Social environment regulates corticotropin releasing factor, corticosterone and vasopressin in juvenile prairie voles
Abstract
Stressful social conditions, such as isolation, that occur during sensitive developmental periods may alter present and future social behavior. Changes in the neuroendocrine mechanisms closely associated with affiliative behaviors and stress reactivity are likely to underlie these changes in behavior. In the present study, we assessed the effects of post-weaning social housing conditions on the neuropeptides arginine vasopressin (AVP) and oxytocin (OT), and components of the hypothalamic-pituitary-adrenal axis (corticotropin releasing factor: [CRF], and corticosterone: [CORT]) in the prairie vole (Microtus ochrogaster), a socially monogamous bi-parental rodent. Following weaning at 21 days of age, prairie voles were maintained in one of three housing conditions: social isolation (isolate), paired with a same sex sibling (sibling) or paired with a stranger (stranger) of the same sex and age. Housing conditions were maintained for either 4 or 21 days. Central CRF, AVP and OT immunoreactivity (ir) were quantified and circulating plasma CORT, AVP and OT were assayed. Isolated voles had higher CRF-ir in the paraventricular nucleus of the hypothalamus (PVN) compared with sibling and stranger housed voles. Plasma CORT was significantly higher in isolates. AVP-ir was significantly lower in the PVN of isolate females compared to either sibling females or stranger females. However, AVP-ir was significantly higher in the supraoptic nucleus (SON) of isolates compared to siblings. There were no differences in central OT-ir or plasma OT. These results identify neuroendocrine mechanisms which respond to isolation and potentially modulate behavior.
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Heightened HPA activity, shown by increased circulating corticosterone and ACTH, occurs after 1-5 days of isolation in juvenile or pair-bonded adult prairie voles.
“Heightened HPA axis activity (evidenced by a robust increase in circulating corticosterone and ACTH) is observed after 1–5 days of social isolation in juvenile (3–5 weeks old)68,69 or pair-bonded adult70–72 prairie voles.”
From Neural mechanisms of social homeostasis (2019) · cites this paper as [68]
Cites
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
The Evolution of Parental Care
Clutton‐Brock, T. H. (2019) · Princeton University Press eBooks · doi:10.2307/j.ctvs32ssj · Cited by 3,161 · see citing works
(2009) · Elsevier eBooks · doi:10.1016/c2009-1-03789-7 · Cited by 1,543 · see citing works
Limbic system mechanisms of stress regulation: Hypothalamo-pituitary-adrenocortical axis
Herman, J. P., Ostrander, M. M., Mueller, N. K., & Figueiredo, H. (2005) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2005.08.006 · Cited by 1,322 · see citing works
Landgraf, R., & Neumann, I. D. (2004) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2004.05.001 · Cited by 1,059 · see citing works
Stressor specificity of central neuroendocrine responses: implications for stress-related disorders
Pacák, K., & Palkovits, M. (2001) · Endocrine Reviews · doi:10.1210/edrv.22.4.0436 · Cited by 926 · see citing works
Goodson, J. L., & Bass, A. H. (2001) · Brain Research Reviews · doi:10.1016/s0165-0173(01)00043-1 · Cited by 632 · see citing works
Brain mechanisms of emotion and emotional learning
LeDoux, J. E. (1992) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(92)90011-9 · Cited by 593 · see citing works
Regulation of the hypothalamic corticotropin-releasing hormone neurosecretory system
Whitnall, M. H. (1993) · Progress in Neurobiology · doi:10.1016/0301-0082(93)90035-q · Cited by 582 · see citing works
Cho, M. M., DeVries, A. C., Williams, J. R., & Carter, C. S. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.5.1071 · Cited by 529 · see citing works
Plotsky, P. M., Thrivikraman, K. V., Nemeroff, C. B., Caldji, C., Sharma, S., & Meaney, M. J. (2005) · Neuropsychopharmacology · doi:10.1038/sj.npp.1300769 · Cited by 522 · see citing works
Effect of social isolation on stress-related behavioural and neuroendocrine state in the rat
Weiss, I. C., Pryce, C. R., Jongen-Rêlo, A. L., Nanz-Bahr, N. I., & Feldon, J. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.10.015 · Cited by 512 · cited 2× · see citing works
“Results from previous studies measuring basal CORT levels following isolation in rodents are mixed, showing increases (Gamallo et al., 1986; Hatch et al., 1965), decreases (Viveros et al., 1988; Sanchez et al., 1998) or no change (Holson et al., 1991; Morinan and Leonard, 1980; Weiss et al., 2004 ).”
