Depressive-like behavior, its sensitization, social buffering, and altered cytokine responses in rhesus macaques moved from outdoor social groups to indoor housing

References

• Agid, O., Shapira, B., Zislin, J., Ritsner, M., Hanin, B., Murad, H., … Lerer, B. (1999). Environment and vulnerability to major psychiatric illness: A case control study of early parental loss in major depression, bipolar disorder and schizophrenia. Molecular Psychiatry, 4, 163–172. doi:10.1038/sj.mp.4000473
   PubMed Web of Science ®Google Scholar
• Anisman, H. (2009). Cascading effects of stressors and inflammatory immune system activation: Implications for major depression. Journal of Psychiatry & Neuroscience, 34, 4–20.
   PubMed Web of Science ®Google Scholar
• Aubert, A. (1999). Sickness and behaviour in animals: A motivational perspective. Neuroscience & Biobehavioral Reviews, 23, 1029–1036. doi:10.1016/S0149-7634(99)00034-2
   PubMed Web of Science ®Google Scholar
• Barak, O., Weidenfeld, J., Goshen, I., Ben-Hur, T., Taylor, A. N., & Yirmiya, R. (2002). Intracerebral HIV-1 glycoprotein 120 produces sickness behavior and pituitary–adrenal activation in rats: Role of prostaglandins. Brain, Behavior, and Immunity, 16, 720–735. doi:10.1016/S0889-1591(02)00025-9
   PubMed Web of Science ®Google Scholar
• Bernet, C. Z., & Stein, M. B. (1999). Relationship of childhood maltreatment to the onset and course of major depression in adulthood. Depression and Anxiety, 9, 169–174. doi:10.1002/(ISSN)1520-6394
   PubMedGoogle Scholar
• Bertone-Johnson, E. R., Whitcomb, B. W., Missmer, S. A., Karlson, E. W., & Rich-Edwards, J. W. (2012). Inflammation and early-life abuse in women. American Journal of Preventive Medicine, 43, 611–620. doi:10.1016/j.amepre.2012.08.014
   PubMed Web of Science ®Google Scholar
• Bogdanova, O. V., Kanekar, S., D’Anci, K. E., & Renshaw, P. F. (2013). Factors influencing behavior in the forced swim test. Physiology & Behavior, 118, 227–239. doi:10.1016/j.physbeh.2013.05.012
   PubMed Web of Science ®Google Scholar
• Brown, G. W., Harris, T., & Copeland, J. R. (1977). Depression and loss. The British Journal of Psychiatry, 130, 1–18. doi:10.1192/bjp.130.1.1
   PubMed Web of Science ®Google Scholar
• Bull, S. J., Huezo-Diaz, P., Binder, E. B., Cubells, J. F., Ranjith, G., Maddock, C., … Pariante, C. M. (2009). Functional polymorphisms in the interleukin-6 and serotonin transporter genes, and depression and fatigue induced by interferon-α and ribavirin treatment. Molecular Psychiatry, 14, 1095–1104. doi:10.1038/mp.2008.48
   PubMed Web of Science ®Google Scholar
• Capitanio, J. P., Kyes, R. C., & Fairbanks, L. A. (2006). Considerations in the selection and conditioning of Old World Monkeys for laboratory research: Animals from domestic sources. ILAR Journal, 47, 294–306. doi:10.1093/ilar.47.4.294
   PubMed Web of Science ®Google Scholar
• Capuron, L., Gumnick, J. F., Musselman, D. L., Lawson, D. H., Reemsnyder, A., Nemeroff, C. B., & Miller, A. H. (2002). Neurobehavioral effects of interferon-α in cancer patients phenomenology and paroxetine responsiveness of symptom dimensions. Neuropsychopharmacology, 26, 643–652. doi:10.1016/S0893-133X(01)00407-9
   PubMed Web of Science ®Google Scholar
• Carpenter, L. L., Gawuga, C. E., Tyrka, A. R., Lee, J. K., Anderson, G. M., & Price, L. H. (2010). Association between plasma IL-6 response to acute stress and early-life adversity in healthy adults. Neuropsychopharmacology, 35, 2617–2623. doi:10.1038/npp.2010.159
   PubMed Web of Science ®Google Scholar
• Coelho, R., Viola, T. W., Walss-Bass, C., Brietzke, E., & Grassi-Oliveira, R. (2014). Childhood maltreatment and inflammatory markers: A systematic review. Acta Psychiatrica Scandinavica, 129, 180–192. doi:10.1111/acps.2014.129.issue-3
   PubMed Web of Science ®Google Scholar
• Danese, A., Moffitt, T. E., Pariante, C. M., Ambler, A., Poulton, R., & Caspi, A. (2008). Elevated inflammation levels in depressed adults with a history of childhood maltreatment. Archives of General .Psychiatry, 65, 409–416. doi:10.1001/archpsyc.65.4.409
