Empathic Fear Responses in Mice Are Triggered by Recognition of a Shared Experience
Open accessAbstract
Empathy is an important psychological capacity that involves the ability to recognize and share emotions with others. In humans, empathy for others is facilitated by having had a similar prior experience. It increases with the intensity of distress that observers believe is occurring to others, and is associated with acute emotional responses to witnessing others' distress. We sought to develop a relatively simple and fast mouse model of human empathy that resembled these characteristics. We modeled empathy by measuring the freezing of observer mice to observing the footshock of a subject mouse. Observer mice froze to subject footshocks only when they had a similar shock experience 24 hours earlier. Moreover, this freezing increased with the number of footshocks given to the subject and it was accentuated within seconds after footshock delivery. Freezing was not seen in naïve observers or in experienced observers that observed a subject who was spared footshock. Observers did not freeze to a subject's footshock when they had experienced a swim stress 24 hours prior, demonstrating a specific effect for shared experience, as opposed to a generalized stressor in eliciting observer mouse freezing. We propose that this two-day experimental protocol resembles many aspects of human empathy in a mouse model that is amenable to transgenic analysis of neural substrates for empathy and its impairment in certain clinical disorders.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
No statistical methods were used to predetermine sample sizes.
“No statistical methods were used to predetermine sample sizes, although sample sizes were consistent with those from previous studies of this kind7,9,29.”
From Oxytocin enhances observational fear in mice (2017) · cites this paper as [9]
Observer mice did not have experience with foot-shock prior to demonstrator conditioning.
“Observer mice did not have experience with foot-shock (i.e., “priming”) prior to demonstrator conditioning (cf. 7–9).”
From Oxytocin enhances observational fear in mice (2017) · cites this paper as [9]
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 Sanders et al., 2013
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
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
The Neurobiology of Consolidations, Or, How Stable is the Engram?
Dudai, Y. (2004) · Annual Review of Psychology · doi:10.1146/annurev.psych.55.090902.142050 · Cited by 1,671 · see citing works
Empathy and pro-social behavior in rats
Bartal, I. B.-A., Decety, J., & Mason, P. (2011) · Science · doi:10.1126/science.1210789 · Cited by 934 · 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
Localization of a Stable Neural Correlate of Associative Memory
Reijmers, L. G. J. E., Perkins, B. L., Matsuo, N., & Mayford, M. R. (2007) · Science · doi:10.1126/science.1143839 · Cited by 853 · see citing works
Self-citationBlair, J., Colledge, E., Murray, L. K., & Mitchell, D. G. V. (2001) · Research on Child and Adolescent Psychopathology · doi:10.1023/a:1012225108281 · Cited by 713 · 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
Gender differences in brain networks supporting empathy
Schulte-Rüther, M., Markowitsch, H. J., Shah, N. J., Fink, G. R., & Piefke, M. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.04.180 · Cited by 536 · see citing works
Empathy toward strangers triggers oxytocin release and subsequent generosity
Barraza, J. A., & Zak, P. J. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04504.x · Cited by 489 · see citing works
The development of psychopathy
Blair, J., Peschardt, K. S., Budhani, S., Mitchell, D. G. V., & Pine, D. S. (2006) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2006.01596.x · Cited by 486 · see citing works
Golan, O., Ashwin, E., Granader, Y., McClintock, S. W., Day, K. A., Leggett, V., & Baron‐Cohen, S. (2009) · Journal of Autism and Developmental Disorders · doi:10.1007/s10803-009-0862-9 · Cited by 441 · see citing works
Altruism born of suffering: The roots of caring and helping after victimization and other trauma.
Staub, E., & Vollhardt, J. R. (2008) · American Journal of Orthopsychiatry · doi:10.1037/a0014223 · Cited by 433 · see citing works
Are Women More Empathetic than Men? A Longitudinal Study in Adolescence
Mestre, M. V., García, P. S., Navarro, M. D. F., & Porcar, A. M. T. (2009) · The Spanish Journal of Psychology · doi:10.1017/s1138741600001499 · Cited by 391 · see citing works
Psychopathy, aggression, and the processing of emotional stimuli in non‐referred girls and boys
Kimonis, E. R., Frick, P. J., Fazekas, H., & Loney, B. R. (2006) · Behavioral Sciences & the Law · doi:10.1002/bsl.668 · Cited by 286 · 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
Predictors of antisocial personality
Simonoff, E. A., Elander, J., Holmshaw, J., Pickles, A. R., Murray, R. M., & Rutter, M. L. (2004) · The British Journal of Psychiatry · doi:10.1192/bjp.184.2.118 · Cited by 261 · 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
Neurobiology of empathy and callousness: Implications for the development of antisocial behavior
Shirtcliff, E. A., Vitacco, M. J., Graf, A., Gostisha, A. J., Merz, J., & Zahn‐Waxler, C. (2009) · Behavioral Sciences & the Law · doi:10.1002/bsl.862 · Cited by 244 · see citing works
Rodent empathy and affective neuroscience
Panksepp, J. B., & Lahvis, G. P. (2011) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.05.013 · Cited by 224 · see citing works
Danziger, N., Faillenot, I., & Peyron, R. (2009) · Neuron · doi:10.1016/j.neuron.2008.11.023 · Cited by 215 · 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
Carbone, E., & Hey, J. D. (2004) · Cited by 197 · see citing works
Experience modulates vicarious freezing in rats: a model for empathy
Atsak, P., Orre, M., Bakker, P., Cerliani, L., Roozendaal, B., Gazzola, V., Moita, M., & Keysers, C. (2011) · PLoS ONE · doi:10.1371/journal.pone.0021855 · Cited by 193 · see citing works
Habituation and prepulse inhibition of acoustic startle in rodents.
