Neonatal melanocortin receptor agonist treatment reduces play fighting and promotes adult attachment in prairie voles in a sex-dependent manner

Barrett, Catherine E.; Modi, Meera E.; Zhang, Billy C.; Walum, Hasse; Inoue, Kiyoshi; Young, Larry J.

doi:10.1016/j.neuropharm.2014.05.041

Cited by 36Neuroendocrine regulation and behaviorNeuropeptides and Animal PhysiologyRegulation of Appetite and Obesity

Neonatal melanocortin receptor agonist treatment reduces play fighting and promotes adult attachment in prairie voles in a sex-dependent manner

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Barrett, Catherine E., Modi, Meera E., Zhang, Billy C., Walum, Hasse, Inoue, Kiyoshi, Young, Larry J.·2014·Neuropharmacology

DOI 10.1016/j.neuropharm.2014.05.041PMC PMC4158739

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Abstract

The melanocortin receptor (MCR) system has been studied extensively for its role in feeding and sexual behavior, but effects on social behavior have received little attention. α-MSH interacts with neural systems involved in sociality, including oxytocin, dopamine, and opioid systems. Acute melanotan-II (MTII), an MC3/4R agonist, potentiates brain oxytocin (OT) release and facilitates OT-dependent partner preference formation in socially monogamous prairie voles. Here we examined the long-term impact of early-life MCR stimulation on hypothalamic neuronal activity and social development in prairie voles. Male and female voles were given daily subcutaneous injections of 10 mg/kg MTII or saline between postnatal days (PND) 1-7. Neonatally-treated males displayed a reduction in initiated play fighting bouts as juveniles compared to control males. Neonatal exposure to MTII facilitated partner preference formation in adult females, but not males, after a brief cohabitation with an opposite-sex partner. Acute MTII injection elicited a significant burst of the immediate early gene EGR-1 immunoreactivity in hypothalamic OT, vasopressin, and corticotrophin releasing factor neurons, when tested in PND 6-7 animals. Daily neonatal treatment with 1 mg/kg of a more selective, brain penetrant MC4R agonist, PF44687, promoted adult partner preferences in both females and males compared with vehicle controls. Thus, developmental exposure to MCR agonists lead to a persistent change in social behavior, suggestive of structural or functional changes in the neural circuits involved in the formation of social relationships.

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Melanocortin receptor agonists facilitate OT-dependent partner preferences in prairie voles.
“facilitate OT-dependent partner preferences in prairie voles (35, 37, 39, 40)”
From Statistical and Methodological Considerations for the Interpretation of Intranasal Oxytocin Studies (2016) · cites this paper as [40]
Peripheral MT-II removes social behaviour deficits caused by neonatal social isolation in prairie voles.
“Peripheral MT-II administration also facilitates OT-dependent social bonding in prairie voles and eliminates the social behaviour deficits associated with neonatal social isolation in prairie voles (23,103,104).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [104]
Peripheral MT-II facilitates OT-dependent social bonding in prairie voles.
“Peripheral MT-II administration also facilitates OT-dependent social bonding in prairie voles and eliminates the social behaviour deficits associated with neonatal social isolation in prairie voles (23,103,104).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [104]
Early-life OT signaling, likely influenced by parental nurturing and attachment behaviors, can help establish the neural networks needed later in life to form adult social bonds.
“early-life OT signaling, which is likely influenced by parental nurturing and attachment behaviors, can help establish the neural networks needed later in life to form adult social bonds”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Barrett et al. 2014