Hall, F. S. (1998) · Critical Reviews™ in Neurobiology · doi:10.1615/critrevneurobiol.v12.i1-2.50 · Cited by 512 · see citing works
Heim, C., & Nemeroff, C. B. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00224-3 · Cited by 502 · see citing works
Social modulation of stress responses
DeVries, A. C., Glasper, E. R., & Detillion, C. E. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00152-5 · Cited by 482 · see citing works
Engelmann, M., Landgraf, R., & Wotjak, C. T. (2004) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2004.09.001 · Cited by 450 · see citing works
Heidbreder, C. A., Weiss, I. C., Domeney, A. M., Pryce, C., Homberg, J., Hedou, G., Feldon, J., Moran, M. C., & Nelson, P. (2000) · Neuroscience · doi:10.1016/s0306-4522(00)00336-5 · Cited by 404 · see citing works
Social organization of the prairie vole (Microtus ochrogaster)
Getz, L. L., McGuire, B., Pizzuto, T., Hofmann, J. E., & Frase, B. (1993) · Journal of Mammalogy · doi:10.2307/1381904 · Cited by 350 · see citing works
Amygdaloid CRF Pathways: Role in Autonomic, Neuroendocrine, and Behavioral Responses to Stress
Gray, T. S. (1993) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1993.tb49922.x · Cited by 288 · see citing works
Stressor Specificity of Central Neuroendocrine Responses: Implications for Stress-Related Disorders
Pacák, K. (2001) · Endocrine Reviews · doi:10.1210/er.22.4.502 · Cited by 280 · see citing works
The evolution of parental care
(1992) · Choice Reviews Online · doi:10.5860/choice.29-3305 · Cited by 267 · see citing works
de Goeij, D. C. E., Kvetnansky, R., Whitnall, M. H., Jezova, D., Berkenbosch, F., & Tilders, F. J. H. (2008) · Neuroendocrinology · doi:10.1159/000125712 · Cited by 250 · cited 1× · see citing works
“Differences in AVPir density may reflect long-term qualitative changes in central AVP production following chronic stress (de Goeij et al., 1991; Sanchez et al., 1998; Whitnall, 1993), potentially associated with behavioral and physiological adaptations to the social environment.”
Carter, C. S., Getz, L. L., Gavish, L., Dermott, J. L. M., & Arnold, P. (1980) · Biology of Reproduction · doi:10.1095/biolreprod23.5.1038 · Cited by 242 · see citing works
Dissociation of oxytocin, vasopressin and corticotropin secretion during different types of stress
Gibbs, D. M. (1984) · Life Sciences · doi:10.1016/0024-3205(84)90241-8 · Cited by 233 · cited 2× · see citing works
“social defeat, forced swim, restraint, cold) (Engelmann et al., 2004; Gibbs, 1984; Pacak and Palkovits, 2001).”
The effects of stress on social preferences are sexually dimorphic in prairie voles.
