Physiological and behavioral responses to observing a sibling experience a direct stressor in prairie voles
Open accessAbstract
Uncontrollable stress precipitates negative mental and physical health outcomes. Furthermore, the vicarious experience of stress (e.g. observing another individual experience a direct stressor) can mimic the effects of directly experiencing the stressor. The current experiment examined the behavioral and physiological effects of the vicarious experience of stress using the socially monogamous prairie vole. Male prairie voles were exposed to either an empty open field chamber, or a chamber in which the animal observed a sibling undergoing a concurrent direct physical stressor (tail suspension test) for five minutes. Exploratory and anxiety-like behaviors were recorded in all observers during the test session. Cardiac indices of heart rate and heart rate variability were recorded in a subset of observers prior to, during, and following the test session. Corticosterone levels were measured in all observers and siblings following the test session. When compared to animals exposed to an empty open field chamber, animals that observed a sibling undergo a direct physical stressor exhibited increased heart rate and circulating corticosterone, and decreased heart rate variability. These physiological stress indicators were supported by behavioral changes, including increased freezing followed immediately by orienting of the head toward the center of the apparatus, and decreased locomotion, grooming, and rearing. These preliminary results suggest that prairie voles experience stress vicariously, and provide a foundation for additional studies focused on the underlying mechanisms of vicarious stress. The use of this model may inform our understanding of the social transmission of stress among social species, including humans.LAY SUMMARYThe experience of stress, including observing stress in a loved one, has negative consequences on mental and physical health. This study used a social rodent (prairie voles) to demonstrate that stress transfers among social individuals, consequently producing an increased physiological and behavioral stress response in prairie voles observing their siblings experience stress. This research informs our understanding of the interactions of social experiences and stress in humans.
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Previous studies suggest that prairie voles show empathy-like behavior, such as freezing caused by emotional contagion of conspecifics' fear, and consolation.
“Previous studies suggest that prairie voles show empathy-like behavior, such as freezing caused by emotional contagion of conspecifics' fear, and consolation (Burkett et al., 2016; Stetzik et al., 2018; Wardwell et al., 2020).”
From Helping behavior in prairie voles: a model of empathy and the importance of oxytocin (2022) · cites this paper as Wardwell et al., 2020
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Cites
Diagnostic and Statistical Manual of Mental Disorders
American Psychiatric Association (2013) · doi:10.1176/appi.books.9780890425596 · Cited by 116,369 · see citing works
Diagnostic and Statistical Manual of Mental Disorders, 5th ed.
Carter, M. J. (2014) · Therapeutic Recreation Journal · Cited by 15,154 · see citing works
An overview of heart rate variability metrics and norms
Shaffer, F., & Ginsberg, J. P. (2017) · Frontiers in Public Health · doi:10.3389/fpubh.2017.00258 · Cited by 7,185 · 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
Does Rejection Hurt? An fMRI Study of Social Exclusion
Eisenberger, N. I., Lieberman, M. D., & Williams, K. D. (2003) · Science · doi:10.1126/science.1089134 · Cited by 3,849 · see citing works
Review of personality and social psychology
Davies, M. (1983) · Personality and Individual Differences · doi:10.1016/0191-8869(83)90072-7 · Cited by 3,393 · see citing works
The open-field test: A critical review.