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Targeted disruption of the melanocortin-4 receptor results in obesity in mice
Huszar, D., Lynch, C. A., Fairchild-Huntress, V., Dunmore, J. H., Fang, Q., Berkemeier, L. R., Gu, W., Kesterson, R. A., Boston, B. A., Cone, R. D., et al. (1997) · Cell · doi:10.1016/s0092-8674(00)81865-6 · Cited by 3,030 · see citing works
The neurobiology of pair bonding.
Young, L. J., & Wang, Z. (2004) · Nature Neuroscience · doi:10.1038/nn1327 · Cited by 1,523 · cited 3× · see citing works
“As pair bond formation requires social learning, attention to relevant social cues, and the drive to preferentially associate with a partner (Young and Wang, 2004), these changes in adult behavior would serve to promote social attachment.”
Self-citation
Inactivation of the mouse melanocortin-3 receptor results in increased fat mass and reduced lean body mass
Chen, A. S., Marsh, D. J., Trumbauer, M. E., Frazier, E. G., Guan, X.-M., Yu, H., Rosenblum, C. I., Vongs, A., Feng, Y., Cao, L., et al. (2000) · Nature Genetics · doi:10.1038/79254 · Cited by 896 · see citing works
Brain-derived neurotrophic factor regulates energy balance downstream of melanocortin-4 receptor
Xu, B., Goulding, E. H., Zang, K., Cepoi, D., Cone, R. D., Jones, K. R., Tecott, L. H., & Reichardt, L. F. (2003) · Nature Neuroscience · doi:10.1038/nn1073 · Cited by 896 · see citing works
Periadolescence: age-dependent behavior and psychopharmacological responsivity in rats
Spear, L. P., & Brake, S. C. (1983) · Developmental Psychobiology · doi:10.1002/dev.420160203 · Cited by 539 · see citing works
The Melanocortin-4 Receptor: Physiology, Pharmacology, and Pathophysiology
Tao, Y.-X. (2010) · Endocrine Reviews · doi:10.1210/er.2009-0037 · Cited by 531 · see citing works
Nucleus accumbens dopamine differentially mediates the formation and maintenance of monogamous pair bonds
Aragona, B. J., Liu, Y., Yu, Y. J., Curtis, J. T., Detwiler, J. M., Insel, T. R., & Wang, Z. (2006) · Nature Neuroscience · doi:10.1038/nn1613 · Cited by 473 · cited 2× · see citing works
“The socially monogamous, biparental prairie vole (Microtus ochrogaster) exhibits a complex repertoire of social behaviors that have been associated with oxytocin, dopamine, opioid, and CRF signaling (Young and Wang, 2004; Aragona et al., 2006; Lim et al., 2007; Bosch et al., 2009; Burkett et al., 2011), and provides a…”
Development of partner preferences in female prairie voles (Microtus ochrogaster): The role of social and sexual experience
WILLIAMS, J. (1992) · Hormones and Behavior · doi:10.1016/0018-506x(92)90004-f · Cited by 471 · see citing works
Social deprivation and play in rats
Panksepp, J., & Beatty, W. W. (1980) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(80)91077-8 · Cited by 409 · see citing works
Brain‐derived neurotrophic factor functions as a metabotrophin to mediate the effects of exercise on cognition
Gómez‐Pinilla, F., Vaynman, S., & Ying, Z. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06524.x · Cited by 379 · see citing works
Transgenic Mice Expressing Green Fluorescent Protein under the Control of the Melanocortin-4 Receptor Promoter
Liu, H., Kishi, T., Roseberry, A. G., Cai, X., Lee, C. E., Montez, J. M., Friedman, J. M., & Elmquist, J. K. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-18-07143.2003 · Cited by 375 · see citing works
Anhedonia requires MC4R-mediated synaptic adaptations in nucleus accumbens
Lim, B. K., Huang, K. W., Grueter, B. A., Rothwell, P. E., & Malenka, R. C. (2012) · Nature · doi:10.1038/nature11160 · Cited by 368 · see citing works
Influence of oxytocin on feeding behavior in the rat
Arletti, R., Benelli, A., & Bertolini, A. (1989) · Peptides · doi:10.1016/0196-9781(89)90082-x · Cited by 328 · see citing works
New aspects on the melanocortins and their receptors
Wikberg, J. E. S., Muceniece, R., Mandrika, I., Prūsis, P., Lindblom, J., Post, C., & Skottner, A. (2000) · Pharmacological Research · doi:10.1006/phrs.2000.0725 · Cited by 320 · see citing works
Neurophysin in the hypothalamo-neurohypophysial system. I. Production and characterization of monoclonal antibodies
Ben-Barak, Y., Russell, J., Whitnall, M., Ozato, K., & Gainer, H. (1985) · The Journal of Neuroscience · doi:10.1523/jneurosci.05-01-00081.1985 · Cited by 313 · see citing works
The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction
Burkett, J. P., & Young, L. J. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2794-x · Cited by 307 · cited 1× · see citing works
“In addition to impacting hypothalamic neuropeptide systems, MC4R signaling has been linked to dopaminergic and opioid-mediating reward and reinforcement systems, which are critically involved in pair bond formation (Burkett and Young, 2012).”
Self-citation
The prairie vole: An emerging model organism for understanding the social brain
McGraw, L. A., & Young, L. J. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2009.11.006 · Cited by 276 · see citing works
Self-citation
Interaction between α-Melanocyte-Stimulating Hormone and Corticotropin-Releasing Hormone in the Regulation of Feeding and Hypothalamo-Pituitary-Adrenal Responses
Lu, X., Barsh, G. S., Akil, H., & Watson, S. J. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-21-07863.2003 · Cited by 240 · see citing works
The impact of early life family structure on adult social attachment, alloparental behavior, and the neuropeptide systems regulating affiliative behaviors in the monogamous prairie vole (Microtus ochrogaster)
Ahern, T. H. (2009) · Frontiers in Behavioral Neuroscience · doi:10.3389/neuro.08.017.2009 · Cited by 239 · see citing works
ACTH-(1–24) and α-MSH antagonize feeding behavior stimulated by kappa opiate agonists
Poggioli, R., Vergoni, A. V., & Bertolini, A. (1986) · Peptides · doi:10.1016/0196-9781(86)90104-x · Cited by 237 · see citing works