   PubMed Web of Science ®Google Scholar
• Danese, A., Pariante, C. M., Caspi, A., Taylor, A., & Poulton, R. (2007). Childhood maltreatment predicts adult inflammation in a life-course study. Proceedings of the National Academy of Sciences, 104, 1319–1324. doi:10.1073/pnas.0610362104
   PubMed Web of Science ®Google Scholar
• Dantzer, R. (2004). Cytokine-induced sickness behaviour: A neuroimmune response to activation of innate immunity. European Journal of Pharmacology, 500, 399–411. doi:10.1016/j.ejphar.2004.07.040
   PubMed Web of Science ®Google Scholar
• Edgar, J., Held, S., Paul, E., Pettersson, I., Price, R. I., & Nicol, C. (2015). Social buffering in a bird. Animal Behaviour, 105, 11–19. doi:10.1016/j.anbehav.2015.04.007
   Web of Science ®Google Scholar
• Eyre, H., & Baune, B. T. (2012). Neuroimmunological effects of physical exercise in depression. Brain Behavior and Immunity, 26, 251–266. doi:10.1016/j.bbi.2011.09.015
   PubMed Web of Science ®Google Scholar
• Felger, J. C., Alagbe, O., Hu, F., Mook, D., Freeman, A. A., Sanchez, M. M., … Miller, A. H. (2007). Effects of interferon-alpha on rhesus monkeys: A nonhuman primate model of cytokine-induced depression. Biological Psychiatry, 62, 1324–1333. doi:10.1016/j.biopsych.2007.05.026
   PubMed Web of Science ®Google Scholar
• Friedman, E. M., Boinski, S., & Coe, C. L. (1995). Interleukin-1 induces sleep-like behavior and alters call structure in juvenile rhesus macaques. American Journal of Primatology, 35, 143–153. doi:10.1002/(ISSN)1098-2345
   PubMed Web of Science ®Google Scholar
• Ganguly, P., & Brenhouse, H. C. (2015). Broken or maladaptive? Altered trajectories in neuroinflammation and behavior after early life adversity. Developmental Cognitive Neuroscience, 11, 18–30. doi:10.1016/j.dcn.2014.07.001
   PubMed Web of Science ®Google Scholar
• Glaser, R., & Kiecolt-Glaser, J. K. (2005). Science and society: Stress-induced immune dysfunction: Implications for health. Nature Reviews Immunology, 5, 243–251. doi:10.1038/nri1571
   PubMed Web of Science ®Google Scholar
• Gold, P. W., Goodwin, F. K., & Chrousos, G. P. (1988). Clinical and biochemical manifestations of depression: Relation to the neurobiology of stress (Part 2). New England Journal of Medicine, 319, 413–420. doi:10.1056/NEJM198808183190706
   PubMed Web of Science ®Google Scholar
• Gouin, J.-P., Glaser, R., Malarkey, W. B., Beversdorf, D., & Kiecolt-Glaser, J. K. (2012). Childhood abuse and inflammatory responses to daily stressors. Annals of Behavioral Medicine, 44, 287–292. doi:10.1007/s12160-012-9386-1
   PubMed Web of Science ®Google Scholar
• Haapakoski, R., Mathieu, J., Ebmeier, K. P., Alenius, H., & Kivimäki, M. (2015). Cumulative meta-analysis of interleukins 6 and 1β, tumour necrosis factor α and C-reactive protein in patients with major depressive disorder. Brain, Behavior, and Immunity, 49, 206–215. doi:10.1016/j.bbi.2015.06.001
   PubMed Web of Science ®Google Scholar
• Harb, F., Hidalgo, M. P., & Martau, B. (2015). Lack of exposure to natural light in the workspace is associated with physiological, sleep, and depressive symptoms. Chronobiology International, 32, 368–375. doi:10.3109/07420528.2014.982757
   PubMed Web of Science ®Google Scholar
• Hart, B. L. (1988). Biological basis of the behavior of sick animals. Neuroscience & Biobehavioral Reviews, 12, 123–137. doi:10.1016/S0149-7634(88)80004-6
   PubMed Web of Science ®Google Scholar
• Heim, C., Newport, D. J., Mletzko, T., Miller, A. H., & Nemeroff, C. B. (2008). The link between childhood trauma and depression: Insights from HPA axis studies in humans. Psychoneuroendocrinology, 33, 693–710. doi:10.1016/j.psyneuen.2008.03.008
   PubMed Web of Science ®Google Scholar
• Hennessy, M. B. (2014). Filial attachment and its disruption: Insights from the guinea pig. Developmental Psychobiology, 56, 1747–1754. doi:10.1002/dev.v56.8