Valsamis, B., & Schmid, S. (2011) · Journal of Visualized Experiments · doi:10.3791/3446 · Cited by 183 · see citing works
The Social neuroscience of empathy
(2009) · Choice Reviews Online · doi:10.5860/choice.47-0576 · Cited by 182 · see citing works
Deafness to fear in boys with psychopathic tendencies
Blair, J., Budhani, S., Colledge, E., & Scott, S. K. (2004) · Journal of Child Psychology and Psychiatry · doi:10.1111/j.1469-7610.2004.00356.x · Cited by 181 · see citing works
Danziger, N. (2006) · Brain · doi:10.1093/brain/awl155 · Cited by 174 · see citing works
Avian maternal response to chick distress
Edgar, J. L., Lowe, J. C., Paul, E. S., & Nicol, C. J. (2011) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2010.2701 · Cited by 172 · see citing works
Can emotion recognition be taught to children with autism spectrum conditions?
Baron‐Cohen, S., Golan, O., & Ashwin, E. (2009) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0191 · Cited by 170 · see citing works
What Is Empathy, and Can Empathy Be Taught?
Davis, C. M. (1990) · Physical Therapy · doi:10.1093/ptj/70.11.707 · Cited by 161 · 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
Maurage, P., Grynberg, D., Noël, X., Joassin, F., Philippot, P., Hanak, C., Verbanck, P., Luminet, O., de Timary, P., & Campanella, S. (2011) · Alcoholism: Clinical and Experimental Research · doi:10.1111/j.1530-0277.2011.01512.x · Cited by 155 · see citing works
The Sight of Others' Pain Modulates Motor Processing in Human Cingulate Cortex
Morrison, I., Peelen, M. V., & Downing, P. E. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhl129 · Cited by 147 · see citing works
Gery, I., Miljkovitch, R., Berthoz, S., & Soussignan, R. (2009) · Psychiatry Research · doi:10.1016/j.psychres.2007.11.006 · Cited by 142 · see citing works
Skin Conductance Response to the Pain of Others Predicts Later Costly Helping
Hein, G., Lamm, C., Brodbeck, C. J., & Singer, T. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022759 · Cited by 133 · see citing works
“I've also experienced loss and fear”: Effects of prior similar experience on empathy
Eklund, J. H., Andersson-Stråberg, T., & Hansen, E. M. (2008) · Scandinavian Journal of Psychology · doi:10.1111/j.1467-9450.2008.00673.x · Cited by 119 · see citing works
Watanabe, S., & Ono, K. (1986) · Behavioural Processes · doi:10.1016/0376-6357(86)90089-6 · Cited by 90 · see citing works
The unique predisposition to criminal violations in frontotemporal dementia.
