Oxytocin modulates behavioral and physiological responses to a stressor in marmoset monkeys
Open accessAbstract
Social isolation is a major source of stress and can lead to activation of the hypothalamic-pituitary-adrenal (HPA) axis. The presence of a close social partner can reduce the magnitude of the HPA-axis response during a stressor, a phenomenon known as social buffering. The oxytocin (OXT) system has been identified as one candidate for mediating social buffering due to its role in the facilitation of social bonding and the expression of prosocial behavior. The goal of the present study was to determine whether the OXT system contributes to social buffering of HPA-axis activity in response to stressor exposure in marmoset monkeys (Callithrix jacchus). Male and female marmosets experienced a standardized psychogenic stressor with and without their long-term mate under OXT-treatments (Pro(8)-OXT, Leu(8)-OXT, OXT antagonist, and saline); we assessed HPA-axis activity by measuring urinary cortisol across the stressor. We found that blocking, but not augmenting, the OXT system altered patterns of cortisol and proximity behavior in response to a stressor. We demonstrated that (1) the presence of a mate during a stressor significantly attenuated HPA-axis activity in female, but not male, marmosets; (2) male, but not female, marmosets treated with an OXT antagonist had significantly higher HPA-axis activity across the stressor than when they were treated with saline, suggesting that the OXT system may reduce the stressor-induced rise in cortisol levels; (3) male and female marmosets treated with an OXT antagonist spent significantly less time in close proximity to their mate during the first 30 min of the stressor than when they were treated with saline, suggesting that the OXT system may be important for the expression of partner-seeking behavior during a stressor. Thus, the OXT system and social context differentially influenced how the HPA-axis responded to a stressor in male and female marmosets, and may modulate HPA-axis activity by promoting the expression of proximity behavior with a close social partner.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The presence of a mate during a stressor significantly attenuated HPA-axis activity in female marmosets, but not males, relative to when marmosets experienced a stressor in complete isolation.
“The presence of a mate during a stressor significantly attenuated HPA-axis activity in females, but not males, relative to when marmosets experienced a stressor in complete isolation.”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Cavanaugh et al., 2016
Blocking OT signaling in marmosets with an OTa led to significantly higher cortisol levels in males during the stressor, suggesting that OT may reduce the stress-induced elevations in cortisol levels.
“blocking OT signaling in marmosets with an OTa led to significantly higher cortisol levels in males during the stressor, suggesting that OT may reduce the stress-induced elevations in cortisol levels.”
From Neuropeptide diversity and the regulation of social behavior in New World primates (2016) · cites this paper as Cavanaugh et al., 2016
Marmoset monkeys treated with an oxytocin receptor antagonist had elevated glucocorticoid levels in response to the stressor and showed a greater tendency to engage in maladaptive fear-related behaviour such as isolation.
“Indeed, a recent study found that marmoset monkeys treated with an oxytocin receptor antagonist had elevated glucocorticoid levels in response to the stressor and showed a greater tendency to engage in maladaptive fear-related behaviour such as isolation (Cavanaugh et al., 2016).”
From Meta-analytic review of the effects of a single dose of intranasal oxytocin on threat processing in humans (2018) · cites this paper as Cavanaugh et al., 2016
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Stress, social support, and the buffering hypothesis
Cohen, S., & Wills, T. A. (1985) · Psychological Bulletin · doi:10.1037/0033-2909.98.2.310 · Cited by 18,093 · see citing works
Pruessner, J. C., Kirschbaum, C., Meinlschmid, G., & Hellhammer, D. H. (2003) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(02)00108-7 · Cited by 3,638 · see citing works
Biobehavioral responses to stress in females: Tend-and-befriend, not fight-or-flight.
Taylor, S. E., Klein, L. C., Lewis, B. P., Gruenewald, T. L., Gurung, R. A. R., & Updegraff, J. A. (2000) · Psychological Review · doi:10.1037/0033-295x.107.3.411 · Cited by 3,308 · see citing works
The oxytocin receptor system: structure, function, and regulation
Gimpl, G., & Fahrenholz, F. (2001) · Physiological Reviews · doi:10.1152/physrev.2001.81.2.629 · Cited by 3,089 · see citing works
Heinrichs, M., Baumgartner, T., Kirschbaum, C., & Ehlert, U. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00465-7 · Cited by 2,091 · 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
Oxytocin and vasopressin in the human brain: social neuropeptides for translational medicine
Meyer-Lindenberg, A., Domes, G., Kirsch, P., & Heinrichs, M. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3044 · Cited by 1,688 · see citing works
Neumann, I. D., & Landgraf, R. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2012.08.004 · Cited by 954 · see citing works
Ditzen, B., Schaer, M., Gabriel, B., Bodenmann, G., Ehlert, U., & Heinrichs, M. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2008.10.011 · Cited by 784 · cited 1× · see citing works
“When OXT was administered intranasally during conflict in marital couples, positive communication between partners increased and circulating cortisol levels decreased (Ditzen et al., 2009), relative to individuals that received a placebo.”