   PubMed Web of Science ®Google Scholar
• Hennessy, M. B., Deak, T., & Schiml-Webb, P. A. (2010). Early attachment figure separation and increased risk for later depression: Potential mediation by proinflammatory processes. Neuroscience & Biobehavioral Reviews, 34, 782–790. doi:10.1016/j.neubiorev.2009.03.012
   PubMed Web of Science ®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
• Hennessy, M. B., McCowan, B., Jiang, J., & Capitanio, J. P. (2014). Depressive-like behavioral response of adult male rhesus monkeys during routine animal husbandry procedure. Frontiers in Behavioral Neuroscience, 8, Article 309, 1–8. doi:10.3389/fnbeh.2014.00309
   PubMed Web of Science ®Google Scholar
• Hennessy, M. B., Schiml-Webb, P. A., & Deak, T. (2009). Separation, sickness, and depression: A new perspective on an old animal model. Current Directions in Psychological Science, 18, 227–231. doi:10.1111/cdir.2009.18.issue-4
   PubMed Web of Science ®Google Scholar
• Hennessy, M. B., Schiml-Webb, P. A., Miller, E. E., Maken, D. S., Bullinger, K. L., & Deak, T. (2007). Anti-inflammatory agents attenuate the passive responses of guinea pig pups: Evidence for stress-induced sickness behavior during maternal separation. Psychoneuroendocrinology, 32, 508–515. doi:10.1016/j.psyneuen.2007.03.004
   PubMed Web of Science ®Google Scholar
• Hennessy, M. B., Stafford, N. P., Yusko-Osborne, B., Schiml, P. A., Xanthos, E. D., & Deak, T. (2015). Naproxen attenuates sensitization of depressive-like behavior and fever during maternal separation. Physiology & Behavior, 139, 34–40. doi:10.1016/j.physbeh.2014.11.030
   PubMed Web of Science ®Google Scholar
• Horowitz, M. A., & Zunszain, P. A. (2015). Neuroimmune and neuroendocrine abnormalities in depression: Two sides of the same coin. Annals of the New York Academy of Sciences, 1351, 68–79. doi:10.1111/nyas.12781
   PubMed Web of Science ®Google Scholar
• Iwata, M., Ota, K. T., & Duman, R. S. (2013). The inflammasome: Pathways linking psychological stress, depression, and systemic illnesses. Brain, Behavior, and Immunity, 31, 105–114. doi:10.1016/j.bbi.2012.12.008
   PubMed Web of Science ®Google Scholar
• Kendler, K. S., Hettema, J. M., Butera, F., Gardner, C. O., & Prescott, C. A. (2003). Life event dimensions of loss, humiliation, entrapment, and danger in the prediction of onsets of major depression and generalized anxiety. Archives of General Psychiatry, 60, 789–796. doi:10.1001/archpsyc.60.8.789
   PubMed Web of Science ®Google Scholar
• Kendler, K. S., Karkowski, L. M., & Prescott, C. A. (1999). Causal relationship between stressful life events and the onset of major depression. American Journal of Psychiatry, 156, 837–841. doi:10.1176/ajp.156.6.837
   PubMed Web of Science ®Google Scholar
• Kiyokawa, Y. (2015). Social odors; alarm pheromones and social buffering. Current Topics in Behavioral Neuroscience. [Epub ahead of print]
   PubMedGoogle Scholar
• Köhler, O., Benros, M. E., Nordentoft, M., Farkouh, M. E., Iyengar, R. L., Mors, O., & Krogh, J. (2014). Effect of anti-inflammatory treatment on depression, depressive symptoms, and adverse effects: A systematic review and meta-analysis of randomized clinical trials. JAMA Psychiatry, 71, 1381–1391. doi:10.1001/jamapsychiatry.2014.1611
   PubMed Web of Science ®Google Scholar
• LeMay, L. G., Vander, A. J., & Kluger, M. J. (1990). The effects of psychological stress on plasma interleukin-6 activity in rats. Physiology & Behavior, 47, 957–961. doi:10.1016/0031-9384(90)90024-X
   PubMed Web of Science ®Google Scholar
• Maier, S. F., & Watkins, L. R. (1998). Cytokines for psychologists: Implications of bidirectional immune-to-brain communication for understanding behavior, mood, and cognition. Psychological Review, 105, 83–107. doi:10.1037/0033-295X.105.1.83
   PubMed Web of Science ®Google Scholar
• Miller, G. E., & Chen, E. (2010). Harsh family climate in early life presages the emergence of a proinflammatory phenotype in adolescence. Psychological Science, 21, 848–856. doi:10.1177/0956797610370161