DeVries, A. C., DeVries, M. B., Taymans, S. E., & Carter, C. S. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.21.11980 · Cited by 219 · see citing works
Environmental animal models for sensorimotor gating deficiencies in schizophrenia: a review
Weiss, I. C., & Feldon, J. (2001) · Psychopharmacology · doi:10.1007/s002130100800 · Cited by 194 · see citing works
Sawchenko, P. E. (1987) · Brain Research · doi:10.1016/0006-8993(87)91641-6 · Cited by 184 · see citing works
Bamshad, M., Novak, M. A., & De Vries, G. J. (1993) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1993.tb00480.x · Cited by 175 · see citing works
Stress adaptation and adrenal activity in isolated and crowded rats
Gamallo, A., Villanua, A., Trancho, G. J., & Fraile, A. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90006-5 · Cited by 169 · see citing works
Early experience and depressive disorders: human and non-human primate studies
Gilmer, W. S., & McKinney, W. T. (2003) · Journal of Affective Disorders · doi:10.1016/s0165-0327(03)00046-6 · Cited by 169 · see citing works
“Isolation stress” revisited: isolation-rearing effects depend on animal care methods
Holson, R. R., Scallet, A. C., Ali, S. F., & Turner, B. B. (1991) · Physiology & Behavior · doi:10.1016/0031-9384(91)90338-o · Cited by 166 · see citing works
Bamshad, M., Novak, M. A., & de Vries, G. J. (1994) · Physiology & Behavior · doi:10.1016/0031-9384(94)90238-0 · Cited by 162 · see citing works
Hatch, A., Wiberg, G., Zawidzka, Z., Cann, M. C., Airth, J. M., & Grice, H. C. (1965) · Toxicology and Applied Pharmacology · doi:10.1016/0041-008x(65)90132-8 · Cited by 158 · see citing works
Cooperative breeding and monogamy in prairie voles: influence of the sire and geographical variation
Roberts, R. L., WILLIAMS, J. R., Wang, A. S., & Carter, C. S. (1998) · Animal Behaviour · doi:10.1006/anbe.1997.0659 · Cited by 152 · see citing works
Reyes, T. M., Walker, J. R., DeCino, C., Hogenesch, J. B., & Sawchenko, P. E. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-13-05607.2003 · Cited by 149 · see citing works
Suppression of Growth and Reproduction of Microtine Rodents by Social Factors
Batzli, G. O., Getz, L. L., & Hurley, S. S. (1977) · Journal of Mammalogy · doi:10.2307/1380006 · Cited by 141 · see citing works
McGuire, B., Getz, L. L., Hofmann, J. E., Pizzuto, T., & Frase, B. A. (1993) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00183784 · Cited by 139 · see citing works
Wang, Z., Young, L. J., Vries, G. J. D., & Insel, T. R. (1999) · Progress in brain research · doi:10.1016/s0079-6123(08)61589-7 · Cited by 132 · see citing works
Sánchez, M. M., Aguado, F., Sánchez-Toscano, F., & Saphier, D. (1998) · Endocrinology · doi:10.1210/endo.139.2.5720 · Cited by 129 · see citing works
The Neurobiology of Social Affiliation and Pair Bonding
Carter, C. S., & Keverne, E. B. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00004-8 · Cited by 128 · see citing works
Bester‐Meredith, J. K., & Marler, C. A. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.3.455 · Cited by 118 · see citing works
Ferris, C. F., Axelson, J. F., Martin, A., & Roberge, L. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90140-1 · Cited by 116 · see citing works
Kollack‐Walker, Don, Watson, & Akil (1999) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.1999.00354.x · Cited by 113 · see citing works
Taymans, S. E., DeVries, A. C., DeVries, M. B., Nelson, R. J., Friedman, T. C., de Castro, M., Detera‐Wadleigh, S. D., Carter, C. S., & Chrousos, G. P. (1997) · General and Comparative Endocrinology · doi:10.1006/gcen.1996.6849 · Cited by 112 · see citing works
The Neurobiology of Social Affiliation and Pair Bonding
Carter, C. S., & Keverne, E. B. (2002) · Elsevier eBooks · doi:10.1016/b978-012532104-4/50006-8 · Cited by 109 · see citing works
Interaction among Social Environment, the Hypothalamic–Pituitary–Adrenal Axis, and Behavior
DeVries, A. C. (2002) · Hormones and Behavior · doi:10.1006/hbeh.2002.1780 · Cited by 101 · see citing works