BackgroundTend and Befriend: Biobehavioral Bases of Affiliation Under Stress
Taylor, S. E. (2006) · Current Directions in Psychological Science · doi:10.1111/j.1467-8721.2006.00451.x · Cited by 755 · 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
Intranasal Drug Delivery: How, Why and What For?
Pires, A., Fortuna, A., Alves, G., & Falcão, A. (2009) · Journal of Pharmacy & Pharmaceutical Sciences · doi:10.18433/j3nc79 · Cited by 641 · see citing works
Grewen, K. M., Girdler, S. S., Amico, J., & Light, K. C. (2005) · Psychosomatic Medicine · doi:10.1097/01.psy.0000170341.88395.47 · Cited by 513 · cited 1× · see citing works
“In humans, central and peripheral OXT release during social support from a long-term partner following a stressor facilitated the attenuation of the HPA-axis and anxiety-like behavior (Grewen et al., 2005; Heinrichs et al., 2003).”
BackgroundInfluentialIncreased brain and plasma oxytocin after nasal and peripheral administration in rats and mice
Neumann, I. D., Maloumby, R., Beiderbeck, D. I., Lukas, M., & Landgraf, R. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.03.003 · Cited by 511 · see citing works
Neumann, Wigger, Torner, Holsboer, & Landgraf (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00442.x · Cited by 452 · see citing works
Striepens, N., Kendrick, K. M., Hanking, V., Landgraf, R., Wüllner, U., Maier, W., & Hurlemann, R. (2013) · Scientific Reports · doi:10.1038/srep03440 · Cited by 452 · see citing works
Choi, D. C., Furay, A. R., Evanson, N. K., Ostrander, M. M., Ulrich-Lai, Y. M., & Herman, J. P. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.4301-06.2007 · Cited by 392 · see citing works
Choleris, E., Gustafsson, J.-Å., Korach, K. S., Muglia, L. J., Pfaff, D. W., & Ogawa, S. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0631699100 · Cited by 386 · see citing works
Anxiety and stress responses in female oxytocin deficient mice
Amico, J. A., Mantella, R. C., Vollmer, R. R., & Li, X. (2004) · Journal of Neuroendocrinology · doi:10.1111/j.0953-8194.2004.01161.x · Cited by 327 · see citing works
Psychobiology of social support: The social dimension of stress buffering
Ditzen, B., & Heinrichs, M. (2014) · Restorative Neurology and Neuroscience · doi:10.3233/rnn-139008 · Cited by 298 · cited 5× · see citing works
“Brosnan et al. (2015) suggested that treatment with OXT elicited an anxiolytic response, thus diminished the motivation, and potentially the need, for social contact (which can be anxiolytic itself; Ditzen and Heinrichs, 2014).”