Mendez, M. F. (2010) · PubMed · Cited by 74 · 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
Prkachin, K. M., Solomon, P. E., Hwang, T., & Mercer, S. R. (2001) · Pain Research and Management · doi:10.1155/2001/108098 · Cited by 67 · see citing works
Empathy for pain: The effects of prior experience and sex
Preis, M. A., & Kröner‐Herwig, B. (2012) · European Journal of Pain · doi:10.1002/j.1532-2149.2012.00119.x · Cited by 65 · see citing works
The surprising empathic abilities of rodents
Mogil, J. S. (2011) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2011.12.012 · Cited by 56 · see citing works
Toward an Animal Model for Antisocial Behavior: Parallels Between Mice and Humans
Sluyter, F., Arseneault, L., Moffitt, T. E., Veenema, A. H., de Boer, S. F., & Koolhaas, J. M. (2003) · Behavior Genetics · doi:10.1023/a:1025730901955 · Cited by 55 · see citing works
A Mouse Model for Observational Fear Learning and the Empathetic Response
Jeon, D., & Shin, H. (2011) · Current Protocols in Neuroscience · doi:10.1002/0471142301.ns0827s57 · Cited by 50 · 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
Empathy and Reversed Empathy of Stress in Mice
Watanabe, S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023357 · Cited by 40 · see citing works
No Evidence for Emotional Empathy in Chickens Observing Familiar Adult Conspecifics
Edgar, J. L., Paul, E. S., Harris, L., Penturn, S., & Nicol, C. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031542 · Cited by 39 · see citing works
Reliability assessment of an automated forced swim test device using two mouse strains
Kürtüncü, M., Luka, L. J., Dimitrijević, N., Uz, T., & Manev, H. (2005) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2005.04.010 · Cited by 35 · see citing works
Anders Breivik, the public, and psychiatry
Wessely, S. C. (2012) · The Lancet · doi:10.1016/s0140-6736(12)60655-2 · Cited by 23 · see citing works
Heldt, S. A. (2009) · Frontiers in Molecular Neuroscience · doi:10.3389/neuro.02.022.2009 · Cited by 18 · see citing works
Insight and empathy in schizophrenia
Didehbani, N., Shad, M. U., Tamminga, C. A., Kandalaft, M. R., Allen, T. T., Chapman, S. B., & Krawczyk, D. C. (2012) · Schizophrenia Research · doi:10.1016/j.schres.2012.09.010 · Cited by 10 · see citing works
Law & Psychiatry: Treatment of Incompetent, Dangerous Criminal Defendants: Parsing the Law
Appelbaum, P. S. (2012) · Psychiatric Services · doi:10.1176/appi.ps.201200630 · Cited by 5 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Empathy: Gender effects in brain and behavior
Christov-Moore, L., Simpson, E. A., Coudé, G., Grigaityte, K., Iacoboni, M., & Ferrari, P. F. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.09.001 · Cited by 1,137 · see citing works
“…emotional and behavioral responses, including sensitivity to conspecifics’ distress, are common in the animal kingdom as well (e.g., monkeys: Nagasaka et al., 2013; pigs: Reimert et al., 2013; rats: Ben-Ami Bartal et al., 2014; mice: Sanders et al., 2013; Mancini et al., 2013; Palagi et al., 2009).”
BackgroundOxytocin-dependent consolation behavior in rodents
Burkett, J. P., Andari, E., Johnson, Z. V., Curry, D. C., de Waal, F. B. M., & Young, L. J. (2016) · Science · doi:10.1126/science.aac4785 · Cited by 692 · 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
“Prior experience with punishments from an imperceptible source may equip animals with the added advantage of not only being able to identify predictive cues, but to also avoid the source of the aversive event (Masuda and Aou, 2009; Mineka and Cook, 1993; Sanders et al., 2013).”
Insular cortex mediates approach and avoidance responses to social affective stimuli
Rogers-Carter, M. M., Varela, J. A., Gribbons, K. B., Pierce, A. F., McGoey, M. T., Ritchey, M., & Christianson, J. P. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0071-y · Cited by 277 · see citing works
“More investigation of the arena and time spent self-grooming was observed in the PN 50 rats (FAGE*BEHAVIOR*TEST(4, 60) = 3.”
BackgroundThe neural and computational systems of social learning
Olsson, A., Knapska, E., & Lindström, B. (2020) · Nature reviews. Neuroscience · doi:10.1038/s41583-020-0276-4 · Cited by 267 · see citing works
“The same effect has been observed in rodents where an animal’s own experiences of shocks enhance 119,128,130 , but are not necessary for 118,131,227 , vicarious threat conditioning to occur.”
BackgroundJeste, D. V., Palmer, B. W., Rettew, D. C., & Boardman, S. (2015) · The Journal of Clinical Psychiatry · doi:10.4088/jcp.14nr09599 · Cited by 246 · see citing works
Self-citationEmotional Mirror Neurons in the Rat’s Anterior Cingulate Cortex
Carrillo, M., Han, Y., Migliorati, F., Liu, M., Gazzola, V., & Keysers, C. (2019) · Current Biology · doi:10.1016/j.cub.2019.03.024 · Cited by 229 · see citing works
The roots of empathy: Through the lens of rodent models
Meyza, K. Z., Bartal, I. B.-A., Monfils, M., Panksepp, J. B., & Knapska, E. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.10.028 · Cited by 167 · see citing works
“Magnitude of vicarious freezing response was modulated by previous experience with shocks (Atsak et al., 2011; Sanders et al., 2013), familiarity (Jeon et al., 2010; Gonzalez-Liencres et al., 2014), genetic background (Chen et al., 2009), and rearing conditions (Yusufishaq and Rosenkranz, 2013;…”
BackgroundOxytocin 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
“048) but not M1 (two-tailed Student’s t-test: t(9)= 0.”
Anxiolytic Treatment Impairs Helping Behavior in Rats
Ben-Ami Bartal, I., Shan, H., Molasky, N. M. R., Murray, T. M., Williams, J. Z., Decety, J., & Mason, P. (2016) · Frontiers in Psychology · doi:10.3389/fpsyg.2016.00850 · Cited by 143 · see citing works
<scp>O</scp>xytocin modulation of neural circuits for social behavior
Marlin, B. J., & Froemke, R. C. (2017) · Developmental Neurobiology · doi:10.1002/dneu.22452 · Cited by 130 · see citing works
“Consolation and other empathy-related behaviors have also been observed in rodents (Church, 1959; Rice and Gainer, 1962; Langford et al., 2006; Chen et al., 2009; Jeon et al., 2010; Kim et al., 2010; Sanders et al., 2013).”