Sex and species differences in plasma oxytocin using an enzyme immunoassay
Kramer, K. M., Cushing, B. S., Carter, C. S., Wu, J., & Ottinger, M. A. (2004) · Canadian Journal of Zoology · doi:10.1139/z04-098 · Cited by 99 · see citing works
Social isolation in animal models of relevance to neuropsychiatric disorders
Kim, J. W., & Kirkpatrick, B. (1996) · Biological Psychiatry · doi:10.1016/0006-3223(95)00546-3 · Cited by 95 · see citing works
Weiss, I. C., Domeney, A. M., Moreau, J., Russig, H. D., & Feldon, J. (2001) · Behavioural Brain Research · doi:10.1016/s0166-4328(01)00166-8 · Cited by 91 · see citing works
Wang, Z. (1995) · Behavioral Neuroscience · doi:10.1037/0735-7044.109.2.305 · Cited by 91 · see citing works
Sibling recognition in the prairie vole, Microtus ochrogaster
Gavish, L. Y., Hofmann, J. E., & Getz, L. L. (1984) · Animal Behaviour · doi:10.1016/s0003-3472(84)80269-9 · Cited by 90 · see citing works
Familiarity and gender influence social preferences in prairie voles (Microtus ochrogaster)
DeVries, A. C., Johnson, C. L., & Carter, C. S. (1997) · Canadian Journal of Zoology · doi:10.1139/z97-037 · Cited by 84 · see citing works
Klein, S. L., Hairston, J. E., DeVries, A. C., & Nelson, R. J. (1997) · Hormones and Behavior · doi:10.1006/hbeh.1997.1402 · Cited by 77 · see citing works
Stowe, J. R., Liu, Y. T., CURTIS, J., FREEMAN, M., & WANG, Z. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.08.007 · Cited by 75 · see citing works
Kramer, K. M., Choe, C., Carter, C. S., & Cushing, B. S. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.07.001 · Cited by 58 · see citing works
Neuropeptides and non‐human primate social deficits associated with pathogenic rearing experience
Winslow, J. (2004) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2004.03.003 · Cited by 56 · see citing works
Sanchez, M. M. (1998) · Endocrinology · doi:10.1210/en.139.2.579 · Cited by 46 · see citing works
Ježová, D., Michajlovskij, N., Květňanský, R., & Makara, G. B. (2008) · Neuroendocrinology · doi:10.1159/000126436 · Cited by 45 · see citing works
Wilson, S. C. (1982) · Animal Behaviour · doi:10.1016/s0003-3472(82)80053-5 · Cited by 45 · see citing works
Female—female interactions and social stress in praine voles
Firestone, K., Thompson, K. V., & Carter, C. S. (1991) · Behavioral and Neural Biology · doi:10.1016/0163-1047(91)80125-x · Cited by 43 · see citing works
Some anatomical and physiological correlates of social isolation in the young rat
Morinan, A., & Leonard, B. E. (1980) · Physiology & Behavior · doi:10.1016/0031-9384(80)90265-6 · Cited by 40 · see citing works
Stress mediated changes in hypothalamic corticotropin releasing factor-like immunoreactivity
Moldow, R. L., Kastin, A. J., Graf, M., & Fischman, A. J. (1987) · Life Sciences · doi:10.1016/0024-3205(87)90144-5 · Cited by 40 · see citing works
Effects of social isolation and crowding upon adrenocortical reactivity and behavior in the rat.
Viveros, M., Hernández, R., Martínez, I. T. M., & González, P. (1988) · PubMed · Cited by 39 · see citing works
Ontogeny of Corticotropin-Releasing Factor and Arginine Vasopressein in the Rat
Rundle, S. E., & Funder, J. W. (2008) · Neuroendocrinology · doi:10.1159/000124941 · Cited by 37 · see citing works
Inoue, T., Koyama, T., Muraki, A., & Yamashita, I. (1993) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/0278-5846(93)90040-y · Cited by 33 · see citing works
Effects of isolation on sibling recognition in prairie voles,Microtus ochrogaster
MIÑATNO, G. P. Y., & Tang‐Martínez, Z. (1999) · Animal Behaviour · doi:10.1006/anbe.1999.1082 · Cited by 23 · see citing works
Social behavior, reproduction and demography of the prairie vole,Microtus ochrogaster
Getz, L. L., McGuire, B., & Carter, C. S. (2003) · Ethology Ecology & Evolution · doi:10.1080/08927014.2003.9522676 · Cited by 22 · see citing works
Sexual maturation in male prairie voles: Effects of the social environment
Mateo, J. M., Holmes, W., Bell, A. M., & Turner, M. (1994) · Physiology & Behavior · doi:10.1016/0031-9384(94)90198-8 · Cited by 22 · see citing works
