 · 2020: 25 · 2019: 19 · 2018: 26 · 2017: 9 · 2016: 19 · 2015: 14 · 2014: 4 · 2013: 4 · 2012: 1
- FWCI
- 1.46
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion, other-oa)
- KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (acceptedVersion, other-oa)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (acceptedVersion, cc-by)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by)
- Funders
- Ministry of Education, Culture, Sports, Science and Technology
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (452-04-305)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
- Social Sciences › Psychology › Social Psychology › Action Observation and Synchronization
- Keywords
- empathy, affective empathy, rats, ultrasonic vocalizations, social behavior
- MeSH terms
- Animals, Behavior, Animal, Empathy, Fear, Female, Freezing, Humans, Models, Psychological, Social Behavior, Sound Spectrography, Rats, Long-Evans, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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