BackgroundInfluentialDabrowska, J., Hazra, R., Ahern, T. H., Guo, J.-D., McDonald, A. J., Mascagni, F., Muller, J. F., Young, L. J., & Rainnie, D. G. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2011.03.003 · Cited by 274 · see citing works
Bahr, N. I., Palme, R., Möhle, U., Hodges, J. K., & Heistermann, M. (2000) · General and Comparative Endocrinology · doi:10.1006/gcen.1999.7431 · Cited by 270 · see citing works
Positive couple interactions and daily cortisol: On the stress-protecting role of intimacy
Ditzen, B., Hoppmann, C., & Klumb, P. (2008) · Psychosomatic Medicine · doi:10.1097/psy.0b013e318185c4fc · Cited by 242 · see citing works
Grippo, A. J., Trahanas, D. M., Zimmerman, R. R., Porges, S. W., & Carter, C. S. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.05.017 · Cited by 240 · see citing works
Smith, A. S., Ågmo, A., Birnie, A. K., & French, J. A. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2009.12.004 · Cited by 228 · see citing works
Interplay of oxytocin, vasopressin, and sex hormones in the regulation of social recognition
Gabor, C. S., Phan, A., Clipperton-Allen, A. E., Kavaliers, M., & Choleris, E. (2012) · Behavioral Neuroscience · doi:10.1037/a0026464 · Cited by 221 · see citing works
Intranasal oxytocin administration attenuates the ACTH stress response in monkeys
Parker, K. J., Buckmaster, C. L., Schatzberg, A. F., & Lyons, D. M. (2005) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2005.04.002 · Cited by 204 · see citing works
Tribollet, E., Audigier, S., Dubois-Dauphin, M., & Dreifuss, J. J. (1990) · Brain Research · doi:10.1016/0006-8993(90)90232-z · Cited by 203 · see citing works
Arginine Vasopressin and Oxytocin Modulate Human Social Behavior
Ebstein, R. P., Israel, S., Lerer, E., Uzefovsky, F., Shalev, I., Gritsenko, I., Riebold, M., Salomon, S., & Yirmiya, N. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04541.x · Cited by 194 · see citing works
Oxytocin-Induced Analgesia and Scratching Are Mediated by the Vasopressin-1A Receptor in the Mouse
Schorscher-Petcu, A., Sotocinal, S., Ciura, S., Dupre, A., Ritchie, J., Sorge, R. E., Crawley, J. N., Hu, S.-B., Nishimori, K., Young, L. J., et al. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1594-10.2010 · Cited by 189 · see citing works
Intranasal oxytocin attenuates the cortisol response to physical stress: a dose-response study
Cardoso, C., Ellenbogen, M. A., Orlando, M. A., Bacon, S. L., & Joober, R. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.07.013 · Cited by 187 · see citing works
MacDonald, K., & Feifel, D. (2013) · Frontiers in Neuroscience · doi:10.3389/fnins.2013.00035 · Cited by 181 · see citing works
CSF and blood oxytocin concentration changes following intranasal delivery in macaque
Dal Monte, O., Noble, P. L., Turchi, J., Cummins, A., & Averbeck, B. B. (2014) · PLoS ONE · doi:10.1371/journal.pone.0103677 · Cited by 177 · see citing works
Making room for oxytocin in understanding depression
McQuaid, R. J., McInnis, O. A., Abizaid, A. B., & Anisman, H. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.07.005 · Cited by 172 · see citing works
Sex differences in vasopressin and oxytocin innervation of the brain
DEVRIES, G. (2008) · Progress in Brain Research · doi:10.1016/s0079-6123(08)00402-0 · Cited by 169 · see citing works
Neurobiological mechanisms of social attachment and pair bonding
Johnson, Z. V., & Young, L. J. (2015) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2015.01.009 · Cited by 169 · see citing works
Legros, J.-J. (2001) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(01)00018-x · Cited by 159 · see citing works
Geary, D. C., & Flinn, M. V. (2002) · Psychological Review · doi:10.1037/0033-295x.109.4.745 · Cited by 143 · see citing works
Oxytocin׳s role in anxiety: A critical appraisal
MacDonald, K., & Feifel, D. (2014) · Brain Research · doi:10.1016/j.brainres.2014.01.025 · Cited by 139 · see citing works
Elevated salivary levels of oxytocin persist more than 7 h after intranasal administration
van IJzendoorn, M. H., Bhandari, R., van der Veen, R., Grewen, K. M., & Bakermans-Kranenburg, M. J. (2012) · Frontiers in Neuroscience · doi:10.3389/fnins.2012.00174 · Cited by 137 · see citing works
Dissecting the Role of Oxytocin in the Formation and Loss of Social Relationships
Hurlemann, R., & Scheele, D. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.05.013 · Cited by 136 · see citing works
Boccia, M. L., Goursaud, A.-P. S., Bachevalier, J., Anderson, K. D., & Pedersen, C. A. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.05.009 · Cited by 136 · see citing works