Peptide Metabolism and the Control of Body Fluid Homeostasis
Silveira, P. F., Gil, J., Casis, L., & Irazusta, J. (2004) · Current Medicinal Chemistry - Cardiovascular & Hematological Agents · doi:10.2174/1568016043356264 · Cited by 16 · see citing works
Châtelain, A., Boudouresque, F., Chautard, T., Dupouyt, J. P., & Oliver, C. (1988) · Journal of Endocrinology · doi:10.1677/joe.0.1190059 · Cited by 15 · see citing works
Paz‐y‐Miño‐C, G., & Tang‐Martínez, Z. (1999) · Canadian Journal of Zoology · doi:10.1139/z98-190 · Cited by 15 · see citing works
Wang (1996) · doi:10.1002/(sici)1096-9861(19960318)366:4
Flagged first, then by citations
Cited by
Sorted by citations
Oxytocin, vasopressin and sociality
CARTER, C., GRIPPO, A., POURNAJAFINAZARLOO, H., RUSCIO, M., & PORGES, S. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00427-5 · Cited by 380 · see citing works
Self-citationStress, social behavior, and resilience: Insights from rodents
Beery, A. K., & Kaufer, D. (2014) · Neurobiology of Stress · doi:10.1016/j.ynstr.2014.10.004 · Cited by 373 · see citing works
Grippo, A. J., Gerena, D., Huang, J., Kumar, N., Shah, M., Ughreja, R., & Sue Carter, C. (2007) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2007.07.004 · Cited by 336 · see citing works
Neural mechanisms of social homeostasis
Matthews, G. A., & Tye, K. M. (2019) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.14016 · Cited by 273 · see citing works
Effects of social isolation on glucocorticoid regulation in social mammals
Hawkley, L. C., Cole, S. W., Capitanio, J. P., Norman, G. J., & Cacioppo, J. T. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.05.011 · Cited by 262 · 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
Social influences on neurobiology and behavior: Epigenetic effects during development
Curley, J. P., Jensen, C. L., Rahia Mashoodh, A., & Champagne, F. A. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.06.005 · Cited by 195 · see citing works
Social allostasis: anticipatory regulation of the internal milieu
Schulkin, J. (2011) · Frontiers in Evolutionary Neuroscience · doi:10.3389/fnevo.2010.00111 · Cited by 157 · see citing works
Early Life Experiences and Exercise Associate with Canine Anxieties
Tiira, K., & Lohi, H. (2015) · PLoS ONE · doi:10.1371/journal.pone.0141907 · Cited by 147 · 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
The Neurobiology of Social Affiliation and Pair Bonding
Carter, C. S., & Keverne, E. B. (2009) · Elsevier eBooks · doi:10.1016/b978-008088783-8.00004-8 · Cited by 128 · see citing works
The CRF system and social behavior: a review
Hostetler, C. M., & Ryabinin, A. E. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00092 · Cited by 105 · see citing works
Donovan, M., Mackey, C. S., Platt, G. N., Rounds, J., Brown, A. N., Trickey, D. J., Liu, Y., Jones, K. M., & Wang, Z. (2020) · Neurobiology of Stress · doi:10.1016/j.ynstr.2020.100278 · Cited by 85 · see citing works
An evolutionary social psychological approach to studying the effects of ostracism.
Wesselmann, E. D., Nairne, J. S., & Williams, K. D. (2012) · Journal of Social Evolutionary and Cultural Psychology · doi:10.1037/h0099249 · Cited by 106 · see citing works
Todeschin, A. S., Duarte, E. C. W., Jacob, M., Aranda, B. C. C., Jacobs, S., Fernandes, M. D. C., Ribeiro, M. F. M., Sanvitto, G. L., & Lucion, A. B. (2009) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.03.006 · Cited by 99 · see citing works
Are behavioral effects of early experience mediated by oxytocin?
Bales, K. L., Boone, E., Epperson, P., Hoffman, G., & Carter, C. S. (2011) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2011.00024 · Cited by 99 · see citing works
Pan, Y., Liu, Y., Young, K. A., Zhang, Z., & Wang, Z. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.02.064 · Cited by 94 · see citing works
Jiang, Z., Cowell, R. M., & Nakazawa, K. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00116 · Cited by 89 · see citing works
Autonomic, behavioral and neuroendocrine correlates of paternal behavior in male prairie voles