BackgroundEmotional contagion and prosocial behavior in rodents
Keysers, C., Knapska, E., Moita, M. A. P., & Gazzola, V. (2022) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2022.05.005 · Cited by 123 · see citing works
“Footshocks to a demonstrator result in higher levels of freezing in both demonstrator and observer rats than mice [10,15,17,18,45,67] (Figure I), even though the number and intensity of shocks to the demonstrator mice (typically”
Understanding others: Emotion recognition in humans and other animals
Ferretti, V., & Papaleo, F. (2018) · Genes Brain & Behavior · doi:10.1111/gbb.12544 · Cited by 128 · see citing works
“Emotional contagion of fear has also been shown to occur in mice,(123,143,187,188) and to be dependent on several aspects such as genetic background,(141) familiarity,(123,143) social context and status(159,189) and on previous experience of the shock by the observer.(188)”
BackgroundHippocampal-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
“Rodent studies have established behavioral models of OF (Atsak et al., 2011; Chen et al., 2009; Gonzalez-Liencres et al., 2014; Jeon and Shin, 2011; Pereira et al., 2012; Sanders et al., 2013) and identified several neural mechanisms, particularly in the anterior cingulate cortex (ACC) and basolateral amygdala (BLA) n…”
Social Decision-Making and the Brain: A Comparative Perspective
Tremblay, S., Sharika, K. M., & Platt, M. L. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2017.01.007 · Cited by 105 · see citing works
Neural Basis of Observational Fear Learning: A Potential Model of Affective Empathy
Keum, S., & Shin, H.-S. (2019) · Neuron · doi:10.1016/j.neuron.2019.09.013 · Cited by 104 · see citing works
Emotional contagion in nonhuman animals: A review
Pérez‐Manrique, A., & Gomila, A. (2021) · Wiley Interdisciplinary Reviews Cognitive Science · doi:10.1002/wcs.1560 · Cited by 90 · see citing works
Harm to Others Acts as a Negative Reinforcer in Rats
Hernandez-Lallement, J., Attah, A. T., Soyman, E., Pinhal, C. M., Gazzola, V., & Keysers, C. (2020) · Current Biology · doi:10.1016/j.cub.2020.01.017 · Cited by 90 · see citing works
“It has been shown that freezing while observing another animal receive shocks is potentiated by prior shock experience [9, 19, 21, 47], but other arousing experiences, such as a forced swim test, do not have the same potentiating effect [22, 48].”
BackgroundA Missense Variant at the Nrxn3 Locus Enhances Empathy Fear in the Mouse
Keum, S., Kim, A., Shin, J. J., Kim, J., Park, J., & Shin, H. (2018) · Neuron · doi:10.1016/j.neuron.2018.03.041 · Cited by 77 · see citing works
Goumon, S., & Špinka, M. (2016) · Animal Cognition · doi:10.1007/s10071-015-0950-5 · Cited by 75 · 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
“…of prior experience with unconditioned stimuli for an observer to acquire a fear association by observation of a conspecific (Chen et al., 2009; Bruchey et al., 2010; Jeon et al., 2010; E. J. Kim et al., 2010; Atsak et al., 2011; Pereira et al., 2012; Sanders et al., 2013; Allsop et al., 2018).”
BackgroundMethodResultInfluentialRodent models for studying empathy
Keum, S., & Shin, H. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.07.022 · Cited by 67 · see citing works
Observational fear behavior in rodents as a model for empathy
Kim, A., Keum, S., & Shin, H. (2018) · Genes Brain & Behavior · doi:10.1111/gbb.12521 · Cited by 60 · see citing works
“Indeed, observer mice froze more when they had a similar shock experience 24 hours earlier.(33) A recent study also showed that observer mice with prior shock experience showed more robust acquisition of tone-dependent fear response than naïve mice during observational conditioning.”
BackgroundResultBidirectional cingulate-dependent danger information transfer across rats
Han, Y., Bruls, R., Soyman, E., Thomas, R. M., Pentaraki, V., Jelinek, N., Heinemans, M., Bassez, I., Verschooren, S., Pruis, I., et al. (2019) · PLoS Biology · doi:10.1371/journal.pbio.3000524 · Cited by 59 · see citing works
“In mice, results indicate that prior exposure to forced swimming, unlike prior exposure to foot shocks, does not sensitize mice to freeze while witnessing another mice receive foot shocks [14], speaking in favor of a more selective explanation, but whether the same is true in rats remains to be investigated.”