WALSH, R. N., & Cummins, R. A. (1976) · Psychological Bulletin · doi:10.1037/0033-2909.83.3.482 · Cited by 2,389 · see citing works
Stress-induced immune dysfunction: implications for health
Glaser, R., & Kiecolt-Glaser, J. K. (2005) · Nature Reviews Immunology · doi:10.1038/nri1571 · Cited by 2,190 · see citing works
Thayer, J. F., & Lane, R. D. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.08.004 · Cited by 2,040 · see citing works
McEwen, B. S. (2008) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.11.071 · Cited by 1,864 · see citing works
Cryan, J. F., Mombereau, C., & Vassout, A. (2005) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2005.03.009 · Cited by 1,674 · see citing works
Use of the Open Field Maze to Measure Locomotor and Anxiety-like Behavior in Mice
Seibenhener, M. L., & Wooten, M. C. (2015) · Journal of Visualized Experiments · doi:10.3791/52434 · Cited by 1,467 · 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
Choleris, E. (2001) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(01)00011-2 · Cited by 761 · see citing works
Hostinar, C. E., Sullivan, R. M., & Gunnar, M. R. (2014) · Psychological Bulletin · doi:10.1037/a0032671 · Cited by 739 · see citing works
Carola, V., D'Olimpio, F., Brunamonti, E., Mangia, F., & Renzi, P. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00452-1 · Cited by 735 · see citing works
Oxytocin-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
Gould, T. D., Dao, D. T., & Kovacsics, C. E. (2009) · Neuromethods · doi:10.1007/978-1-60761-303-9_1 · Cited by 509 · see citing works
Loneliness in the Modern Age: An Evolutionary Theory of Loneliness (ETL)
Cacioppo, J. T., & Cacioppo, S. (2018) · Advances in Experimental Social Psychology · doi:10.1016/bs.aesp.2018.03.003 · Cited by 481 · see citing works
Social buffering of the stress response: diversity, mechanisms, and functions
Hennessy, M. B., Kaiser, S., & Sachser, N. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.06.001 · Cited by 477 · see citing works
Cortical 5-HT 2A Receptor Signaling Modulates Anxiety-Like Behaviors in Mice
Weisstaub, N., Zhou, M., Lira, A., Lambe, E. K., González‐Maeso, J., Hornung, J., Sibille, E. L., Underwood, M. D., Itohara, S., Dauer, W. T., et al. (2006) · Science · doi:10.1126/science.1123432 · Cited by 425 · see citing works
The neurobiology of pair bonding: Insights from a socially monogamous rodent
Young, K. A., Gobrogge, K. L., Liu, Y., & Wang, Z. (2011) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.07.006 · Cited by 389 · see citing works
Hypothalamic Oxytocin Mediates Social Buffering of the Stress Response
Smith, A. S., & Wang, Z. (2014) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.09.017 · Cited by 359 · see citing works
LEVENSON, R. W. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1280.016 · Cited by 335 · see citing works
Carter, C. S., & Getz, L. L. (1993) · Scientific American · doi:10.1038/scientificamerican0693-100 · Cited by 310 · see citing works
Meyer, M. L., Masten, C. L., Ma, Y., Wang, C., Shi, Z., Eisenberger, N. I., & Han, S. (2012) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nss019 · Cited by 277 · see citing works
Bosch, O. J., Nair, H. P., Ahern, T. H., Neumann, I. D., & Young, L. J. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2008.154 · Cited by 216 · see citing works
Vicarious Social Defeat Stress Induces Depression-Related Outcomes in Female Mice
Iñiguez, S. D., Flores‐Ramirez, F. J., Riggs, L. M., Alipio, J. B., Garcia-Carachure, I., Hernandez, M. A., Sánchez, D. O. M., Lobo, M. K., Serrano, P. A., Braren, S. H., et al. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.07.014 · Cited by 206 · 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
Grippo, A. J., Lamb, D. G., Carter, C. S., & Porges, S. W. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.04.011 · Cited by 188 · see citing works
Self-citationSocial transmission and buffering of synaptic changes after stress
Sterley, T.-L., Baimoukhametova, D., Füzesi, T., Zurek, A. A., Daviu, N., Rasiah, N. P., Rosenegger, D., & Bains, J. S. (2018) · Nature Neuroscience · doi:10.1038/s41593-017-0044-6 · Cited by 179 · 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
Cortisol increase in empathic stress is modulated by emotional closeness and observation modality
Engert, V., Plessow, F., Miller, R. E., Kirschbaum, C., & Singer, T. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.04.005 · Cited by 159 · see citing works
Sun, P., Smith, A. S., Lei, K., Liu, Y., & Wang, Z. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.02.016 · Cited by 141 · see citing works