The CRF system mediates increased passive stress-coping behavior following the loss of a bonded partner in a monogamous rodent
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
Self-citation
Sex differences and developmental effects of oxytocin on aggression and social behavior in prairie voles (Microtus ochrogaster)
Bales, K. L., & Carter, C. S. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(03)00154-5 · Cited by 195 · see citing works
Identifying key features of early stressful experiences that produce stress vulnerability and resilience in primates
Parker, K. J., & Dario Maestripieri, A. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.09.003 · Cited by 192 · see citing works
Oxytocin has dose-dependent developmental effects on pair-bonding and alloparental care in female prairie voles
Bales, K. L., van Westerhuyzen, J. A., Lewis-Reese, A. D., Grotte, N. D., Lanter, J. A., & Carter, C. S. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.05.004 · Cited by 192 · see citing works
Maternal separation enhances offensive play-fighting, basal corticosterone and hypothalamic vasopressin mRNA expression in juvenile male rats
Veenema, A. H., & Neumann, I. D. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2008.10.017 · Cited by 191 · see citing works
α-Melanocyte-Stimulating Hormone Stimulates Oxytocin Release from the Dendrites of Hypothalamic Neurons While Inhibiting Oxytocin Release from Their Terminals in the Neurohypophysis
Sabatier, N., Caquineau, C., Dayanithi, G., Bull, P., Douglas, A. J., Guan, X. M. M., Jiang, M., Van der Ploeg, L., & Leng, G. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-32-10351.2003 · Cited by 190 · see citing works
Oxytocin-induced penile erection and yawning: site of action in the brain
Melis, M. R., Argiolas, A., & Gessa, G. L. (1986) · Brain Research · doi:10.1016/0006-8993(86)91485-x · Cited by 190 · see citing works
Consequences of Early Experiences and Exposure to Oxytocin and Vasopressin Are Sexually Dimorphic
Carter, C. S., Boone, E. M., Pournajafi-Nazarloo, H., & Bales, K. L. (2009) · Developmental Neuroscience · doi:10.1159/000216544 · Cited by 176 · see citing works
The influence of natural variations in maternal care on play fighting in the rat
Parent, C. I., & Meaney, M. J. (2008) · Developmental Psychobiology · doi:10.1002/dev.20342 · Cited by 175 · see citing works
Developmental exposure to oxytocin facilitates partner preferences in male prairie voles (Microtus ochrogaster)
Bales, K. L., & Carter, C. S. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.4.854 · Cited by 155 · see citing works
Interaction of dual intracellular signaling pathways activated by the melanocortin-3 receptor.
Konda, Y., Gantz, I., DelValle, J., Shimoto, Y., Miwa, H., & Yamada, T. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)36813-8 · Cited by 154 · see citing works
Increasing oxytocin receptor expression in the nucleus accumbens of pre-pubertal female prairie voles enhances alloparental responsiveness and partner preference formation as adults
Keebaugh, A. C., & Young, L. J. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.07.018 · Cited by 154 · see citing works
Self-citation
Maternal Deprivation and Stress Induce Immediate Early Genes in the Infant Rat Brain
Smith, M. A., Kim, S.-Y., van Oers, H. J. J., & Levine, S. D. (1997) · Endocrinology · doi:10.1210/endo.138.11.5529 · Cited by 151 · see citing works
An investigation of individual, age and sexual differences in the play of <i>Rattus norvegicus</i> (Mammalia: Rodentia)
Poole, T. B., & Fish, J. (1976) · Journal of Zoology · doi:10.1111/j.1469-7998.1976.tb02294.x · Cited by 149 · see citing works
Morphine down-regulates melanocortin-4 receptor expression in brain regions that mediate opiate addiction.
Alvaro, J. D., Tatro, J. B., Quillan, J. M., Fogliano, M., Eisenhard, M. E., Lerner, M. R., Nestler, E. J., & Duman, R. S. (1996) · Molecular Pharmacology · doi:10.1016/s0026-895x(25)09317-4 · Cited by 140 · see citing works
Activation of μ-Opioid Receptors in the Dorsal Striatum is Necessary for Adult Social Attachment in Monogamous Prairie Voles
Burkett, J. P., Spiegel, L. L., Inoue, K., Murphy, A. Z., & Young, L. J. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2011.117 · Cited by 133 · see citing works
Self-citation
ACTH- and α-MSH-induced grooming, stretching, yawning and penile erection in male rats: Site of action in the brain and role of melanocortin receptors
Argiolas, A., Melis, M. R., Murgia, S., & Schiöth, H. B. (2000) · Brain Research Bulletin · doi:10.1016/s0361-9230(99)00270-1 · Cited by 132 · see citing works
Early interactions with mother and peers independently build adult social skills and shape BDNF and oxytocin receptor brain levels
Branchi, I., Curley, J. P., D’Andrea, I., Cirulli, F., Champagne, F. A., & Alleva, E. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.07.010 · Cited by 131 · see citing works
Patterns of Induction of the Immediate-Early Genes c-fos and egr-1 in the Female Rat Brain following Differential Amounts of Mating Stimulation
Polston, E. K., & Erskine, M. S. (2008) · Neuroendocrinology · doi:10.1159/000127027 · Cited by 130 · see citing works
Corticotropin (ACTH) acts directly on amygdala neurons to down‐regulate corticotropin‐releasing hormone gene expression
Brunson, K. L., Khan, N., Eghbal-Ahmadi, M., & Baram, T. Z. (2001) · Annals of Neurology · doi:10.1002/ana.66 · Cited by 129 · see citing works
Developmental exposure to vasopressin increases aggression in adult prairie voles
Stribley, J. M., & Carter, C. S. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.22.12601 · Cited by 124 · see citing works
Influence of neonatal injections of α-MSH on learning, memory and attention in rats