Social Organization in a Wild Population of Callithrix jacchus
Digby, L. J., & Barreto, C. E. (1993) · Folia Primatologica · doi:10.1159/000156739 · Cited by 135 · see citing works
Oxytocin facilitates the sensation of social stress
Eckstein, M., Scheele, D., Weber, K., Stoffel‐Wagner, B., Maier, W., & Hurlemann, R. (2014) · Human Brain Mapping · doi:10.1002/hbm.22508 · Cited by 119 · see citing works
Rukstalis, M., & French, J. A. (2004) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.09.004 · Cited by 115 · see citing works
Song, Z., McCann, K. E., McNeill, J. K., Larkin, T. E., Huhman, K. L., & Albers, H. E. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.08.005 · Cited by 111 · see citing works
Smith, T. E., McGreer-Whitworth, B., & French, J. A. (1998) · Hormones and Behavior · doi:10.1006/hbeh.1998.1469 · Cited by 111 · see citing works
A novel form of oxytocin in New World monkeys
Lee, A. G., Cool, D. R., Grunwald, W. C., Neal, D. E., Buckmaster, C. L., Cheng, M. Y., Hyde, S. A., Lyons, D. M., & Parker, K. J. (2011) · Biology Letters · doi:10.1098/rsbl.2011.0107 · Cited by 91 · see citing works
Social organization in a wild population ofCallithrix jacchus: II. Intragroup social behavior
Digby, L. J. (1995) · Primates · doi:10.1007/bf02382859 · Cited by 90 · see citing works
Salubrious effects of oxytocin on social stress-induced deficits
Smith, A. S., & Wang, Z. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.11.010 · Cited by 88 · see citing works
Oxytocin changes primate paternal tolerance to offspring in food transfer
Saito, A., & Nakamura, K. (2011) · Journal of Comparative Physiology A · doi:10.1007/s00359-010-0617-2 · Cited by 86 · see citing works
Assessing Anxiety in Nonhuman Primates
Coleman, K., & Pierre, P. J. (2014) · ILAR Journal · doi:10.1093/ilar/ilu019 · Cited by 80 · see citing works
Cardoso, C., Ellenbogen, M. A., Serravalle, L., & Linnen, A. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.05.006 · Cited by 76 · see citing works
French, J. A., Brewer, K. J., Schaffner, C. M., Schalley, J., Hightower‐Merritt, D., Smith, T. E., & Bell, S. M. (1996) · American Journal of Primatology · doi:10.1002/(sici)1098-2345(1996)40:3 · Cited by 75 · see citing works
Cavanaugh, J., Mustoe, A. C., Taylor, J. H., & French, J. A. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.06.020 · Cited by 72 · see citing works
Self-citationThe Influence of Social Factors on the Response to Stress
Levine, S. (2010) · Psychotherapy and Psychosomatics · doi:10.1159/000288677 · Cited by 72 · see citing works
van den Burg, E. H., Stindl, J., Grund, T., Neumann, I. D., & Strauß, O. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.147 · Cited by 68 · see citing works
Oxytocin and vasopressin enhance responsiveness to infant stimuli in adult marmosets
Taylor, J. H., & French, J. A. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.10.002 · Cited by 68 · see citing works
Schaffner, C. M., Shepherd, R. E., Santos, C. V., & French, J. A. (1995) · American Journal of Primatology · doi:10.1002/ajp.1350360303 · Cited by 67 · see citing works
Self-citationShalev, I., Israel, S., Uzefovsky, F., Gritsenko, I., Kaitz, M., & Ebstein, R. P. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.04.005 · Cited by 65 · see citing works
Fernández‐Duque, E., Mason, W. A., & Mendoza, S. P. (1997) · American Journal of Primatology · doi:10.1002/(sici)1098-2345(1997)43:3 · Cited by 64 · see citing works
Do marmosets care to share? Oxytocin treatment reduces prosocial behavior toward strangers
Mustoe, A. C., Cavanaugh, J., Harnisch, A. M., Thompson, B. E., & French, J. A. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.04.015 · Cited by 59 · see citing works
Vargas-Pinilla, P., Paixão-Côrtes, V. R., Paré, P., Tovo-Rodrigues, L., Vieira, C. M. D. A. G., Xavier, A., Comas, D., Pissinatti, A., Sinigaglia, M., Rigo, M. M., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1419399112 · Cited by 59 · see citing works
Intensity of aggressive interactions modulates testosterone in male marmosets
Ross, C. N., French, J. A., & Patera, K. J. (2004) · Physiology & Behavior · doi:10.1016/j.physbeh.2004.08.036 · Cited by 54 · see citing works
Genetic Diversity in Oxytocin Ligands and Receptors in New World Monkeys
Ren, D., Lu, G., Moriyama, H., Mustoe, A. C., Harrison, E. B., & French, J. A. (2015) · PLOS ONE · doi:10.1371/journal.pone.0125775 · Cited by 47 · see citing works
Self-citationPharmacokinetics and disposition of the oxytocin receptor antagonist L-368,899 in rats and dogs.
