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κ-Opioid Receptors within the Nucleus Accumbens Shell Mediate Pair Bond Maintenance
Open accessAbstract
The prairie vole is a socially monogamous species in which breeder pairs typically show strong and selective pair bonds. The establishment of a pair bond is associated with a behavioral transition from general affiliation to aggressive rejection of novel conspecifics. This “selective aggression” is indicative of mate guarding that is necessary to maintain the initial pair bond. In the laboratory, the neurobiology of this behavior is studied using resident-intruder testing. Although it is well established that social behaviors in other species are mediated by endogenous opioid systems, opiate regulation of pair bond maintenance has never been studied. Here, we used resident-intruder testing to determine whether endogenous opioids within brain motivational circuitry mediate selective aggression in prairie voles. We first show that peripheral blockade of κ-opioid receptors with the antagonist norbinaltorphimine (nor-BNI; 100 mg/kg), but not with the preferential μ-opioid receptor antagonist naloxone (1, 10, or 30 mg/kg), decreased selective aggression in males. We then provide the first comprehensive characterization of κ- and μ-opioid receptors in the prairie vole brain. Finally, we demonstrate that blockade of κ-opioid receptors (500 ng nor-BNI) within the nucleus accumbens (NAc) shell abolishes selective aggression in both sexes, but blockade of these receptors within the NAc core enhances this behavior specifically in females. Blockade of κ-opioid receptors within the ventral pallidum or μ-opioid receptors with the specific μ-opioid receptor antagonist H-D-Phe-Cys-Tyr-D-Trp-Arg-Thr-PenThr-NH2 (1 ng CTAP) within the NAc shell had no effect in either sex. Thus, κ-opioid receptors within the NAc shell mediate aversive social motivation that is critical for pair bond maintenance.
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“Opioid signaling at KORs occurs downstream of NAc shell DA activation of D1Rs to generate selective aggression, whereas affiliative behavior remains unchanged following manipulations to NAc D1Rs and KORs [156,157].”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [156]
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“In addition to changes in D1R density, the NAc sees an upregulation of k-opioid receptors (KORs) following pair bonding in male and female voles.”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [156]
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“KORs in the shell of the NAc encode social aversion to novel conspecifics, and blockade of KORs in the NAc shell diminishes selective aggression from both males and females [156].”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [156]
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“This suggests that the two receptor systems are acting in a coordinated fashion in the striatum to modulate different aspects of pair bonding (Resendez et al 2012).”
From The behavioral, anatomical and pharmacological parallels between social attachment, love and addiction (2012) · cites this paper as Resendez et al 2012
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Cites
Neural systems of reinforcement for drug addiction: from actions to habits to compulsion
Everitt, B. J., & Robbins, T. W. (2005) · Nature Neuroscience · doi:10.1038/nn1579 · Cited by 3,785 · cited 4×
“, 2006; Aragona and Wang, 2007) and unconditioned incentives, including those of an aversive nature (Kalivas and Duffy, 1995; Ikemoto and Panksepp, 1999; Kelley and Berridge, 2002; Everitt and Robbins, 2005; Becker, 2009).”
BackgroundInfluentialD 1 and D 2 Dopamine Receptor-regulated Gene Expression of Striatonigral and Striatopallidal Neurons
Gerfen, C. R., Engber, T. M., Mahan, L. C., Susel, Z., Chase, T. N., Monsma, F. J., & Sibley, D. R. (1990) · Science · doi:10.1126/science.2147780 · Cited by 2,967 · cited 2×
“Moreover, activation of D1-like receptors increases dynorphin levels (Gerfen et al., 1990), indicating a direct interaction between these systems.”
BackgroundDopamine in motivational control: rewarding, aversive, and alerting
Bromberg-Martin, E. S., Matsumoto, M., & Hikosaka, O. (2010) · Neuron · doi:10.1016/j.neuron.2010.11.022 · Cited by 2,396 · cited 2×
“While recent data have demonstrated that different subsets of DA containing neurons within the VTA are activated by rewarding versus aversive stimuli (Brischoux et al., 2009; Matsumoto and Hikosaka, 2009; Bromberg-Martin et al., 2010; Lammel et al., 2011), it has yet to be determined how this may be associated with so…”
BackgroundThe neurobiology of pair bonding.
