Abstract
Rationale
Empathy, or the ability to perceive, share, and act upon the emotions of another, is a crucial social skill and is dysfunctional in autism and schizophrenia. While the complexities of human empathy are difficult to model in rodents, behavioral paradigms utilizing rats which study decision-making in social contexts may provide a translational framework for assessing biological, pharmacotherapeutic, and environmental interventions.
Objectives
Modify and expand upon the three-session rat harm aversion task, which measures the willingness of rats to cease pressing a lever that earns them sucrose reward but delivers a shock to their cage mate. We sought to test the sustainability of harm aversion across seven sessions in male and female rats.
Methods
Same-sex pair-housed rats were assigned as either the observer, which had access to the lever, or the demonstrator, which would receive shocks. After training the observer to press the lever to receive sucrose pellets, the demonstrator was placed into an adjacent chamber at which point lever responses would also deliver a shock. If the observer did not press the lever, no shock and no sucrose was delivered.
Results
A sex difference in harm aversion was observed with female rats having significantly higher response rates and decreased response latencies across the seven test sessions, thus delivering more shocks and obtaining more sucrose, relative to males.
Conclusions
These data demonstrate that male rats sustain harm aversion to a greater extent relative to females.
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Abbreviations
- HAT:
-
Harm aversion task
- ACC:
-
Anterior cingulate cortex
- ITI:
-
Inter-trial interval
- RT:
-
Re-test
- BL:
-
Baseline
- RDT:
-
Risky decision-making task
References
Baron-Cohen S, Wheelwright S (2004) The empathy quotient: an investigation of adults with Asperger syndrome or high functioning autism, and normal sex differences. J Autism Dev Disord 34:163–175
Baumrind D (1964) Some thoughts on ethics of research: after reading Milgram's "Behavioral Study of Obedience". Am Psychol 19:421–423
Bonfils KA, Lysaker PH, Minor KS, Salyers MP (2016) Affective empathy in schizophrenia: a meta-analysis. Schizophr Res 175:109–117
Caspar EA (2021) A novel experimental approach to study disobedience to authority. Sci Rep 11:22927
De Gregorio D, Aguilar-Valles A, Preller KH, Heifets BD, Hibicke M, Mitchell J, Gobbi G (2021) Hallucinogens in mental health: preclinical and clinical studies on LSD, Psilocybin, MDMA, and Ketamine. J Neurosci 41:891–900
Fehr E, Fischbacher U (2003) The nature of human altruism. Nature 425:785–791
Gonzalez-Franco M, Slater M, Birney ME, Swapp D, Haslam SA, Reicher SD (2018) Participant concerns for the learner in a virtual reality replication of the Milgram obedience study. PloS One 13:e0209704
Greene JT (1969) Altruistic behavior in the albino rat. Psychonomic Science 14:47–48
Han Y, Sichterman B, Carrillo M, Gazzola V, Keysers C (2020) Similar levels of emotional contagion in male and female rats. Sci Rep 10:2763
Healey ML, Grossman M (2018) Cognitive and affective perspective-taking: evidence for shared and dissociable anatomical substrates. Front Neurol 9:491
Henry JD, Bailey PE, Rendell PG (2008) Empathy, social functioning and schizotypy. Psychiatry Res 160:15–22
Hernandez-Lallement J, Attah AT, Soyman E, Pinhal CM, Gazzola V, Keysers C (2020) Harm to others acts as a negative reinforcer in rats. Curr Biol 30:949–961.e7
Ku KM, Weir RK, Silverman JL, Berman RF, Bauman MD (2016) Behavioral phenotyping of juvenile Long-Evans and Sprague-Dawley Rats: implications for preclinical models of autism spectrum disorders. PloS One 11:e0158150
Lockwood PL (2016) The anatomy of empathy: vicarious experience and disorders of social cognition. Behav Brain Res 311:255–266
Marcondes FK, Bianchi FJ, Tanno AP (2002) Determination of the estrous cycle phases of rats: some helpful considerations. Brazilian Journal of Biology = Revista brasleira de biologia 62:609–614
Meyza KZ, Bartal IB, Monfils MH, Panksepp JB, Knapska E (2017) The roots of empathy: through the lens of rodent models. Neurosci Biobehav Rev 76:216–234
Milgram S (1963) Behavioral study of obedience. J Abnorm Psychol 67:371–378
Nadler A, Camerer CF, Zava DT, Ortiz TL, Watson NV, Carré JM, Nave G (2019) Does testosterone impair men's cognitive empathy? Evidence from two large-scale randomized controlled trials. Proc Biol Sci 286:20191062
Nestler EJ, Hyman SE (2010) Animal models of neuropsychiatric disorders. Nat Neurosci 13:1161–1169
Neyret S, Navarro X, Beacco A, Oliva R, Bourdin P, Valenzuela J, Barberia I, Slater M (2020) An embodied perspective as a victim of sexual harassment in virtual reality reduces action conformity in a later milgram obedience scenario. Sci Rep 10:6207
Orsini CA, Blaes SL, Hernandez CM, Betzhold SM, Perera H, Wheeler AR, Ten Eyck TW, Garman TS, Bizon JL, Setlow B (2021) Regulation of risky decision making by gonadal hormones in males and females. Neuropsychopharmacology 46:603–613
Orsini CA, Willis ML, Gilbert RJ, Bizon JL, Setlow B (2016) Sex differences in a rat model of risky decision making. Behav Neurosci 130:50–61
Panksepp J, Panksepp JB (2013) Toward a cross-species understanding of empathy. Trends Neurosci 36:489–496
Puiu AA, Votinov M, Habel U, Konrad K (2022) Testosterone administration does not alter the brain activity supporting cognitive and affective empathy. Comprehensive Psychoneuroendocrinology 10:100134
Rodrigues AMM, Gardner A (2022) Reproductive value and the evolution of altruism. Trends Ecol Evol 37:346–358
Shirayama Y, Matsumoto K, Hamatani S, Muneoka K, Okada A, Sato K (2022) Associations among autistic traits, cognitive and affective empathy, and personality traits in adults with autism spectrum disorder and no intellectual disability. Sci Rep 12:3125
Simon NW, Gilbert RJ, Mayse JD, Bizon JL, Setlow B (2009) Balancing risk and reward: a rat model of risky decision making. Neuropsychopharmacology 34:2208–2217
Slater M, Antley A, Davison A, Swapp D, Guger C, Barker C, Pistrang N, Sanchez-Vives MV (2006) A virtual reprise of the Stanley Milgram obedience experiments. PloS One 1:e39
Acknowledgements
The authors thank the support by NIH grants T32-MH067533 through the Maryland Psychiatric Research Center (to EMH); R01-MH107615 (to TDG); and the U.S. Department of Veterans Affairs Merit Awards 101BX004062, 101BX003631, and 101BX006018 (to TDG). The authors thank Dr. Stephen Wolf from the University of Maryland School of Medicine Department of Pharmacology for assistance with fabricating the plexiglass divider used in the operant chambers. The authors also thank the anonymous reviewers for their helpful comments.
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Hess, E.M., Venniro, M. & Gould, T.D. Relative to females, male rats are more willing to forego obtaining sucrose reward in order to prevent harm to their cage mate. Psychopharmacology (2023). https://doi.org/10.1007/s00213-023-06435-2
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DOI: https://doi.org/10.1007/s00213-023-06435-2