BackgroundParameters That Affect Fear Responses in Rodents and How to Use Them for Management
Bedoya‐Pérez, M. A., Smith, K. L., Kevin, R. C., Luo, J. L., Crowther, M. S., & McGregor, I. S. (2019) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2019.00136 · Cited by 55 · see citing works
Psychopathy to Altruism: Neurobiology of the Selfish–Selfless Spectrum
Sonne, J., & Gash, D. M. (2018) · Frontiers in Psychology · doi:10.3389/fpsyg.2018.00575 · Cited by 61 · see citing works
“These rodents vicariously learn the conditions of the experimental shock more rapidly if they also have experienced the shock for themselves, regardless of whether that shock was experienced within the context of the conditioning experiment or not (Sanders et al., 2013; Lahvis, 2017).”
BackgroundTowards a unified theory of emotional contagion in rodents—A meta-analysis
Hernandez-Lallement, J., Gómez-Sotres, P., & Carrillo, M. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.09.010 · Cited by 53 · see citing works
“In contrast, in mice the effect of pre-exposure is not clear, as some studies that explicitly examined the role of pre-exposure find that it is necessary to pre-expose animals (Sanders et al., 2013), while other studies, in agreement with our results, find that it is not required in mice (Kavaliers et al.”
Zoratto, F., Sbriccoli, M., Martinelli, A., Glennon, J. C., Macrı̀, S., & Giovanni Laviola, A. (2018) · Neuropharmacology · doi:10.1016/j.neuropharm.2018.09.010 · Cited by 51 · see citing works
Similar levels of emotional contagion in male and female rats
Han, Y., Sichterman, B., Carrillo, M., Gazzola, V., & Keysers, C. (2020) · Scientific Reports · doi:10.1038/s41598-020-59680-2 · Cited by 44 · see citing works
“To date the majority of studies investigating sex differences on emotional contagion have been conducted in mice (Chen, Panksepp, & Lahvis, 2009; S. Keum et al., 2016; Langford et al., 2006, 2011, 2010; Pisansky, Hanson, Gottesman, & Gewirtz, 2017; Sanders et al., 2013; Smith, Hostetler, Heinricher, & Ryabinin, 2016).”
BackgroundCruz, A., Heinemans, M., Márquez, C., & Moita, M. A. P. (2019) · Current Biology · doi:10.1016/j.cub.2020.01.025 · Cited by 42 · see citing works
Vicarious Emotions of Fear and Pain in Rodents
Keysers, C., & Gazzola, V. (2023) · Affective Science · doi:10.1007/s42761-023-00198-x · Cited by 37 · see citing works
“Vicarious freezing is also increased in observers that have themselves experienced footshocks in the past (Atsak et al., 2011; Cruz et al., 2020; Han et al., 2019; Sanders et al., 2013).”
BackgroundRepeated Witnessing of Conspecifics in Pain: Effects on Emotional Contagion
Carrillo, M., Migliorati, F., Bruls, R., Han, Y., Heinemans, M., Pruis, I. J., Gazzola, V., & Keysers, C. (2015) · PLoS ONE · doi:10.1371/journal.pone.0136979 · Cited by 37 · see citing works
“Confirming previous findings [9;11;12;16] in the first testing session (i.”
ResultThe differential effects of agency on fear induction using a horror-themed video game
Madsen, K. E. (2016) · Computers in Human Behavior · doi:10.1016/j.chb.2015.11.041 · Cited by 31 · see citing works
Panksepp, J. B., & Lahvis, G. P. (2016) · Behavioral Neuroscience · doi:10.1037/bne0000133 · Cited by 37 · see citing works
“To familiarize observers with a distressful stimulus, they were exposed to a single, unconditioned stimulus (US; 3-s, 1 mA scrambled shock) halfway through this habituation period (see Chen et al., 2009 for rationale; also see Sanders et al., 2013 for empirical support).”
Jeste, D. V., Lee, E. E., Palmer, B. W., & Treichler, E. B. H. (2020) · Psychological Inquiry · doi:10.1080/1047840x.2020.1757984 · Cited by 36 · see citing works
Self-citationHelping behavior in prairie voles: a model of empathy and the importance of oxytocin
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
Luo, W.-J., Li, C.-L., Geng, K.-W., Wang, X., Du, R., Yang, Y., Wei, N., He, T., Wang, Y., Yu, Y., et al. (2020) · Neuroscience Letters · doi:10.1016/j.neulet.2020.134840 · Cited by 29 · see citing works
Ability to share emotions of others as a foundation of social learning
Puścian, A., Bryksa, A., Kondrakiewicz, L., Kostecki, M., Winiarski, M. J., & Knapska, E. (2021) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2021.11.022 · Cited by 26 · see citing works
Zheng, C., Huang, Y., Bo, B., Lei, W. I., Liang, Z., & Wang, Z. (2019) · Neuroscience Bulletin · doi:10.1007/s12264-019-00427-z · Cited by 25 · see citing works
Social Reward and Empathy as Proximal Contributions to Altruism: The Camaraderie Effect
Lahvis, G. P. (2016) · Current topics in behavioral neurosciences · doi:10.1007/7854_2016_449 · Cited by 26 · see citing works
Ventromedial prefrontal neurons represent self-states shaped by vicarious fear in male mice
Huang, Z., Chung, M., Tao, K., Watarai, A., Wang, M., Ito, H., & Okuyama, T. (2023) · Nature Communications · doi:10.1038/s41467-023-39081-5 · Cited by 21 · see citing works
“Previous research has shown that observers with prior foot shock experience respond more to demonstrators ’ fear 65 .”