Beckwith, B. E., Sandman, C. A., Hothersall, D., & Kastin, A. J. (1977) · Physiology & Behavior · doi:10.1016/0031-9384(77)90095-6 · Cited by 121 · see citing works
Involvement of melanocortin-4 receptor in anxiety and depression
Chaki, S., & Okuyama, S. (2005) · Peptides · doi:10.1016/j.peptides.2004.11.029 · Cited by 116 · see citing works
Distribution and Function of Melanocortin Receptors within the Brain
Mountjoy, K. G. (2010) · Advances in experimental medicine and biology · doi:10.1007/978-1-4419-6354-3_3 · Cited by 114 · see citing works
The MC4 receptor mediates α-MSH induced release of nucleus accumbens dopamine
Lindblom, J., Opmane, B., Mutulis, F., Mutule, I., Petrovska, R., Klusa, V. Z., Bergström, L., & Wikberg, J. E. S. (2001) · Neuroreport · doi:10.1097/00001756-200107200-00022 · Cited by 105 · see citing works
α‐MSH and the Regulation of Melanocyte Function
Thody, A. J. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb08679.x · Cited by 102 · see citing works
CRF receptors in the nucleus accumbens modulate partner preference in prairie voles
Lim, M. M., Liu, Y., Ryabinin, A. E., Bai, Y., Wang, Z., & Young, L. J. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2007.01.006 · Cited by 99 · see citing works
Self-citation
Variation in maternal care and individual differences in play, exploration, and grooming of juvenile Norway rat offspring
Moore, C., & Power, K. L. (1992) · Developmental Psychobiology · doi:10.1002/dev.420250303 · Cited by 98 · see citing works
Oxytocin-induced facilitation of lordosis behaviour in rats is progesterone-dependent
Gorzalka, B. B. (1987) · Neuropeptides · doi:10.1016/0143-4179(87)90089-8 · Cited by 97 · see citing works
Melanocortin-4 Receptor Regulates Hippocampal Synaptic Plasticity through a Protein Kinase A-Dependent Mechanism
Shen, Y., Fu, W., Cheng, E. Y. L., Fu, A. K. Y., & Ip, N. Y. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.3282-12.2013 · Cited by 96 · see citing works
Blockade of melanocortin transmission inhibits cocaine reward
Hsu, R., Taylor, J. R., Newton, S. S., Alvaro, J. D., Haile, C. N., Han, G. U., Hruby, V. J., Nestler, E. J., & Duman, R. S. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04038.x · Cited by 94 · see citing works
Fighting in juvenile rats and the ontogeny of agonistic behavior.
Taylor, G. T. (1980) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077816 · Cited by 88 · see citing works
Melanocortin-4 receptor activation stimulates hypothalamic brain-derived neurotrophic factor release to regulate food intake, body temperature and cardiovascular function
Nicholson, J. R., Peter, J. ‐., Lecourt, A. ‐., Barde, Y. ‐., & Hofbauer, K. G. (2007) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2007.01610.x · Cited by 87 · see citing works
Melanocortin receptor agonists facilitate oxytocin-dependent partner preference formation in the Prairie Vole
Modi, M. E., Inoue, K., Barrett, C. E., Kittelberger, K. A., Smith, D. G., Landgraf, R., & Young, L. J. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.35 · Cited by 82 · see citing works
Self-citation
Melanocortin-4 receptor in the medial amygdala regulates emotional stress-induced anxiety-like behaviour, anorexia and corticosterone secretion
Liu, J., Garza, J. C., Li, W., & Lu, X. (2011) · The International Journal of Neuropsychopharmacology · doi:10.1017/s146114571100174x · Cited by 82 · see citing works
Social environment regulates corticotropin releasing factor, corticosterone and vasopressin in juvenile prairie voles
Ruscio, M. G., Sweeny, T., Hazelton, J., Suppatkul, P., & Sue Carter, C. (2007) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.08.004 · Cited by 81 · see citing works
Play-solicitation behavior in juvenile male and female rats
Thor, D. H., & Holloway, W. R. (1983) · Animal Learning & Behavior · doi:10.3758/bf03199645 · Cited by 80 · see citing works
Developmental effects of oxytocin on stress response: Single versus repeated exposure
KRAMER, K., CUSHING, B., & CARTER, C. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00175-6 · Cited by 79 · see citing works
Evaluation of two automated metrics for analyzing partner preference tests
Ahern, T. H., Modi, M. E., Burkett, J. P., & Young, L. J. (2009) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2009.06.010 · Cited by 79 · see citing works
Self-citation
Postnatal Ablation of POMC Neurons Induces an Obese Phenotype Characterized by Decreased Food Intake and Enhanced Anxiety-Like Behavior
Greenman, Y., Kuperman, Y., Drori, Y., Asa, S. L., Navon, I., Forkosh, O., Gil, S., Stern, N., & Chen, A. (2013) · Molecular Endocrinology · doi:10.1210/me.2012-1344 · Cited by 78 · see citing works
The Hypothalamic Melanocortin System Stimulates the Hypothalamo-Pituitary-Adrenal Axis in vitro and in vivo in Male Rats
Dhillo, W. S., Small, C. J., Seal, L., Kim, M.-S., Stanley, S. A., Murphy, K. G., Ghatei, M. A., & Bloom, S. R. (2002) · Neuroendocrinology · doi:10.1159/000054712 · Cited by 71 · see citing works
Suckling and genital stroking induces Fos expression in hypothalamic oxytocinergic neurons of rabbit pups
Caba, M., Rovirosa-Hernández, M. D. J., & Silver, R. (2003) · Developmental Brain Research · doi:10.1016/s0165-3806(03)00064-6 · Cited by 65 · see citing works
Effects of hormonal, sexual, and social history on mating and pair bonding in prairie voles
Carter, C. S., Witt, D. M., Thompson, E. G., & Carlstead, K. (1988) · Physiology & Behavior · doi:10.1016/0031-9384(88)90049-2 · Cited by 64 · see citing works
Conformation of the Core Sequence in Melanocortin Peptides Directs Selectivity for the Melanocortin MC3 and MC4 Receptors
Oosterom, J., Nijenhuis, W. A. J., Schaaper, W. M. M., Slootstra, J. W., Meloen, R. H., Gispen, W. H., Burbach, J. P. H., & Adan, R. A. H. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.24.16853 · Cited by 59 · see citing works
Melanocortins and opiate addiction
