Physiological and behavioral responses to observing a sibling experience a direct stressor in prairie voles

References

• American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders (5th ed.). Arlington, VA: American Psychiatric Association.
   Google Scholar
• American Psychological Association. (2017). Stress in America: The state of our nation. Retrieved from www.stressinamerica.org
   Google Scholar
• Atsak, P., Orre, M., Bakker, P., Cerliani, L., Roozendaal, B., Gazzola, V., … Keysers, C. (2011). Experience modulates vicarious freezing in rats: A model for empathy. PLoS One, 6, e21885. doi:10.1371/journal.pone.0021855
   PubMed Web of Science ®Google Scholar
• Bailey, M.T., Avitsur, R., Engler, H., Padgett, D.A., & Sheridan, J.F. (2004). Physical defeat reduces the sensitivity of murine splenocytes to the suppressive effects of corticosterone. Brain, Behavior and Immunity, 18, 416–424. doi:10.1016/j.bbi.2003.09.012
   PubMed Web of Science ®Google Scholar
• Borta, A., & Schwarting, R. (2005). Inhibitory avoidance, pain reactivity, and plus-maze behavior in Wistar rats with high versus low rearing activity. Physiology & Behavior, 84, 387–396. doi:10.1016/j.physbeh.2005.01.009
   PubMed Web of Science ®Google Scholar
• Bosch, O.J., Nair, H.P., Ahern, T.H., Neumann, I.D., & Young, L.J. (2009). The CRF system mediates increased passive stress-coping behavior following the loss of a bonded partner in a monogamous rodent. Neuropsychopharmacology, 34, 1406–1415. doi:10.1038/npp.2008.154
   PubMed Web of Science ®Google Scholar
• Burkett, J.P., Andari, E., Johnson, Z.V., Curry, D.C., de Waal, F.B.M., & Young, L.J. (2016). Oxytocin-dependent consolation behavior in rodents. Science, 351, 375–378. doi:10.1126/science.aac4785
   PubMed Web of Science ®Google Scholar
• Cacioppo, J.T., & Cacioppo, S. (2018). Loneliness in the modern age: An evolutionary theory of loneliness (ETL). Advances in Experimental Social Psychology, 58, 127–197.
   Web of Science ®Google Scholar
• Carnevali, L., Montano, N., Statello, R., Coudé, G., Vacondio, F., Rivara, S., … Sgoifo, A. (2017). Social stress contagion in rats: Behavioural, autonomic and neuroendocrine correlates. Psychoneuroendocrinology, 82, 155–163. doi:10.1016/j.psyneuen.2017.05.017
   PubMed Web of Science ®Google Scholar
• Carola, V., D'Olimpio, F., Brunamonti, E., Mangia, F., & Renzi, P. (2002). Evaluation of the elevated plus-maze and open-field tests for the assessment of anxiety-related behaviour in inbred mice. Behavioural Brain Research, 134, 49–57. doi:10.1016/S0166-4328(01)00452-1
   PubMed Web of Science ®Google Scholar
• Carter, C.S., & Getz, L.L. (1993). Monogamy and the prairie vole. Scientific American, 268, 100–106. doi:10.1038/scientificamerican0693-100
   PubMed Web of Science ®Google Scholar
• Choleris, E., Thomas, A.W., Kavaliers, M., & Prato, F.S. (2001). A detailed ethological analysis of the mouse open field test: Effects of diazepam, chlordiazepoxide and an extremely low frequency pulsed magnetic field. Neuroscience and Biobehavioral Reviews, 25, 235–260. doi:10.1016/s0149-7634(01)00011-2
   PubMed Web of Science ®Google Scholar