   PubMed Web of Science ®Google Scholar
• Miller, G. E., & Cole, S. W. (2012). Clustering of depression and inflammation in adolescents previously exposed to childhood adversity. Biological Psychiatry, 72, 34–40. doi:10.1016/j.biopsych.2012.02.034
   PubMed Web of Science ®Google Scholar
• Miller, G. E., Rohleder, N., & Cole, S. W. (2009). Chronic interpersonal stress predicts activation of pro- and anti-inflammatory signaling pathways 6 months later. Psychosomatic Medicine, 71, 57–62. doi:10.1097/PSY.0b013e318190d7de
   PubMed Web of Science ®Google Scholar
• Miura, H., Ozaki, N., Sawada, M., Isobe, K., Ohta, T., & Nagatsu, T. (2008). A link between stress and depression: Shifts in the balance between the kynurenine and serotonin pathways of tryptophan metabolism and the etiology and pathophysiology of depression. Stress, 11, 198–209. doi:10.1080/10253890701754068
   PubMed Web of Science ®Google Scholar
• Noldus, J. (1991). The Observer: A software system for collection and analysis of observational data. Behavior Research Methods, Instruments, & Computers, 23, 415–429. doi:10.3758/BF03203406
   Google Scholar
• Perkeybile, A. M., Schiml-Webb, P. A., O’Brien, E., Deak, T., & Hennessy, M. B. (2009). Anti-inflammatory influences on behavioral, but not cortisol, responses during maternal separation. Psychoneuroendocrinology, 34, 1101–1108. doi:10.1016/j.psyneuen.2009.02.014
   PubMed Web of Science ®Google Scholar
• Reinherz, H. Z., Giaconia, R. M., Carmola Hauf, A. M., Wasserman, M. S., & Silverman, A. B. (1999). Major depression in the transition to adulthood: Risks and impairments. Journal of Abnormal Psychology, 108, 500–510. doi:10.1037/0021-843X.108.3.500
   PubMed Web of Science ®Google Scholar
• Roque, S., Correia-Neves, M., Mesquita, A. R., Palha, J. A., & Sousa, N. (2009). Interleukin-10: A key cytokine in depression? Cardiovascular Psychiatry and Neurology, 2009, 1–5. doi:10.1155/2009/187894
   Google Scholar
• Réus, G. Z., Fries, G. R., Stertz, L., Badawy, M., Passos, I. C., Barichello, T., … Quevedo, J. (2015). The role of inflammation and microglial activation in the pathophysiology of psychiatric disorders. Neuroscience, 300, 141–154.
   PubMed Web of Science ®Google Scholar
• Schiml-Webb, P. A., Deak, T., Greenlee, T., Maken, D. S., & Hennessy, M. B. (2006). Alpha melanocyte stimulating hormone reduces putative stress-induced sickness behaviors in isolated guinea pig pups. Behavioural Brain Research, 168, 326–330. doi:10.1016/j.bbr.2005.08.022
   PubMed Web of Science ®Google Scholar
• Schulkin, J., McEwen, B. S., & Gold, P. W. (1994). Allostasis, amygdala, and anticipatory angst. Neuroscience & Biobehavioral Reviews, 18, 385–396. doi:10.1016/0149-7634(94)90051-5
   PubMed Web of Science ®Google Scholar
• Slavich, G. M., & Irwin, M. R. (2014). From stress to inflammation and major depressive disorder: A social signal transduction theory of depression. Psychological Bulletin, 140, 774–815. doi:10.1037/a0035302
   PubMed Web of Science ®Google Scholar
• Slavich, G. M., O’Donovan, A., Epel, E. S., & Kemeny, M. E. (2010). Black sheep get the blues: A psychobiological model of social rejection and depression. Neuroscience & Biobehavioral Reviews, 35, 39–45. doi:10.1016/j.neubiorev.2010.01.003
   PubMed Web of Science ®Google Scholar
• Slopen, N., Kubzansky, L. D., McLaughlin, K. A., & Koenen, K. C. (2013). Childhood adversity and inflammatory processes in youth: A prospective study. Psychoneuroendocrinology, 38, 188–200. doi:10.1016/j.psyneuen.2012.05.013
   PubMed Web of Science ®Google Scholar
• Strawbridge, R., Arnone, D., Danese, A., Papadopoulos, A., Herane Vives, A., & Cleare, A. J. (2015). Inflammation and clinical response to treatment in depression: A meta-analysis. European Neuropsychopharmacology, 25, 1532–1543. (epub ahead of print). doi:10.1016/j.euroneuro.2015.06.007
   PubMed Web of Science ®Google Scholar