Alvaro, J. D., Tatro, J. B., & Duman, R. S. (1997) · Life Sciences · doi:10.1016/s0024-3205(97)00029-5 · Cited by 57 · see citing works
α‐Melanocyte‐Stimulating Hormone and Oxytocin: A Peptide Signalling Cascade in the Hypothalamus
Sabatier, N. (2006) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2006.01464.x · Cited by 54 · see citing works
The effects of neonatal injections of α-MSH on the open-field behavior of juvenile and adult rats
Beckwith, B. E., O’quin, R. K., Petro, M. S., Kastin, A. J., & Sandman, C. A. (1977) · Physiological Psychology · doi:10.3758/bf03335334 · Cited by 53 · see citing works
Male-female interactions in prairie voles
Gavish, L. Y., Carter, C. S., & Getz, L. L. (1983) · Animal Behaviour · doi:10.1016/s0003-3472(83)80073-6 · Cited by 51 · see citing works
Effects of neonatal cerebral ventricular injection of ACTH 4–9 and subsequent adult injections on learning in male and female albino rats
Champney, T. F., Sahley, T. L., & Sandman, C. A. (1976) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(76)90321-x · Cited by 50 · see citing works
Functional Selectivity of Melanocortin 4 Receptor Peptide and Nonpeptide Agonists: Evidence for Ligand-Specific Conformational States
Nickolls, S. A., Fleck, B. A., Hoare, S. R. J., & Maki, R. A. (2005) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.105.083337 · Cited by 49 · see citing works
Discovery of a Selective Small-Molecule Melanocortin-4 Receptor Agonist with Efficacy in a Pilot Study of Sexual Dysfunction in Humans
Lansdell, M. I., Hepworth, D., Calabrese, A. A., Brown, A. D., Blagg, J., Burring, D. J., Wilson, P., Fradet, D., Brown, T. B., Quinton, F., et al. (2010) · Journal of Medicinal Chemistry · doi:10.1021/jm9017866 · Cited by 43 · see citing works
The melanocortin agonist, melanotan II, enhances proceptive sexual behaviors in the female rat
Rössler, A., Pfaus, J. G., Kia, H. K., Bernabé, J., Alexandre, L., & Giuliano, F. (2006) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2006.09.023 · Cited by 43 · see citing works
Paternal deprivation alters play-fighting, serum corticosterone and the expression of hypothalamic vasopressin and oxytocin in juvenile male mandarin voles
Wang, J., Tai, F., Yan, X., & Yu, P. (2012) · Journal of Comparative Physiology A · doi:10.1007/s00359-012-0748-8 · Cited by 39 · see citing works
Melanocortinergic Activation by Melanotan II Inhibits Feeding and Increases Uncoupling Protein 1 Messenger Ribonucleic Acid in the Developing Rat
Glavas, M. M., Joachim, S. E., Draper, S. J., Smith, M. S., & Grove, K. L. (2007) · Endocrinology · doi:10.1210/en.2007-0184 · Cited by 39 · see citing works
Chronic infusion of a melanocortin receptor agonist modulates dopamine receptor binding in the rat brain
Lindblom, J., Kask, A., Hägg, E., Härmark, L., Bergström, L., & Wikberg, J. E. S. (2002) · Pharmacological Research · doi:10.1006/phrs.2001.0913 · Cited by 38 · see citing works
Alpha MSH-induced excessive grooming behavior involves a GABAergic mechanism
de Barioglio, S. R., Lezcano, N. E., & Celis, M. E. (1991) · Peptides · doi:10.1016/0196-9781(91)90189-v · Cited by 31 · see citing works
Neonatal manipulation of oxytocin influences female reproductive behavior and success
Cushing, B. S., Levine, K., & Cushing, N. L. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2004.08.004 · Cited by 31 · see citing works
Alpha-MSH stimulates neurite outgrowth of neonatal rat corticospinal neurons in vitro
Joosten, E. A. J., Verhaagh, S., Martin, D., Robe, P. A. J. T., Franzen, R., Hooiveld, M. J. J., Doornbos, R. P., Bär, P. R., & Moonen, G. (1996) · Brain Research · doi:10.1016/0006-8993(96)00700-7 · Cited by 27 · see citing works
ACTH neuromodulation of the developing motor system and neonatal learning in the rat
Acker, G. R., Berran, J., & Strand, F. L. (1985) · Peptides · doi:10.1016/0196-9781(85)90133-0 · Cited by 27 · see citing works
Maternal Touch Moderates Sex Differences in Juvenile Social Play Behavior
Edelmann, M. N., Demers, C. H., & Auger, A. P. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057396 · Cited by 27 · cited 1× · see citing works
“A similar phenomenon is found in male rats with altered early care, as high levels of licking and grooming or a simulated tactile stimulation regime reduce juvenile play (Moore and Power, 1992; Parent andMeaney, 2008; Edelmann et al., 2013).”
Is Play Behavior Sexually Dimorphic in Monogamous Species?
Chau, M. J., Stone, A. I., Mendoza, S. P., & Bales, K. L. (2008) · Ethology · doi:10.1111/j.1439-0310.2008.01543.x · Cited by 21 · see citing works
Behavioral Depression: Opposite Effects of Neonatal Dexamethasone and ACTH-(4-9) Analogue (ORG 2766) Treatments in the Rat
Felszeghy, K., Sasvári, M., & Nyakas, C. J. (1993) · Hormones and Behavior · doi:10.1006/hbeh.1993.1028 · Cited by 20 · see citing works
Functional Evaluation of THIQ, a Melanocortin 4 Receptor Agonist, in Models of Food Intake and Inflammation
Muceniece, R., Zvejniece, L., Vilšķe̅rsts, R., Liepinsh, E., Baumane, L., Kalvinsh, I., Wikberg, J. E. S., & Dambrova, M. (2007) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/j.1742-7843.2007.00133.x · Cited by 20 · see citing works
Differentiation of rat hypothalamic dopaminergic neurons is stimulated in vitro by target cells: the melanotrophs
Egles, C., René, Varón, Louis, L., Felix, F., & Schimchowitsch (1998) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1998.00138.x · Cited by 8 · see citing works
Peripherally administered desacetyl α-MSH and α-MSH both influence postnatal rat growth and associated rat hypothalamic protein expression
Wu, C., Greenwood, D. R., Cooney, J. M., Jensen, D. J. A., Tatnell, M. A., Cooper, G. J. S., & Mountjoy, K. G. (2006) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00480.2005 · Cited by 2 · see citing works