• Cryan, J.F., Mombereau, C., & Vassout, A. (2005). The tail suspension test as a model for assessing antidepressant activity: Review of pharmacological and genetic studies in mice. Neuroscience & Biobehavioral Reviews, 29, 571–625. doi:10.1016/j.neubiorev.2005.03.009
   PubMed Web of Science ®Google Scholar
• Eisenberger, N.I., Lieberman, M.D., & Williams, K.D. (2003). Does rejection hurt? An fMRI study of social exclusion. Science, 302, 290–292. doi:10.1126/science.1089134
   PubMed Web of Science ®Google Scholar
• Engert, V., Linz, R., & Grant, J.A. (2019). Embodied stress: The physiological resonance of psychosocial stress. Psychoneuroendocrinology, 105, 138–146. doi:10.1016/j.psyneuen.2018.12.221
   PubMed Web of Science ®Google Scholar
• Engert, V., Plessow, F., Miller, R., Kirschbaum, C., & Singer, T. (2014). Cortisol increase in empathic stress is modulated by emotional closeness and observation modality. Psychoneuroendocrinology, 45, 192–201. doi:10.1016/j.psyneuen.2014.04.005
   PubMed Web of Science ®Google Scholar
• Finnell, J.E., Lombard, C.M., Padi, A.R., Moffitt, C.M., Wilson, L.B., Wood, C.S., & Wood, S.K. (2017). Physical versus psychological social stress in male rats reveals distinct cardiovascular, inflammatory and behavioral consequences. PLoS One, 12, e0172868 doi:10.1371/journal.pone.0172868
   PubMed Web of Science ®Google Scholar
• Glaser, R., & Kiecolt-Glaser, J.K. (2005). Stress-induced immune dysfunction: Implications for health. Nature Reviews Immunology, 5, 243–251. doi:10.1038/nri1571
   PubMed Web of Science ®Google Scholar
• Gould, T.D., Dao, D.T., & Kovacsics, C.E. (2009). The open field test. In T. Gould (Ed.), Mood and anxiety related phenotypes in mice neuromethods (Vol. 42). Totowa, NJ: Humana Press.
   Google Scholar
• Grippo, A.J., Ihm, E.D., Wardwell, J., McNeal, N., Scotti, M.L., Moenk, D.A., … Preihs, K. (2014). The effects of environmental enrichment on depressive- and anxiety-related behaviors in socially isolated prairie voles. Psychosomatic Medicine, 76, 277–284. doi:10.1097/PSY.0000000000000052
   PubMed Web of Science ®Google Scholar
• Grippo, A.J., Lamb, D.G., Carter, C.S., & Porges, S.W. (2007). Cardiac regulation in the socially monogamous prairie vole. Physiology & Behavior, 90, 386–393. doi:10.1016/j.physbeh.2006.09.037
   PubMed Web of Science ®Google Scholar
• Grippo, A.J., Lamb, D.G., Carter, C.S., & Porges, S.W. (2007). Social isolation disrupts autonomic regulation of the heart and influences negative affective behaviors. Biological Psychiatry, 62, 1162–1170. doi:10.1016/j.biopsych.2007.04.011
   PubMed Web of Science ®Google Scholar
• Grippo, A.J., Scotti, M.A., Wardwell, J., McNeal, N., Bates, S.L., Chandler, D.L., … Jadia, N. (2018). Cardiac and behavioral effects of social isolation and experimental manipulation of autonomic balance. Autonomic Neuroscience, 214, 1–8. doi:10.1016/j.autneu.2018.08.002
   PubMed Web of Science ®Google Scholar
• Hatfield, E., Cacioppo, J., & Rapson, R.L. (1992). Emotional contagion. In M. S. Clark (Ed.), Review of personality and social psychology (Vol. 14 Emotion and Social Behavior, pp. 151–177). Newbury Park, CA: Sage.