Young, L. J., & Wang, Z. (2004) · Nature Neuroscience · doi:10.1038/nn1327 · Cited by 1,523 · cited 1×
“The socially monogamous prairie vole (Microtus ochrogaster) is an excellent model system to study the neurobiology of social attachment (Young and Wang, 2004; Young et al., 2005; Aragona and Wang, 2009).”
BackgroundThe Neuroscience of Natural Rewards: Relevance to Addictive Drugs
Kelley, A. E., & Berridge, K. C. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03306.2002 · Cited by 1,505 · cited 7×
“Thus, site-specific behavioral pharmacology identified -opioid receptors within the NAc shell—a key brain region in mediating unconditioned motivational responses (Ikemoto and Panksepp, 1999; Kelley and Berridge, 2002)—as important for aversive social motivation in pair-bonded prairie voles.”
BackgroundInfluentialIkemoto, S. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.004 · Cited by 1,477 · cited 2×
“For example, both unconditioned rewarding and aversive stimuli increase DA in the NAc shell (Kalivas and Duffy, 1995; Ikemoto, 2007), and this increase is associated with aspects of both approach and avoidance behaviors (Ikemoto and Panksepp, 1999; Di Chiara and Bassareo, 2007; Oleson et al.”
BackgroundIkemoto, S., & Panksepp, J. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00023-5 · Cited by 1,450 · cited 6×
“While the NAc shell is well known to play a critical role in the processing of unconditioned rewarding and aversive stimuli (Ikemoto and Panksepp, 1999; Ito et al., 2000; Di Chiara et al., 2004; Everitt and Robbins, 2005; Aragona et al., 2008, 2009), the neural mechanisms within this brain region…”
BackgroundInfluentialTwo types of dopamine neuron distinctly convey positive and negative motivational signals
Matsumoto, M., & Hikosaka, O. (2009) · Nature · doi:10.1038/nature08028 · Cited by 1,378 · cited 2×
“…that different subsets of DA containing neurons within the VTA are activated by rewarding versus aversive stimuli (Brischoux et al., 2009; Matsumoto and Hikosaka, 2009; Bromberg-Martin et al., 2010; Lammel et al., 2011), it has yet to be determined how this may be associated with social…”
BackgroundAnatomy of CNS opioid receptors
Mansour, A., Khachaturian, H., Lewis, M. E., Akil, H., & Watson, S. J. (1988) · Trends in Neurosciences · doi:10.1016/0166-2236(88)90093-8 · Cited by 1,197
Dynorphin Is a Specific Endogenous Ligand of the κ Opioid Receptor
Chavkin, C., James, I. F., & D, A. G. M. (1982) · Science · doi:10.1126/science.6120570 · Cited by 1,171 · cited 1×
“Conversely, D1-expressing neurons contain dynorphin, the endogenous ligand for -opioid receptors that mediates aversion and negative affect (Chavkin et al., 1982; Mucha and Herz, 1985; Pfeiffer et al., 1986).”
Background
Research works printed but not linked: 2
- Firestone, 1991, Behavioral correlates of intra-female reproductive suppression in prairie voles, Microtus ochrogaster, Behav Neural Biol, 55, 363
- Getz, 1978, Speculation on social structure and population cycles of microtine rodents, Biologist, 60, 134
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The neural mechanisms and circuitry of the pair bond
Walum, H., & Young, L. J. (2018) · Nature Reviews Neuroscience · doi:10.1038/s41583-018-0072-6 · Cited by 353
Stress, 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 395
“Many studies have also investigated the role of the mesolimbic dopamine system and opioid regulation of rewarding social behaviors such as pair-bonds between mates (Aragona, 2009; Resendez et al., 2012); we describe these and additional research avenues throughout.”