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1 of the 86 references couldn’t be matched to a known paper.

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The oxytocin receptor: from intracellular signaling to behavior
Jurek, B., & Neumann, I. D. (2018) · Physiological Reviews · doi:10.1152/physrev.00031.2017 · Cited by 999 · see citing works
The biology of mammalian parenting and its effect on offspring social development
Rilling, J. K., & Young, L. J. (2014) · Science · doi:10.1126/science.1252723 · Cited by 452 · see citing works
Self-citation
Exogenous and evoked oxytocin restores social behavior in the <i>Cntnap2</i> mouse model of autism
Peñagarikano, O., Lázaro, M. T., Lu, X.-H., Gordon, A., Dong, H., Lam, H. A., Peles, E., Maidment, N. T., Murphy, N. P., Yang, X. W., et al. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.3010257 · Cited by 378 · see citing works
Statistical and Methodological Considerations for the Interpretation of Intranasal Oxytocin Studies
Walum, H., Waldman, I. D., & Young, L. J. (2016) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.06.016 · Cited by 345 · see citing works
Self-citation
Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications
Freeman, S. M., & Young, L. J. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12382 · Cited by 196 · see citing works
Self-citation
Can oxytocin treat autism?
Young, L. J., & Barrett, C. E. (2015) · Science · doi:10.1126/science.aaa8120 · Cited by 200 · see citing works
Self-citation
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
Self-citation
Oxytocin and Social Relationships: From Attachment to Bond Disruption
Bosch, O. J., & Young, L. J. (2017) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2017_10 · Cited by 162 · see citing works
Self-citation
RNAi knockdown of oxytocin receptor in the nucleus accumbens inhibits social attachment and parental care in monogamous female prairie voles
Keebaugh, A. C., Barrett, C. E., Laprairie, J. L., Jenkins, J. J., & Young, L. J. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1040893 · Cited by 150 · see citing works
Self-citation
The oxytocin system promotes resilience to the effects of neonatal isolation on adult social attachment in female prairie voles
Barrett, C. E., Arambula, S. E., & Young, L. J. (2015) · Translational Psychiatry · doi:10.1038/tp.2015.73 · Cited by 115 · see citing works
Self-citation
Evolution of sex-specific pace-of-life syndromes: genetic architecture and physiological mechanisms
Immonen, E., Hämäläinen, A., Schuett, W., & Tarka, M. (2018) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-018-2462-1 · Cited by 93 · see citing works
Bench-top to clinical therapies: A review of melanocortin ligands from 1954 to 2016
Ericson, M. D., Lensing, C. J., Fleming, K. A., Schlasner, K. N., Doering, S. R., & Haskell‐Luevano, C. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2017.03.020 · Cited by 86 · see citing works
Melanocortin receptor agonists facilitate oxytocin-dependent partner preference formation in the Prairie Vole
Modi, M. E., Inoue, K., Barrett, C. E., Kittelberger, K. A., Smith, D. G., Landgraf, R., & Young, L. J. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.35 · Cited by 82 · see citing works
Self-citation
Rebalancing the Addicted Brain: Oxytocin Interference with the Neural Substrates of Addiction
Bowen, M. T., & Neumann, I. D. (2017) · Trends in Neurosciences · doi:10.1016/j.tins.2017.10.003 · Cited by 83 · see citing works
Oxytocin, social cognition and psychiatry
Young, L. J. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2014.186 · Cited by 64 · see citing works
Self-citation
Targeting the Oxytocin System: New Pharmacotherapeutic Approaches
Gulliver, D. W., Werry, E. L., Reekie, T. A., Katte, T. A., Jorgensen, W. T., & Kassiou, M. (2018) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2018.11.001 · Cited by 63 · see citing works
Severity of eating disorder symptoms related to oxytocin receptor polymorphisms in anorexia nervosa
Acevedo, S. F., Valencia, C., Lutter, M. L., & McAdams, C. J. (2015) · Psychiatry Research · doi:10.1016/j.psychres.2015.05.040 · Cited by 44 · see citing works
An in Vitro and in Vivo Investigation of Bivalent Ligands That Display Preferential Binding and Functional Activity for Different Melanocortin Receptor Homodimers
Lensing, C. J., Freeman, K. T., Schnell, S. M., Adank, D. N., Speth, R. C., & Haskell‐Luevano, C. (2016) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.5b01894 · Cited by 44 · see citing works
Nanoparticle encapsulated oxytocin increases resistance to induced seizures and restores social behavior in Scn1a-derived epilepsy
Wong, J. C., Shapiro, L. E., Thelin, J. T., Heaton, E. C., Zaman, R. U., D’Souza, M. J., Murnane, K. S., & Escayg, A. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.105147 · Cited by 39 · see citing works
Developing a Biased Unmatched Bivalent Ligand (BUmBL) Design Strategy to Target the GPCR Homodimer Allosteric Signaling (cAMP over β-Arrestin 2 Recruitment) Within the Melanocortin Receptors
Lensing, C. J., Freeman, K. T., Schnell, S. M., Speth, R. C., Zarth, A. T., & Haskell‐Luevano, C. (2018) · Journal of Medicinal Chemistry · doi:10.1021/acs.jmedchem.8b00238 · Cited by 25 · see citing works
Melanocortin-4 receptor regulation of pain
Li, Z., Liu, B., He, Z., & Xiang, H. (2017) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2017.05.021 · Cited by 23 · see citing works
A Direct in Vivo Comparison of the Melanocortin Monovalent Agonist Ac-His-DPhe-Arg-Trp-NH2 versus the Bivalent Agonist Ac-His-DPhe-Arg-Trp-PEDG20-His-DPhe-Arg-Trp-NH2: A Bivalent Advantage
Lensing, C. J., Adank, D. N., Wilber, S. L., Freeman, K. T., Schnell, S. M., Speth, R. C., Zarth, A. T., & Haskell‐Luevano, C. (2017) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.6b00399 · Cited by 18 · see citing works
MC4R expression in pedunculopontine nucleus involved in the modulation of midbrain dopamine system.
Hao, Y., Tian, X., Liu, T., Liu, C., Xiang, H., & Zhang, J. (2015) · Europe PMC (PubMed Central) · Cited by 14 · see citing works
The Neurobiology and Genetics of Affiliation and Social Bonding in Animal Models
Donaldson, Z. R., & Young, L. J. (2016) · Springer eBooks · doi:10.1007/978-1-4939-3777-6_4 · Cited by 11 · see citing works
Self-citation
Effect of Melanotan‐II on Brain Fos Immunoreactivity and Oxytocin Neuronal Activity and Secretion in Rats
Paiva, L., Sabatier, N., Leng, G., & Ludwig, M. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12454 · Cited by 11 · see citing works
Functional Interaction between the Dopamine and Melanocortin Systems of the Brain
Derkach, K. V., Romanova, I. V., & Shpakov, A. O. (2018) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-018-0554-z · Cited by 8 · see citing works
Editorial: Oxytocin's routes in social behavior: into the 21st century
Andari, E. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00224 · Cited by 6 · see citing works
Amphetamine exposure alters behaviors, and neuronal and neurochemical activation in the brain of female prairie voles
Liu, Y., Pan, Y., Curtis, T. J., & Wang, Z. (2022) · Neuroscience · doi:10.1016/j.neuroscience.2022.06.033 · Cited by 5 · see citing works
Melanocortin agonism in a social context selectively activates nucleus accumbens in an oxytocin-dependent manner
Ford, C. L., McDonough, A. A., Horie, K., & Young, L. J. (2024) · Neuropharmacology · doi:10.1016/j.neuropharm.2024.109848 · Cited by 4 · see citing works
Self-citation
Is Infidelity Biologically Determined?
Balon, R. (2016) · Current Sexual Health Reports · doi:10.1007/s11930-016-0084-z · Cited by 3 · see citing works
Is Infidelity Biologically Determined?
Balon, R. (2015) · European Psychiatry · doi:10.1016/s0924-9338(15)30061-4 · Cited by 1 · see citing works
Nature and Nurture in Parental Care
Royle, N. J., & Moore, A. J. (2019) · doi:10.1002/9781119313663.ch7 · Cited by 1 · see citing works
Discovery of Peptide and Peptidomimetic Based Ligands Targeting the Melanocortin Receptors: A campaign in mixture-based positional scanning, chemical topology, and structure-activity relationships
Doering, S. R. (2016) · University of Minnesota Digital Conservancy (University of Minnesota)
Preconception Exposure to Chronic Stressors Impairs Social Behaviors in Prairie Vole Offspring ( Microtus ochrogaster ): Partial Mediation by Parental Pair‐Bonding and Parenting Behaviors
Watanasriyakul, W. T. (2026) · Developmental Psychobiology · doi:10.1002/dev.70158
BindingDB Entry 50047392: An in Vitro and in Vivo Investigation of Bivalent Ligands That Display Preferential Binding and Functional Activity for Different Melanocortin Receptor Homodimers.
BindingDB (2017) · UC San Diego · doi:10.7270/q2r2139s
BindingDB Entry 50006771: Developing a Biased Unmatched Bivalent Ligand (BUmBL) Design Strategy to Target the GPCR Homodimer Allosteric Signaling (cAMP over β-Arrestin 2 Recruitment) Within the Melanocortin Receptors.
BindingDB (2021) · UC San Diego · doi:10.7270/q2vh5s39