Thompson, K. L., Vincent, S. H., Miller, R. R., Colletti, A. E., Alvaro, R. F., Wallace, M. A., Feeney, W. P., & Chiu, S. H. (1997) · PubMed · Cited by 41 · see citing works
Marmosets treated with oxytocin are more socially attractive to their long-term mate
Cavanaugh, J., Huffman, M. C., Harnisch, A. M., & French, J. A. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00251 · Cited by 36 · see citing works
Oxytocin reduces food sharing in capuchin monkeys by modulating social distance
Brosnan, S. F., Talbot, C. F., Essler, J. L., Leverett, K., Flemming, T., Dougall, P., Heyler, C., & Zak, P. J. (2015) · Behaviour · doi:10.1163/1568539x-00003268 · Cited by 30 · see citing works
Inglett, B. J., French, J. A., & Dethlefs, T. M. (1990) · Journal of comparative psychology · doi:10.1037/0735-7036.104.2.131 · Cited by 26 · see citing works
French, J. A., Smith, A. S., Gleason, A., Birnie, A. K., Mustoe, A. C., & Korgan, A. C. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.12.006 · Cited by 17 · see citing works
Wang (1997) · doi:10.1002/(sici)1098-2396(199709)27:1
Flagged first, then by citations
1 of the 72 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Freeman, S. M., & Young, L. J. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12382 · Cited by 196 · see citing works
“This compound is already being used in behavioural pharmacological studies in marmosets, including investigations of pair bonding and adult sociosexual behaviour (93,96,97), stress reactivity (98), and responsiveness to infant cues (99).”
BackgroundMeta-analysis of the effects of intranasal oxytocin on interpretation and expression of emotions
Leppanen, J., Ng, K. W., Tchanturia, K., & Treasure, J. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.04.010 · Cited by 188 · see citing works
Roles of Oxytocin in Stress Responses, Allostasis and Resilience
Takayanagi, Y., & Onaka, T. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms23010150 · Cited by 164 · see citing works
Rault, J., van den Munkhof, M. H., & Buisman‐Pijlman, F. T. A. (2017) · Frontiers in Psychology · doi:10.3389/fpsyg.2017.01521 · Cited by 118 · see citing works
Bales, K. L., Ardekani, C. S., Baxter, A., Karaskiewicz, C. L., Kuske, J. X., Lau, A. R., Savidge, L. E., Sayler, K. R., & Witczak, L. R. (2021) · Hormones and Behavior · doi:10.1016/j.yhbeh.2021.105062 · Cited by 108 · see citing works
Role of oxytocin in the control of stress and food intake
Onaka, T., & Takayanagi, Y. (2019) · Journal of Neuroendocrinology · doi:10.1111/jne.12700 · Cited by 98 · see citing works
Social Monogamy in Nonhuman Primates: Phylogeny, Phenotype, and Physiology
French, J. A., Cavanaugh, J., Mustoe, A. C., Carp, S. B., & Womack, S. L. (2017) · The Journal of Sex Research · doi:10.1080/00224499.2017.1339774 · Cited by 72 · see citing works
Neuropeptide diversity and the regulation of social behavior in New World primates
French, J. A., Taylor, J. H., Mustoe, A. C., & Cavanaugh, J. (2016) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2016.03.004 · Cited by 66 · see citing works
The Role of Oxytocin in Social Buffering: What Do Primate Studies Add?