Kenkel, W. M., Suboc, G., & Carter, C. S. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.02.006 · Cited by 79 · 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
Central corticotropin releasing factor and social stress
Bäckström, T., & Winberg, S. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00117 · Cited by 76 · see citing works
Grippo, A. J., Pournajafi-Nazarloo, H., Sanzenbacher, L., Trahanas, D. M., McNeal, N., Clarke, D. A., Porges, S. W., & Sue Carter, C. (2012) · Stress · doi:10.3109/10253890.2011.605486 · Cited by 74 · see citing works
Rubin, L. H., Carter, C. S., Bishop, J. R., Pournajafi‐Nazarloo, H., Harris, M. S. H., Hill, S. K., Reilly, J. L., & Sweeney, J. A. (2013) · Schizophrenia Research · doi:10.1016/j.schres.2013.01.019 · Cited by 65 · see citing works
Neuropeptidergic regulation of pair-bonding and stress buffering: Lessons from voles
Gobrogge, K. L., & Wang, Z. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.08.010 · Cited by 62 · see citing works
Spencer, K. A. (2017) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2016.0242 · Cited by 56 · see citing works
Pournajafi-Nazarloo, H., Partoo, L., Yee, J., Stevenson, J., Sanzenbacher, L., Kenkel, W., Mohsenpour, S. R., Hashimoto, K., & Carter, C. S. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.10.015 · Cited by 53 · see citing works
Stress in groups: Lessons from non-traditional rodent species and housing models
Beery, A. K., Holmes, M. M., Lee, W., & Curley, J. P. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.03.033 · Cited by 51 · see citing works
Miyetani Chauke, A., Malisch, J. L., Robinson, C., A, T. R. D. J., & Wendy Saltzman, A. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.04.002 · Cited by 49 · see citing works
Schulkin, J. A. (2011) · Brain Research · doi:10.1016/j.brainres.2011.03.055 · Cited by 51 · see citing works
Relations between mechanisms of CNS arousal and mechanisms of stress
Pfaff, D. W., Martin, E. M., & Ribeiro, A. C. D. M. (2007) · Stress · doi:10.1080/10253890701638030 · Cited by 47 · see citing works
Curley, J. P., Rock, V., Moynihan, A. M., Bateson, P., Keverne, E. B., & Champagne, F. A. (2010) · Behavior Genetics · doi:10.1007/s10519-010-9334-4 · Cited by 46 · see citing works
Neuropeptide Regulation of Social Attachment: The Prairie Vole Model
Tabbaa, M., Paedae, B., Liu, Y., & Wang, Z. (2016) · Comprehensive physiology · doi:10.1002/cphy.c150055 · Cited by 53 · see citing works
Perkeybile, A. M., & Bales, K. L. (2017) · Journal of Experimental Biology · doi:10.1242/jeb.142182 · Cited by 42 · see citing works
Perkeybile, A. M., & Bales, K. L. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.01.025 · Cited by 39 · see citing works
Miyetani Chauke, A., A, T. R. D. J., Garland, T., & Wendy Saltzman, A. (2012) · Physiology & Behavior · doi:10.1016/j.physbeh.2012.05.012 · Cited by 41 · see citing works
Pohorecky, L. A. (2008) · Physiology & Behavior · doi:10.1016/j.physbeh.2008.02.010 · Cited by 39 · see citing works
Yee, J. R., Kenkel, W. M., Frijling, J. L., Dodhia, S., Onishi, K. G., Tovar, S., Saber, M. J., Lewis, G. F., Liu, W., Porges, S. W., et al. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.01.010 · Cited by 39 · see citing works
Barrett, C. E., Modi, M. E., Zhang, B. C., Walum, H., Inoue, K., & Young, L. J. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2014.05.041 · Cited by 34 · see citing works
Effects of population density on corticosterone levels of prairie voles in the field
Blondel, D. V., Wallace, G., Calderone, S., Gorinshteyn, M., Mary, C. M. S., & Phelps, S. M. (2015) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2015.09.002 · Cited by 33 · see citing works
Bardo, M. T., Hammerslag, L. R., & Malone, S. G. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108567 · Cited by 32 · see citing works
Watanasriyakul, W. T., Normann, M. C., Akinbo, O. I., Colburn, W., Dagner, A., & Grippo, A. J. (2019) · Stress · doi:10.1080/10253890.2019.1617691 · Cited by 30 · see citing works