Towards an animal model of callousness
Hernandez-Lallement, J., van Wingerden, M., & Tobias Kalenscher, A. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.12.029 · Cited by 21 · see citing works
“Such putative emotional contagion of others’ distress seems to depend in part on self-experience with the event eliciting distress (Atsak et al., 2011; Parsana et al., 2012b; Sanders et al., 2013; but see Kavaliers et al., 2001).”
Corbitt‐Hall, D. J., Gauthier, J. M., & Troop‐Gordon, W. (2018) · Suicide and Life-Threatening Behavior · doi:10.1111/sltb.12461 · Cited by 21 · see citing works
Albright, B. B., Dhaher, R., Wang, H., Harb, R., Lee, T.-S. W., Zaveri, H. P., & Eid, T. (2016) · Experimental Neurology · doi:10.1016/j.expneurol.2016.10.007 · Cited by 18 · see citing works
“Some groups, however, have developed transgenic mice that allow for the persistent tagging of activated neurons during a given time window by placing reporter genes under the control of the c-Fos promoter (Collaco and Geusz, 2003; Sanders et al., 2013).”
BackgroundChun, E. K., Donovan, M., Liu, Y., & Wang, Z. (2022) · Neurobiology of Stress · doi:10.1016/j.ynstr.2022.100427 · Cited by 18 · see citing works
Maltese, F., Pacinelli, G., Monai, A., Bernardi, F., Capaz, A. M., Niello, M., Walle, R., de León-Reyes, N. S., Managò, F., Leroy, F., et al. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01816-y · Cited by 16 · see citing works
“Empathic responses toward conspecifics in distress can only be triggered by the same stressful experience 3,31 .”
Neurobehavioral and inflammatory responses following traumatic brain injury in male and female mice
Bahader, G. A., Naghavi, F., Alotaibi, A., Dehghan, A., Swain, C. C., Burkett, J. P., & Shah, Z. A. (2023) · Behavioural Brain Research · doi:10.1016/j.bbr.2023.114711 · Cited by 15 · see citing works
Nakatake, Y., Furuie, H., Ukezono, M. M., Yamada, M., Yoshizawa, K., & Yamada, M. (2020) · Scientific Reports · doi:10.1038/s41598-020-73988-z · Cited by 15 · see citing works
Current rodent models for the study of empathic processes
Cox, S. S., & Reichel, C. M. (2020) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000590 · Cited by 15 · see citing works
“In one study, a similar protocol showed that observing a conspecific was not enough to generate vicarious freezing (Sanders et al., 2013).”
BackgroundDinçkol, Ö., Wenger, N. H., Zachry, J. E., & Kutlu, M. G. (2023) · Scientific Reports · doi:10.1038/s41598-023-49686-x · Cited by 12 · see citing works
“A number of studies have shown that aversive information such as fear can be learned through observation and a prior experience of the same aversive event enhances the acquisition of fear learning 18,46,47 .”