Crockford, C., Deschner, T., & Wittig, R. M. (2017) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2017_12 · Cited by 49 · see citing works
Leppanen, J., Ng, K. W., Kim, Y.-R., Tchanturia, K., & Treasure, J. (2018) · Journal of Affective Disorders · doi:10.1016/j.jad.2017.08.041 · Cited by 45 · see citing works
Preis, A., Samuni, L., Mielke, A., Deschner, T., Crockford, C., & Wittig, R. M. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.07.009 · Cited by 42 · see citing works
Lopresti, A. L., Smith, S. J., & Drummond, P. D. (2021) · Nutritional Neuroscience · doi:10.1080/1028415x.2021.1892253 · Cited by 46 · see citing works
Stress, Well-Being and Reproductive Success
Edwards, K. L., Edes, A. N., & Brown, J. L. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-23633-5_5 · Cited by 43 · see citing works
Unified theory of Alzheimer’s disease (UTAD): implications for prevention and curative therapy
Nehls, M. (2016) · Journal of Molecular Psychiatry · doi:10.1186/s40303-016-0018-8 · Cited by 41 · see citing works
Oxytocin regulates reunion affiliation with a pairmate following social separation in marmosets
Cavanaugh, J., Mustoe, A. C., & French, J. A. (2018) · American Journal of Primatology · doi:10.1002/ajp.22750 · Cited by 41 · see citing works
Intranasal oxytocin modulates neural functional connectivity during human social interaction
Rilling, J. K., Chen, X., Chen, X., & Haroon, E. (2018) · American Journal of Primatology · doi:10.1002/ajp.22740 · Cited by 40 · see citing works
Sex differences in cognitive aging: a 4-year longitudinal study in marmosets
Rothwell, E. S., Workman, K. P., Wang, D., & Agnès Lacreuse, A. (2021) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2021.09.015 · Cited by 36 · see citing works
Neuroimaging and behavioral evidence of sex-specific effects of oxytocin on human sociality
Procyshyn, T. L., Dupertuys, J., & Bartz, J. A. (2024) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2024.06.010 · Cited by 29 · see citing works
Therapeutic uses of oxytocin in stress-related neuropsychiatric disorders
Zhang, S., Zhang, Y., Shi, D., & Wang, Z. (2023) · Cell & Bioscience · doi:10.1186/s13578-023-01173-6 · Cited by 28 · see citing works
Grebe, N. M., Sharma, A., Freeman, S. M., Palumbo, M. C., Patisaul, H. B., Bales, K. L., & Drea, C. M. (2021) · Scientific Reports · doi:10.1038/s41598-021-83342-6 · Cited by 26 · see citing works
Oxytocin structure and function in New World monkeys: from pharmacology to behavior
Mustoe, A. C., Taylor, J. H., & French, J. A. (2018) · Integrative Zoology · doi:10.1111/1749-4877.12318 · Cited by 25 · see citing works
Finkenwirth, C., & Burkart, J. M. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2018.02.050 · Cited by 22 · see citing works
Cooperation with closely bonded individuals reduces cortisol levels in long-tailed macaques
Stocker, M., Loretto, M., Sterck, E. H. M., Bugnyar, T., & Massen, J. J. M. (2020) · Royal Society Open Science · doi:10.1098/rsos.191056 · Cited by 20 · see citing works
Oxytocin treatment for alcoholism: Potential neurocircuitry targets
Peris, J., Steck, M. R., & Krause, E. G. (2020) · Neuropharmacology · doi:10.1016/j.neuropharm.2020.108091 · Cited by 21 · see citing works
Effects of aggressive temperament on endogenous oxytocin levels in adult titi monkeys
Witczak, L. R., Ferrer, E. E., & Bales, K. L. (2018) · American Journal of Primatology · doi:10.1002/ajp.22907 · Cited by 20 · see citing works
Faykoo-Martinez, M., Kalinowski, L., & Holmes, M. M. (2021) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2021.111360 · Cited by 18 · see citing works
Testing the effect of oxytocin on social grooming in bonobos
Brooks, J., Kano, F., Yeow, H., Morimura, N., & Yamamoto, S. (2022) · American Journal of Primatology · doi:10.1002/ajp.23444 · Cited by 19 · see citing works
Hayer, S. S., Conrin, M. E., French, J. A., Benson, A. K., Alvarez, S., Cooper, K. M., Fischer, A., Alsafwani, Z. W., Gasper, W., Haute, M. J. S. V., et al. (2024) · Gut Microbes · doi:10.1080/19490976.2024.2305476 · Cited by 22 · see citing works
He, Z., Hou, W., Hao, X., Dong, N., Du, P., Yuan, W., Yang, J., Jia, R., & Tai, F. (2017) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2017.06.020 · Cited by 19 · see citing works