Neural Circuits Underlying Rodent Sociality: A Comparative Approach
Lee, N. S., & Beery, A. K. (2019) · Current topics in behavioral neurosciences · doi:10.1007/7854_2018_77 · Cited by 31 · see citing works
Cardiac dysfunction and hypothalamic activation during a social crowding stressor in prairie voles
Grippo, A. J., Sgoifo, A., Mastorci, F., McNeal, N., & Trahanas, D. M. (2010) · Autonomic Neuroscience · doi:10.1016/j.autneu.2010.03.003 · Cited by 28 · see citing works
Mean Girls: Social Stress Models for Female Rodents
Kuske, J. X., & Trainor, B. C. (2021) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2021_247 · Cited by 27 · see citing works
Adaptation and well-being : social allostasis
Schulkin, J. A. (2011) · Cited by 26 · see citing works
Tanaka, K., Osako, Y., Takahashi, K., Hidaka, C., Tomita, K., & Yuri, K. (2019) · Heliyon · doi:10.1016/j.heliyon.2019.e01646 · Cited by 25 · see citing works
Perkeybile, A. M., & Bales, K. L. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.04.024 · Cited by 21 · see citing works
Beneficial effects of social attachment to overcome daily stress
Babygirija, R., Zheng, J., Bülbül, M., Ludwig, K., & Takahashi, T. (2010) · Brain Research · doi:10.1016/j.brainres.2010.07.028 · Cited by 18 · see citing works
Grippo, A. J., McNeal, N., Normann, M. C., Colburn, W., Dagner, A., & Woodbury, M. (2020) · Stress · doi:10.1080/10253890.2020.1812058 · Cited by 17 · see citing works
Watanasriyakul, W. T., Wardwell, J., McNeal, N., Schultz, R., Woodbury, M., Dagner, A., Cox, M., & Grippo, A. J. (2017) · Social Neuroscience · doi:10.1080/17470919.2017.1365761 · Cited by 16 · see citing works
McNeal, N., Anderson, E. M., Moenk, D. A., Trahanas, D. M., Matuszewich, L., & Grippo, A. J. (2016) · Social Neuroscience · doi:10.1080/17470919.2016.1276473 · Cited by 15 · see citing works
Partner separation rescues pair bond-induced decreases in hypothalamic oxytocin neural densities
Fricker, B. A., Roshko, V. C., Jiang, J., & Kelly, A. M. (2023) · Scientific Reports · doi:10.1038/s41598-023-32076-8 · Cited by 13 · see citing works
The Neurobiology of Social Affiliation and Pair Bonding
Carter, C. S., & Keverne, E. B. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00004-3 · Cited by 13 · see citing works
Ruscio, M. G., King, S. B., & Haun, H. L. (2015) · Physiology & Behavior · doi:10.1016/j.physbeh.2015.08.039 · Cited by 12 · see citing works
Self-citationWu, R., Song, Z., Tai, F., Wang, L., Kong, L., & Wang, J. (2013) · Behavioural Processes · doi:10.1016/j.beproc.2013.05.008 · Cited by 12 · see citing works
Hostetler, C. M., & Bales, K. L. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.03.019 · Cited by 11 · see citing works
Social environment alters central distribution of estrogen receptor alpha in juvenile prairie voles
Ruscio, M. G., Sweeny, T. D., Gomez, A. M., Parker, K., & Carter, C. S. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.06.005 · Cited by 11 · see citing works
Self-citationNeuropeptide Regulation of Social Attachment: The Prairie Vole Model
Tabbaa, M., Paedae, B., Liu, Y., & Wang, Z. (2017) · Comprehensive physiology · doi:10.1002/j.2040-4603.2017.tb00738.x · Cited by 9 · see citing works
Blondel, D. V., & Phelps, S. M. (2016) · Journal of comparative psychology · doi:10.1037/com0000048 · Cited by 9 · see citing works
Iba, H., Watanabe, T., Matsuzawa, K., Saimiya, M., Tanaka, M., Nagao, M., Moriyama, H., Kubota, K., Katsurabayashi, S., & Iwasaki, K. (2019) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.b19-00499 · Cited by 9 · see citing works
Neural Substrates Of Decision-Making In Economic GamesPreprint
Stanton, A. A. (2007) · RePEc: Research Papers in Economics · Cited by 9 · see citing works
Social environment affects central distribution of estrogen receptor-α in Peromyscus californicus
Ruscio, M. G., King, S. B., Sims, S., & McKendrick, G. (2018) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2018.08.018 · Cited by 4 · see citing works