Keter, D. L., Esteves, J. E., Loghmani, M. T., Rossettini, G., & Cook, C. E. (2025) · International journal of osteopathic medicine · doi:10.1016/j.ijosm.2025.100750 · Cited by 14 · see citing works
Socially Transferred Stress Experience Modulates Social Affective Behaviors in Rats
Toyoshima, M., Okuda, E., Hasegawa, N., Kaseda, K., & Yamada, K. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.08.022 · Cited by 14 · see citing works
Rodent Models of Autism, Epigenetics, and the Inescapable Problem of Animal Constraint
Lahvis, G. P. (2016) · Springer eBooks · doi:10.1007/978-1-4939-3777-6_9 · Cited by 12 · see citing works
Harvie, H., Rodrigo, A., Briggs, C., Thiessen, S., & Kelly, D. M. (2021) · Animal Cognition · doi:10.1007/s10071-020-01460-6 · Cited by 11 · see citing works
Langford, D. J., & Williams, A. C. D. C. (2014) · Pain · doi:10.1016/j.pain.2014.03.026 · Cited by 11 · see citing works
The lateralized LC-NAergic system distinguishes vicarious versus direct fear in mice
Kim, J., Choi, D.-E., & Shin, H. (2025) · Nature Communications · doi:10.1038/s41467-025-57701-0 · Cited by 8 · see citing works
Prior stress experience modulates social preference for stressed conspecifics in male rats
Toyoshima, M., Mitsui, K., & Yamada, K. (2021) · Neuroscience Letters · doi:10.1016/j.neulet.2021.136253 · Cited by 9 · see citing works
Kaźmierowska, A. M., Szczepanik, M., Wypych, M., Droździel, D., Marchewka, A., Michałowski, J. M., Olsson, A., & Knapska, E. (2022) · NeuroImage · doi:10.1016/j.neuroimage.2022.119648 · Cited by 8 · see citing works
ARNT2 controls prefrontal somatostatin interneurons mediating affective empathy
Choi, J., Jung, S., Kim, J., So, D., Kim, A., Kim, S., Choi, S., Yoo, E., Kim, J. Y., Jang, Y. C., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114659 · Cited by 8 · see citing works
Treatment Approaches in Rodent Models for Autism Spectrum Disorder
Pietropaolo, S., Crusio, W. E., & D'Amato, F. R. (2015) · Current topics in behavioral neurosciences · doi:10.1007/7854_2015_433 · Cited by 8 · see citing works
Social Transfer of Fear in Rodents
Kondrakiewicz, K., Rokosz, K., Nikolaev, T., Górkiewicz, T., Danielewski, K., Gruszczyńska, A., Meyza, K. Z., & Knapska, E. (2019) · Current Protocols in Neuroscience · doi:10.1002/cpns.85 · Cited by 8 · see citing works
Evaluating Social Support-Like Phenomena in an Animal Model of Posttraumatic Stress Disorder (PTSD)
Thoeringer, C. K. (2014) · Journal of Depression & Anxiety · doi:10.4172/2167-1044.1000143 · Cited by 7 · see citing works
“Because of the ecological characteristics of mice with a single male dominating the cohort and a large territory [52], future experiments should deal with the cohabitation of male and female animals to provide a more natural situation of social support.”
BackgroundWhy help others? Insights from rodent to human early childhood research
Chen, Y., Han, S., & Yin, B. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2023.1058352 · Cited by 6 · see citing works
A novel animal model for understanding secondary traumatic stress and visceral pain in male rats
Lannon, A. S., Brocka, M., Collins, J. M., Fitzgerald, P., O’Mahony, S. M., Cryan, J. F., & Moloney, R. D. (2024) · European Journal of Neuroscience · doi:10.1111/ejn.16353 · Cited by 6 · see citing works
“Several prior studies have shown that observation of the experience of pain induced empathetic response and behavioural changes (Baptista-de-Souza et al., 2015; Mohammadi et al., 2020; Sanders et al., 2013).”
BackgroundSociability versus empathy in adolescent mice: Different or distinctive?
Panksepp, J. B., & Lahvis, G. P. (2023) · Learning and Motivation · doi:10.1016/j.lmot.2023.101892 · Cited by 6 · see citing works
A Model to guide force-based manipulation research and practice
Loghmani, M. T., Keter, D. L., Bove, G. M., Winkelstein, B. A., Bulea, T. C., Olausson, H., Pathak, M. N., Powell, R., & Cook, C. E. (2025) · PLoS ONE · doi:10.1371/journal.pone.0331606 · Cited by 5 · see citing works
Fadaei-kenarsary, M., Farbood, Y., Mansouri, S. M. T., & Moghaddam, H. F. (2015) · Europe PMC (PubMed Central) · Cited by 5 · see citing works
The Fragrant Power of Collective Fear
Harb, R., & Taulor, J. R. (2015) · PLoS ONE · doi:10.1371/journal.pone.0123908 · Cited by 5 · see citing works
Empathy and prosocial behavior powered by orexin-driven theta oscillations
Kim, J. G., Cron, G. O., Kim, M., Hossain, A., & Lee, J. H. (2026) · Science · doi:10.1126/science.aea7140 · Cited by 3 · see citing works
Ruble, S., Kramer, C., West, L., Durrett, H., & Diehl, M. M. (2026) · Scientific Reports · doi:10.1038/s41598-026-50571-6 · Cited by 3 · see citing works
北村, 貴., Ramesh, K., & Terranova, J. I. (2024) · Advances in neurobiology · doi:10.1007/978-3-031-62983-9_12 · Cited by 4 · see citing works
The neural basis of affective empathy: What is known from rodents
Peng, S., Li, M., Yang, X., & Xie, W. (2025) · Neuropharmacology · doi:10.1016/j.neuropharm.2025.110347 · Cited by 3 · see citing works
Li, J., Qin, Y., Zhong, Z., Meng, L., Huang, L., & Li, B. (2024) · Cerebral Cortex · doi:10.1093/cercor/bhae207 · Cited by 2 · see citing works
Cingulate dependent social risk assessment in ratsPreprint
Han, Y., Bruls, R., Thomas, R. M., Pentaraki, V., Jelinek, N., Heinemans, M., Bassez, I., Verschooren, S., Pruis, I., Lierde, T. V., et al. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/452169 · Cited by 2 · see citing works
Emotional “Contagion” in Piglets after Sensory Avoidance of Rewarding and Punishing Treatment
Zhang, Y. Z., Yang, X., Sun, F., Zhang, Y., Yao, Y., Bai, Z., Yu, J., Liu, X., Zhao, Q., Li, X., et al. (2024) · Animals · doi:10.3390/ani14071110 · Cited by 1 · see citing works
“Piglets could also perceive the emotional information from their peers, and their emotional state was affected by their groupmates.”