Intranasal oxytocin affects the stress response to social isolation in sheep
Damián, J. P., de Soto, L., Espindola, D., Gil, J., & van Lier, E. (2020) · Physiology & Behavior · doi:10.1016/j.physbeh.2020.113282 · Cited by 16 · see citing works
Taylor, J. H., Intorre, A. A., & French, J. A. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00181 · Cited by 15 · see citing works
Razo, R. A., Vázquez, M. D. L. V., Turcanu, P., Legrand, M., Lau, A. R., Weinstein, T. A. R., Goetze, L. R., & Bales, K. L. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.877631 · Cited by 13 · see citing works
Awalt, S. L., Boghean, L., Klinkebiel, D. L., & Strasser, R. (2024) · Developmental Psychobiology · doi:10.1002/dev.22482 · Cited by 13 · see citing works
Nonhuman Primate Paternal Care: Species and Individual Differences in Behavior and Mechanisms
Ziegler, T. E., Tecot, S. R., Fernández‐Duque, E., Savage, A., & Snowdon, C. T. (2022) · Advances in neurobiology · doi:10.1007/978-3-030-97762-7_7 · Cited by 13 · see citing works
Oxytocin modulates mate-guarding behavior in marmoset monkeys
Cavanaugh, J., Mustoe, A. C., Womack, S. L., & French, J. A. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.10.009 · Cited by 12 · see citing works
Pierce, M. L., Mehrotra, S., Mustoe, A. C., French, J. A., & Murray, T. F. (2019) · Molecular Pharmacology · doi:10.1124/mol.118.114744 · Cited by 12 · see citing works
Intrahypothalamic effects of oxytocin on PVN CRH neurons in response to acute stress
Pati, D., Krause, E. G., & Frazier, C. J. (2022) · Current Opinion in Endocrine and Metabolic Research · doi:10.1016/j.coemr.2022.100382 · Cited by 10 · see citing works
Duarte, R. B., Maior, R. S., & Barros, M. (2017) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2017.12.005 · Cited by 10 · see citing works
Gnanadesikan, G. E., Bray, E. E., Cook, E. N., Levy, K., Douglas, L. E. L. C., Kennedy, B. S., Tecot, S. R., & MacLean, E. L. (2024) · Hormones and Behavior · doi:10.1016/j.yhbeh.2024.105612 · Cited by 6 · see citing works
Freeman, S. M. (2021) · Methods in molecular biology · doi:10.1007/978-1-0716-1759-5_7 · Cited by 7 · see citing works
Dopamine Modulation of Reunion Behavior in Short and Long Term Marmoset Pairs
Carp, S. B., Taylor, J. H., Womack, S. L., & French, J. A. (2018) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2018.00046 · Cited by 5 · see citing works
Agustí, C., Guix, L., Carbajal, A., Domingo, M., López‐Béjar, M., Manteca, X., & Talló-Parra, O. (2024) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2024.111793 · Cited by 4 · see citing works
Genomics for conservation: a case study of behavioral genes in the Tasmanian devil
Silver, L. W., Hogg, C. J., Wright, B. R., & Grueber, C. E. (2021) · Conservation Genetics · doi:10.1007/s10592-021-01354-1 · Cited by 4 · see citing works
Biological and Hormonal Approaches to the Evolution of Human-Canine Relationships
Wirobski, G., Lazzaroni, M., Marshall‐Pescini, S., & Range, F. (2023) · Nebraska Symposium on Motivation/The Nebraska symposium on motivation · doi:10.1007/978-3-031-29789-2_2 · Cited by 4 · see citing works
Witczak, L. R., Samra, J., Dufek, M. E., Goetze, L. R., Freeman, S. M., Lau, A. R., Rothwell, E. S., Savidge, L. E., Razo, R. A., BAXTER, A. B., et al. (2024) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.15119 · Cited by 4 · see citing works
Młotkowska, P., Marciniak, E., Misztal, A., & Misztal, T. (2023) · Animals · doi:10.3390/ani13101658 · Cited by 4 · see citing works
Agustí, C., Talló-Parra, O., Tejero-Caballo, E., García‐Párraga, D., López-Arjona, M., Álvaro‐Álvarez, T., Cerón, J. M. C., & Manteca, X. (2025) · Animals · doi:10.3390/ani15172628 · Cited by 3 · see citing works
Pierce, M. L., French, J. A., & Murray, T. F. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.109832 · Cited by 3 · see citing works
Serum Oxytocin, Cortisol and Social Behavior in Calves: A Study in the Impossible Task Paradigm
Pinelli, C., Scandurra, A., Mastellone, V., Iommelli, P., Musco, N., Pero, M. E., Lucrezia, A. D., Lotito, D., Tudisco, R., D’Aniello, B., et al. (2023) · Animals · doi:10.3390/ani13040646 · Cited by 3 · see citing works