   Google Scholar
• Hennessy, M.B., Kaiser, S., & Sachser, N. (2009). Social buffering of the stress response: Diversity, mechanisms, and functions. Frontiers in Neuroendocrinology, 30, 470–482. doi:10.1016/j.yfrne.2009.06.001
   PubMed Web of Science ®Google Scholar
• Hostinar, C.E., Sullivan, R.M., & Gunnar, M.R. (2014). Psychobiological mechanisms underlying the social buffering of the hypothalamic-pituitary-adrenocortical axis: A review of animal models and human studies across development. Psychological Bulletin, 140, 256–282. doi:10.1037/a0032671
   PubMed Web of Science ®Google Scholar
• Iñiguez, S.D., Flores-Ramirez, F.J., Riggs, L.E., Alipo, J.B., Garcia, I., Hernandez, M.A., … Castillo, S.A. (2018). Vicarious social defeat stress induces depression-related outcomes in female mice. Biological Psychiatry, 83, 9–17. doi:10.1016/j.biopsych.2017.07.014
   PubMed Web of Science ®Google Scholar
• Kavaliers, M., Colwell, D.D., & Choleris, E. (2003). Learning to fear and cope with a natural stressor: Individually and socially acquired corticosterone and avoidance responses to biting flies. Hormones and Behavior, 43, 99–107. doi:10.1016/S0018-506X(02)00021-1
   PubMed Web of Science ®Google Scholar
• Langford, D.J., Crager, S.E., Shehzad, Z., Smith, S.B., Sotocinal, S.G., Levenstadt, J.S., … Mogil, J.S. (2006). Social modulation of pain as evidence for empathy in mice. Science, 312, 1967–1970. doi:10.1126/science.1128322
   PubMed Web of Science ®Google Scholar
• Levenson, R.W. (2003). Blood, sweat, and fears: The autonomic architecture of emotion. Annals of the New York Academy of Sciences, 1000, 348–366. doi:10.1196/annals.1280.016
   PubMed Web of Science ®Google Scholar
• McEwen, B.S. (2008). Central effects of stress hormones in health and disease: Understanding the protective and damaging effects of stress and stress mediators. European Journal of Pharmacology, 583, 174–185. doi:10.1016/j.ejphar.2007.11.071
   PubMed Web of Science ®Google Scholar
• McNeal, N., Appleton, K.M., Johnson, A.K., Scotti, M.L., Wardwell, J., Murphy, R., … Grippo, A.J. (2017). The protective effects of social bonding on behavioral and pituitary-adrenal axis reactivity to chronic mild stress in prairie voles. Stress, 20, 175–182. doi:10.1080/10253890.2017.1295444
   PubMed Web of Science ®Google Scholar
• McNeal, N., Scotti, M.L., Wardwell, J., Chandler, D.L., Bates, S.L., LaRocca, M.A., … Grippo, A.J. (2014). Disruption of social bonds induces behavioral and physiological dysregulation in male and female prairie voles. Autonomic Neuroscience, 180, 9–16. doi:10.1016/j.autneu.2013.10.001
   PubMed Web of Science ®Google Scholar
• McNeal, N., Watanasriyakul, W.T., Normann, M.C., Akinbo, O.I., Dagner, A., Ihm, E., … Grippo, A.J. (2019). The negative effects of social bond disruption are partially ameliorated by sertraline administration in prairie voles. Autonomic Neuroscience, 219, 5–18. doi:10.1016/j.autneu.2019.03.003
   PubMed Web of Science ®Google Scholar
• Meyer, M.L., Masten, C.L., Ma, Y., Wang, C., Shi, Z., Eisenberger, N.I., & Han, S. (2013). Empathy for the social suffering of friends and strangers recruits distinct patterns of brain activation. Social Cognitive and Affective Neuroscience, 8, 446–454. doi:10.1093/scan/nss019
   PubMed Web of Science ®Google Scholar
• Meyza, K.Z., Bartal, I.-A., Monfils, M.H., Panksepp, J.B., & Knapska, E. (2017). The roots of empathy: Through the lens of rodent models. Neuroscience & Biobehavioral Reviews, 76, 216–234. doi:10.1016/j.neubiorev.2016.10.028
   PubMed Web of Science ®Google Scholar