Self-citationPournajafi‐Nazarloo, H., Partoo, L., Sanzenbacher, L., Esmaeilzadeh, M., Paredes, J., Hashimoto, K., Azizi, F., & Carter, C. S. (2009) · Peptides · doi:10.1016/j.peptides.2009.01.003 · Cited by 4 · see citing works
Scheun, J., Geiser, F., Ganswindt, A., & Nowack, J. (2019) · Australian Mammalogy · doi:10.1071/am18044 · Cited by 3 · see citing works
An integrative view of caviomorph social behavior
Ebensperger, L. A., & Hayes, L. D. (2016) · doi:10.1002/9781118846506.ch13 · Cited by 3 · see citing works
Effects of Group Size on Behavior, Reproduction, and mRNA Expression in Brains of Brandt’s Voles
Lu, W., Huang, S., Liu, J., Batsuren, E., Li, G., Wan, X., Zhao, J., Wang, Z., Han, W., & Zhang, Z. (2023) · Brain Sciences · doi:10.3390/brainsci13020311 · Cited by 2 · see citing works
Wang, Y., Deng, S., Fu, Q.-Y., & Liu, X. (2013) · Cited by 2 · see citing works
Grippo, A. J., Akinbo, O. I., Amidei, A., Wardwell, J., Normann, M. C., Ciosek, S., & Kovalev, D. Y. (2023) · Autonomic Neuroscience · doi:10.1016/j.autneu.2023.103145 · Cited by 2 · see citing works
Mull, N., Erdin, M., Letko, M. C., Seifert, S. N., Sironen, T. A., Smura, T., & Forbes, K. M. (2025) · npj Viruses · doi:10.1038/s44298-025-00153-6 · Cited by 1 · see citing works
Manipulação neonatal, ocitocina, vasopressina e comportamentos sociais em ratos
Todeschin, A. S. (2010) · Americanae (AECID Library)
Effects of Social-Interaction on Reward Sensitivity in Adolescent Mice
Cole, S. L. (2012) · OakTrust (Texas A&M University Libraries)
Methods for the study of behavioral neuroendocrinology
Wilkinson, M., & Brown, R. E. (2015) · Cambridge University Press eBooks · doi:10.1017/cbo9781139045803.015
Blocker, T. D. (2016) · SHAREOK (University of Oklahoma; Oklahoma State University; Central Oklahoma University)
Blondel, D. V. (2013) · University of Florida Digital Collections (University of Florida)
Endocrine and Behavioural Plasticity in Vertebrates
Fry, A. L. (2021) · doi:10.23889/suthesis.56835
The Neuroendocrine and Cardiovascular Responses to a Pup in Male Prairie Voles (M. ochrogaster)
Kenkel, W. M. (2013) · Figshare
(2008) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0b013e3283040e80
Белялетдинов, Р. Р. (2023) · Горизонты гуманитарного знания · doi:10.17805/ggz.2023.3.2
Neurobiology and the Good: Is It Possible to Make a Person Moral?
Belyaletdinov, R. (2020) · Sociology of power · doi:10.22394/2074-0492-2020-2-87-103
Bouamrane, L. (2015) · theses.fr (ABES) · doi:10.70675/00597159za953z4221z95b8z57a6c1d48c8e
Maturation of social adaptation circuits from ontogeny to pathology
Gleske, M., Jeanneteau, F. D., Opendak, M. M., & Coutellier, L. D. (2026) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2026.106874
- Authors
- Ruscio, M. G., Sweeny, T., Hazelton, J., Suppatkul, P., & Sue Carter, C.
- Affiliations
- College of Charleston (US)
- University of Illinois Chicago (US)
- Corresponding author
- Ruscio, Michael G.
- ORCID
- Sweeny, Timothy
- Venue
- Hormones and Behavior
- Publisher
- Elsevier BV
- Published
- 2007-01
- Volume
- 51
- Issue
- 1
- Pages
- 54-61
- ISSN
- 0018-506X (ISSN-L)
- OpenAlex
- W2129988184
- Cited by
- 81
- References
- 72
- Citations by year
- 2026: 1 · 2025: 1 · 2023: 4 · 2021: 3 · 2020: 4 · 2019: 6 · 2018: 1 · 2017: 4 · 2016: 7 · 2015: 8 · 2014: 5 · 2013: 8 · 2012: 5
- FWCI
- 5.16
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Hormones and Behavior (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (P01 HD 38490, P01HD038490)
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- Microtus ochrogaster, social isolation, social housing, corticotropin-releasing factor, corticosterone, vasopressin, oxytocin, hypothalamic-pituitary-adrenal axis, paraventricular nucleus, supraoptic nucleus, post-weaning development, stress reactivity, affiliative behavior, sensitive period, neuroendocrine regulation of behavior
- MeSH terms
- Animals, Brain Chemistry, Corticosterone, Corticotropin-Releasing Hormone, Arvicolinae, Female, Male, Paraventricular Hypothalamic Nucleus, Social Isolation, Supraoptic Nucleus, Vasopressins
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