Melanocortin receptor agonists facilitate oxytocin-dependent partner preference formation in the Prairie Vole
Modi, M. E., Inoue, K., Barrett, C. E., Kittelberger, K. A., Smith, D. G., Landgraf, R., & Young, L. J. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.35 · Cited by 82 · see citing works
Self-citation
Neonatal manipulation of oxytocin influences the partner preference in mandarin voles (Microtus mandarinus)
Jia, R., Tai, F., An, S., Broders, H., & Sun, R. (2008) · Neuropeptides · doi:10.1016/j.npep.2008.06.001 · Cited by 35 · see citing works
Developmental exposure to oxytocin facilitates partner preferences in male prairie voles (Microtus ochrogaster)
Bales, K. L., & Carter, C. S. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.4.854 · Cited by 155 · see citing works
Neonatal oxytocin manipulations have long-lasting, sexually dimorphic effects on vasopressin receptors
Bales, K. L., Plotsky, P. M., Young, L. J., Lim, M. M., Grotte, N., Ferrer, E., & Carter, C. S. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2006.09.009 · Cited by 150 · see citing works
Self-citation
Melanocortin agonism in a social context selectively activates nucleus accumbens in an oxytocin-dependent manner
Ford, C. L., McDonough, A. A., Horie, K., & Young, L. J. (2024) · Neuropharmacology · doi:10.1016/j.neuropharm.2024.109848 · Cited by 4 · see citing works
Self-citation