Freeman, S. M., Catrow, J. L., Cox, J. E., Turano, A., Rich, M. A., Ihrig, H. P., Poudyal, N., Chang, C. T., Gese, E. M., Young, J. K., et al. (2024) · Comparative Medicine · doi:10.30802/aalas-cm-23-000044 · Cited by 2 · see citing works
Pereira, L. C., & Barros, M. (2020) · Brain Research · doi:10.1016/j.brainres.2020.147198 · Cited by 2 · see citing works
Grebe, N. M., Sheikh, A., Ohannessian, L., & Drea, C. M. (2023) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2023.106044 · Cited by 2 · see citing works
Hormonal and behavioural responses to visual social cues in common marmosets (Callithrix jacchus)
Correia‐Caeiro, C., Mouri, K., Huffman, M. A., Wilson, D. A., Wang, X., & Miyabe‐Nishiwaki, T. (2024) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2024.106177 · Cited by 1 · see citing works
Elkattawy, H. A., El-Sherbiny, M., Elsherbiny, N. M., Wahid, R. M., El-sayed, S. F., Henidi, H. A., El‐Gamal, R., Alshehri, S., & Asdaq, S. M. B. (2026) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2026.1742343 · Cited by 1 · see citing works
Vattem, N., Snyder, M., Leschinsky, A., Aziz, A., Amin, J., Butt, M., Aburas, J., & Pierce, M. L. (2026) · NeuroSci · doi:10.3390/neurosci7050100 · Cited by 1 · see citing works
Leeds, A., Schook, M. W., Dennis, P. M., Stoinski, T. S., Willis, M. A., & Lukas, K. E. (2022) · Primates · doi:10.1007/s10329-022-01037-6 · Cited by 1 · see citing works
Oxytocin’s role in the interaction between emotion and cognitive control
Ganzel, A. R., Shalev, H., Hochman, S., Zultan, R., Cohen, N., & Naparstek, S. (2025) · Biological Psychology · doi:10.1016/j.biopsycho.2025.109004 · Cited by 2 · see citing works
Oxytocin, Vasopressin, and Development of Social Behavior in Primates
Bales, K. L. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-804042-3.00094-4
Pharmacological Characterisation of Novel Oxytocin and Vasopressin Receptor Ligands
Gulliver, D. W. (2021) · The Sydney eScholarship Repository (The University of Sydney)
Grebe, N. M., Sheikh, A., Ohannessian, L., & Drea, C. M. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.09.14.507945
The Influence of Self-Adaptors on the Reduction of StressPreprint
Maki, K., & Sekine, K. (2024) · Research Square · doi:10.21203/rs.3.rs-4105150/v1
The impact of SERE training on selected neurotransmitter secretion in special forces soldiers
Grzesik, M., Łach, K., Brożyna, M., Przednówek, K., & Podgórski, R. (2025) · Scientific Reports · doi:10.1038/s41598-025-06270-9
Decoding dog communication through the physiology and behavior of urine marking
Quaranta, A., d’Ingeo, S., Minunno, M., Straziota, V., Nolè, M., Ventriglia, G., Ceci, E., & Siniscalchi, M. (2025) · Scientific Reports · doi:10.1038/s41598-025-31373-8
Agustí, C., Manteca, X., Almunia, J., López-Arjona, M., Cerón, J. M. C., Tejero, E. V., Câmara, N., Guix, L., & Talló-Parra, O. (2026) · Comparative Biochemistry and Physiology Part A Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2026.111993
- Authors
- Cavanaugh, J., Carp, S. B., Rock, C. M., & French, J. A.
- Affiliations
- University of Nebraska at Omaha (US)
- Corresponding author
- Cavanaugh, Jon
- Venue
- Psychoneuroendocrinology
- Publisher
- Elsevier BV
- Published
- 2016-04
- Volume
- 66
- Pages
- 22-30
- ISSN
- 0306-4530 (ISSN-L)
- PMC
- PMC6007987
- OpenAlex
- W2204722956
- Cited by
- 64
- References
- 72
- Citations by year
- 2026: 3 · 2025: 4 · 2024: 9 · 2023: 5 · 2022: 6 · 2021: 9 · 2020: 5 · 2019: 3 · 2018: 8 · 2017: 8 · 2016: 4
- FWCI
- 10.94
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Psychoneuroendocrinology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD 042882, R01HD042882, R56HD042882)
- 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
- oxytocin, social buffering, hypothalamic-pituitary-adrenal axis, cortisol, marmoset monkey, Callithrix jacchus, social isolation, psychogenic stress, oxytocin antagonist, proximity behavior, sex differences
- MeSH terms
- Adaptation, Physiological, Animals, Behavior, Animal, Callithrix, Female, Hormone Antagonists, Hydrocortisone, Hypothalamo-Hypophyseal System, Male, Oxytocin, Pituitary-Adrenal System, Social Behavior, Social Isolation, Stress, Psychological
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