McNeal, N., Scotti, M.-A. L., Wardwell, J., Chandler, D. L., Bates, S. L., LaRocca, M., Trahanas, D. M., & Grippo, A. J. (2014) · Autonomic Neuroscience · doi:10.1016/j.autneu.2013.10.001 · Cited by 135 · see citing works
Self-citationVicarious social defeat stress: Bridging the gap between physical and emotional stress
Sial, O. K., Warren, B. L., Parise, L. F., Parise, E. M., & Bolaños‐Guzmán, C. A. (2015) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2015.10.012 · Cited by 134 · 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
Finnell, J. E., Lombard, C. M., Padi, A. R., Moffitt, C. M., Wilson, L. B., Wood, C. S., & Wood, S. K. (2017) · PLoS ONE · doi:10.1371/journal.pone.0172868 · Cited by 114 · see citing works
Borta, A., & Schwarting, R. K. W. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.01.009 · Cited by 93 · see citing works
Embodied stress: The physiological resonance of psychosocial stress
Engert, V., Linz, R., & Grant, J. A. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.12.221 · Cited by 89 · see citing works
Grippo, A. J., Ihm, E., Wardwell, J., McNeal, N., Scotti, M. L., Moenk, D. A., Chandler, D. L., LaRocca, M. A., & Preihs, K. (2014) · Psychosomatic Medicine · doi:10.1097/psy.0000000000000052 · Cited by 78 · see citing works
Self-citationAutonomic Changes Associated with Enhanced Anxiety in 5-HT1A Receptor Knockout Mice
Pattij, T. (2002) · Neuropsychopharmacology · doi:10.1016/s0893-133x(02)00317-2 · Cited by 78 · see citing works
Bailey, M. T., Avitsur, R., Engler, H., Padgett, D. A., & Sheridan, J. F. (2003) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2003.09.012 · Cited by 74 · see citing works
Cardiac regulation in the socially monogamous prairie vole
Grippo, A. J., Lamb, D. G., Carter, C. S., & Porges, S. W. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.09.037 · Cited by 62 · see citing works
Self-citationKavaliers, M., Colwell, D. D., & Choleris, E. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(02)00021-1 · Cited by 60 · see citing works
Olazábal, D. E., & Young, L. J. (2005) · Developmental Psychobiology · doi:10.1002/dev.20077 · Cited by 58 · see citing works
Social stress contagion in rats: Behavioural, autonomic and neuroendocrine correlates
Carnevali, L., Montano, N., Statello, R., Coudé, G., Vacondio, F., Rivara, S., Ferrari, P. F., & Sgoifo, A. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.05.017 · Cited by 52 · see citing works
McNeal, N., Appleton, K. M., Johnson, A. K., Scotti, M. L., Wardwell, J., Murphy, R., Bishop, C., Knecht, A., & Grippo, A. J. (2017) · Stress · doi:10.1080/10253890.2017.1295444 · Cited by 39 · see citing works
Self-citationWallace, D. G., Martin, M. M., & Winter, S. S. (2008) · Die Naturwissenschaften · doi:10.1007/s00114-008-0410-z · Cited by 34 · see citing works
Grippo, A. J., Scotti, M. L., Wardwell, J., McNeal, N., Bates, S. L., Chandler, D. L., Ihm, E., & Jadia, N. (2018) · Autonomic Neuroscience · doi:10.1016/j.autneu.2018.08.002 · Cited by 9 · see citing works
Self-citationMcNeal, N., Watanasriyakul, W. T., Normann, M. C., Akinbo, O. I., Dagner, A., Ihm, E., Wardwell, J., & Grippo, A. J. (2019) · Autonomic Neuroscience · doi:10.1016/j.autneu.2019.03.003 · Cited by 8 · see citing works
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Helping 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
- Authors
- Wardwell, J., Watanasriyakul, W. T., Normann, M. C., Akinbo, O. I., McNeal, N., Ciosek, S., Cox, M., Holzapfel, N., Sujet, S., & Grippo, A. J.
- Affiliations
- Northern Illinois University (US)
- Corresponding author
- Grippo, Angela J.
- Venue
- Stress
- Publisher
- Informa UK Limited
- Published
- 2020-02-17
- Volume
- 23
- Issue
- 4
- Pages
- 444-456
- ISSN
- 1025-3890 (ISSN-L)
- 1607-8888
- PMC
- PMC7335336
- OpenAlex
- W3005278474
- Cited by
- 16
- References
- 51
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 2 · 2023: 2 · 2022: 2 · 2021: 4 · 2020: 3
- FWCI
- 1.59
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Stress (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health
- National Heart, Lung, and Blood Institute (R15HL147179, R15HL112350)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
- Keywords
- Microtus ochrogaster, tail suspension test, heart rate, heart rate variability, corticosterone, anxiety-like behavior, freezing behavior, social monogamy, social stress
- MeSH terms
- Animals, Arvicolinae, Humans, Male, Social Isolation, Stress, Psychological, Siblings, Grassland
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