Authors: Barrett, C. E., Modi, M. E., Zhang, B. C., Walum, H., Inoue, K., & Young, L. J.
Affiliations: Emory University (US)
Corresponding author: Barrett, Catherine E.
ORCID: Barrett, Catherine E.
Zhang, Billy C.
Inoue, Kiyoshi
Young, Larry J.
Venue: Neuropharmacology
Publisher: Elsevier BV
Published: 2014-10
Volume: 85
Pages: 357-366
ISSN: 0028-3908 (ISSN-L)
DOI: 10.1016/j.neuropharm.2014.05.041
PMC: PMC4158739
OpenAlex: W1986596088
Cited by: 34
References: 86
Citations by year: 2026: 1 · 2024: 1 · 2022: 1 · 2020: 1 · 2019: 1 · 2018: 5 · 2017: 5 · 2016: 6 · 2015: 11 · 2014: 2
FWCI: 12.36
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neuropharmacology (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: Autism Speaks (AS7745)
Pfizer
National Institutes of Health (P51OD011132)
Yerkes National Primate Research Center, Emory University
National Institute of Mental Health (R01MH096983)
Topics: Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
Keywords: melanocortin receptors, melanotan II, Microtus ochrogaster, social behavior, mate preferences, play fighting, adult attachment, oxytocin, vasopressin, corticotropin-releasing factor, EGR1, hypothalamus, sex differences, MC4R agonist, social monogamy
MeSH terms: Aggression, alpha-MSH, Animals, Animals, Newborn, Behavior, Animal, Arvicolinae, Female, Hypothalamus, Male, Neurons, Pair Bond, Peptides, Cyclic, Play and Playthings, Psychotropic Drugs, Random Allocation, Sex Characteristics, Receptor, Melanocortin, Type 3, Receptor, Melanocortin, Type 4, Early Growth Response Protein 1

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Neonatal melanocortin receptor agonist treatment reduces play fighting and promotes adult attachment in prairie voles in a sex-dependent manner

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