BackgroundApoE Isoform-Dependent Effects on Extinction of Contextual Fear Memory and Passive Avoidance Memory
Saltonstall, E., Pederson, A., O’Niel, A., Holden, S. J., Kessler, K., Torres, E. R. S., & Raber, J. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26125820 · Cited by 1 · see citing works
Modern assays for assessing pain and related nociceptive and defensive actions in rodent models
Arakawa, H. (2025) · Behavioural Brain Research · doi:10.1016/j.bbr.2025.115854 · Cited by 1 · see citing works
“Moreover, the adaptive effects of social factors have been reported; mice demonstrate the ability to modify their response to pain in the presence of a human observer [80,93] or in the presence or influence of conspecifics [68, 111].”
Pabón, D. G., Hatfield-King, J., Patel, S., Horn, B., Burkett, J. P., & Andari, E. (2026) · Molecular Autism · doi:10.1186/s13229-026-00712-5 · Cited by 1 · see citing works
Beyond Fear Learning in Isolation: Integration of Social Dimensions into Aversive Learning
Diehl, M. M. (2026) · Current Protocols · doi:10.1002/cpz1.70424
“…pre-exposure, typically a single footshock given before the observation session, is necessary for the observer to understand the ongoing experience of the demonstrator; otherwise, observational learning may not occur (Allsop et al., 2018; Atsak et al., 2011; Kim et al., 2010; Sanders et al., 2013).”
Challenging Convention in Empathy Research: Developing a Mouse Model and Initial Neural Analyses
Panksepp, J. B., & Lahvis, G. P. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-805397-3.00013-9 · Cited by 1 · see citing works
Scientific Autobiography of a Professional Student and a Lifelong Learner
Jeste, D. V. (2018) · American Journal of Geriatric Psychiatry · doi:10.1016/j.jagp.2018.08.004 · Cited by 1 · see citing works
“To study a component of wisdom in animals, we studied a mouse model of empathy.(14) I feel that we will witness even more exciting wisdom research in the next decade.”
BackgroundSelf-citationOxytocin and epigenetic mechanisms in mouse models of empathy and autism
Pisansky, M. T. (2016) · University of Minnesota Digital Conservancy (University of Minnesota)
Auditory Cues in Social Transmission of Fear
Pereira, A. I. P. G. (2015) · Portuguese National Funding Agency for Science, Research and Technology (RCAAP Project by FCT)
Meyza, K. Z. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-805397-3.00014-0
Emotional Mirrors in the Rat's Anterior Cingulate CortexPreprint
Carrillo, M., Han, Y., Migliorati, F., Liu, M., Gazzola, V., & Keysers, C. (2018) · SSRN Electronic Journal · doi:10.2139/ssrn.3299451
Program Verification and Programming Methodology.
Leino, K. R. M. (2005)
Miczek, K. A., & Covington, H. E. (2019) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.733162596.793561606
Lahvis, G. P. (2018) · Springer eBooks · doi:10.1007/978-3-319-47829-6_1574-1
Lahvis, G. P. (2022) · Springer eBooks · doi:10.1007/978-3-319-55065-7_1574
Vicarious Stress in Juvenile Rats
Ali, E. (2022) · doi:10.22215/etd/2022-15177
- Authors
- Sanders, J., Mayford, M., & Jeste, D.
- Affiliations
- University of California San Diego (US)
- Scripps Research Institute (US)
- Corresponding author
- Sanders, Jeff
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2013-09-18
- Volume
- 8
- Issue
- 9
- Pages
- e74609
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3776853
- OpenAlex
- W2082598606
- Cited by
- 90
- References
- 52
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 6 · 2023: 6 · 2022: 7 · 2021: 5 · 2020: 9 · 2019: 8 · 2018: 14 · 2017: 2 · 2016: 12 · 2015: 7 · 2014: 3
- FWCI
- 4.01
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institutes of Health
- National Institute of Mental Health (MH057368, R01MH057368, T32MH019934)
- National Institute on Drug Abuse (R01DA028300, DA028300)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Social Sciences › Psychology › Social Psychology › Action Observation and Synchronization
- Keywords
- empathy, fear response, collective experience, footshock, emotional contagion, swim stress
- MeSH terms
- Animals, Electroshock, Empathy, Extremities, Fear, Female, Humans, Male, Mice, Inbred C57BL, Recognition, Psychology, Freezing Reaction, Cataleptic, Mice
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.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review