• Olazábal, D.E., & Young, L.J. (2005). Variability in ‘‘spontaneous’’ maternal behavior is associated with anxiety-like behavior and affiliation in naïve juvenile and adult female prairie voles (Microtus ochrogaster). Developmental Psychobiology, 47, 166–178. doi:10.1002/dev.20077
   PubMed Web of Science ®Google Scholar
• Pattij, T., Groenink, L., Hijzen, T.H., Oosting, R.S., Maes, R.A.A., van der Gugten, J., & Olivier, B. (2002). Autonomic changes associated with enhanced anxiety in 5-HT1A receptor knockout mice. Neuropsychopharmacology, 27, 380–390. doi:10.1016/S0893-133X(02)00317-2
   PubMed Web of Science ®Google Scholar
• Preston, S.D., & De Waal, F. (2002). Empathy: Its ultimate and proximate bases. Behavioral and Brain Sciences, 25, 1–20. doi:10.1017/S0140525X02000018
   PubMed Web of Science ®Google Scholar
• Seibenhener, M.L., & Wooten, M.C. (2015). Use of the open field maze to measure locomotor and anxiety-like behavior in mice. Journal of Visualized Experiments, e52434, 1–6. doi:10.3791/52434
   Google Scholar
• Shaffer, F., & Ginsberg, J.P. (2017). An overview of heart rate variability metrics and norms. Frontiers in Public Health, 5, 258. doi:10.3389/fpubh.2017.00258
   PubMed Web of Science ®Google Scholar
• Sial, O.K., Warren, B.L., Alcantara, L.F., Parise, E.M., & Bolaños-Guzmán, C.A. (2016). Vicarious social defeat stress: Bridging the gap between physical and emotional stress. Journal of Neuroscience Methods, 258, 94–103. doi:10.1016/j.jneumeth.2015.10.012
   PubMed Web of Science ®Google Scholar
• Sivaselvachandran, S., Acland, E.L., Abdallah, S., & Martin, L.J. (2018). Behavioral and mechanistic insight into rodent empathy. Neuroscience & Biobehavioral Reviews, 91, 130–137. doi:10.1016/j.neubiorev.2016.06.007
   PubMed Web of Science ®Google Scholar
• Smith, A.S., & Wang, Z. (2014). Hypothalamic oxytocin mediates social buffering of the stress response. Biological Psychiatry, 76, 281–288. doi:10.1016/j.biopsych.2013.09.017
   PubMed Web of Science ®Google Scholar
• Sterley, T.-L., Baimoukhametova, D., Füzesi, T., Zurek, A.A., Daviu, N., Rasiah, N.P., … Bains, J.S. (2018). Social transmission and buffering of synaptic changes after stress. Nature Neuroscience, 21, 393–403. doi:10.1038/s41593-017-0044-6
   PubMed Web of Science ®Google Scholar
• Sun, P., Smith, A.S., Lei, K., Liu, Y., & Wang, Z. (2014). Breaking bonds in male prairie vole: Long-term effects on emotional and social behavior, physiology, and neurochemistry. Behavioural Brain Research, 265, 22–31. doi:10.1016/j.bbr.2014.02.016
   PubMed Web of Science ®Google Scholar
• Thayer, J.F., & Lane, R.D. (2009). Claude Bernard and the heart–brain connection: Further elaboration of a model of neurovisceral integration. Neuroscience & Biobehavioral Reviews, 33, 81–88. doi:10.1016/j.neubiorev.2008.08.004
   PubMed Web of Science ®Google Scholar
• Wallace, D.G., Martin, M.M., & Winter, S.S. (2008). Fractionating dead reckoning: Role of the compass, odometer, logbook, and home base establishment in spatial orientation. Die Naturwissenschaften, 95, 1011–1026. doi:10.1007/s00114-008-0410-z
   PubMedGoogle Scholar
• Walsh, R.N., & Cummins, R.A. (1976). The open-field test: A critical review. Psychological Bulletin, 83, 482–504. doi:10.1037/0033-2909.83.3.482
   PubMed Web of Science ®Google Scholar
• Weisstaub, N.V., Zhou, M., Lira, A., Lambe, E., González-Maeso, J., Hornung, J.P., … Gingrich, J.A. (2006). Cortical 5-HT2A receptor signaling modulates anxiety-like behaviors in mice. Science, 313, 536–540. doi:10.1126/science.1123432
   PubMed Web of Science ®Google Scholar
• Young, K.A., Gobrogge, K.L., Liu, Y., & Wang, Z. (2011). The neurobiology of pair bonding: Insights from a socially monogamous rodent. Frontiers in Neuroendocrinology, 32, 53–69. doi:10.1016/j.yfrne.2010.07.006
   PubMed Web of Science ®Google Scholar