BackgroundBurkett, J. P., & Young, L. J. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2794-x · Cited by 307
“A second recent study investigated the role of KOR in the maintenance of pair bonds in prairie voles (Resendez et al. 2012).”
Castro, D. C., & Bruchas, M. R. (2019) · Neuron · doi:10.1016/j.neuron.2019.03.003 · Cited by 306
The Kappa Opioid Receptor: From Addiction to Depression, and Back
Lalanne, L., Ayrancı, G., Kieffer, B. L., & Lutz, P.-É. (2014) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2014.00170 · Cited by 236
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
Nicotine aversion: Neurobiological mechanisms and relevance to tobacco dependence vulnerability
Fowler, C. D., & Kenny, P. J. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.09.008 · Cited by 176
“…and acetylcholine, opioid signaling also appears to be an important mediator of aversive processing within the NAc, most notably through the kappa opioid receptor (KOR) (McCutcheon et al., 2012; Resendez et al., 2012), and interactions between nicotinic and KOR signaling have been established.”
InfluentialOptogenetic insights on the relationship between anxiety-related behaviors and social deficits
Allsop, S. A., Vander Weele, C. M., Wichmann, R., & Tye, K. M. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00241 · Cited by 150
“…www.frontiersin.org July 2014 | Volume 8 | Article 241 | 4 assays of pair bonding in prairie voles to reveal the importance of oxytocin, vasopressin, dopamine, and opioids in selective social attachment (Insel and Hulihan, 1995; Cho et al., 1999; Aragona et al., 2003, 2006; Resendez et al., 2012).”
BackgroundRose, J. H., Karkhanis, A. N., Chen, R., Gioia, D., Lopez, M. F., Becker, H. C., McCool, B. A., & Jones, S. R. (2016) · International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyv127 · Cited by 136
Pearce, E., Wlodarski, R., Machin, A., & Dunbar, R. I. M. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1700712114 · Cited by 131
The multiple facets of opioid receptor function: implications for addiction
Lutz, P.-É., & Kieffer, B. L. (2013) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.02.005 · Cited by 129
“Accordingly, KOR activation in the NAc decreased social play in adolescent rats [19], and mediated selective aggression towards novel conspecifics in prairie voles, thereby supporting pair bond maintenance [26].”
BackgroundBales, 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
Anhedonia in depression symptomatology: appetite dysregulation and defective brain reward processing
Coccurello, R. (2019) · Behavioural Brain Research · doi:10.1016/j.bbr.2019.112041 · Cited by 106
Russell, S. E., Rachlin, A. B., Smith, K. L., Muschamp, J. W., Berry, L., Zhao, Z., & Chartoff, E. H. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.07.042 · Cited by 103
Endogenous opiates and behavior: 2012
Bodnar, R. J. (2013) · Peptides · doi:10.1016/j.peptides.2013.10.001 · Cited by 98
Resendez, S. L., Dome, M., Gormley, G., Franco, D., Nevárez, N., Hamid, A. A., & Aragona, B. J. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.4123-12.2013 · Cited by 93
“…prairie voles (Getz et al., 1981), the choice of a mate that will result in successful reproduction is of critical importance (Curtis, 2010; Resendez et al., 2012), and the present study demonstrates that appropriate MOR activation within distinct regions of the striatum has evolved to…”
BackgroundMethodResultInfluentialEpigenetic Regulation of the Kappa Opioid Receptor by Child Abuse
Lutz, P.-E., Gross, J. A., Dhir, S. K., Maussion, G., Yang, J., Bramoulle, A., Meaney, M. J., & Turecki, G. (2018) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.07.012 · Cited by 96
Dopamine and opioid systems interact within the nucleus accumbens to maintain monogamous pair bonds
Resendez, S. L., Keyes, P. C., Day, J. J., Hambro, C., Austin, C. J., Maina, F. K., Eidson, L. N., Porter-Stransky, K. A., Nevárez, N., McLean, J. W., et al. (2016) · eLife · doi:10.7554/elife.15325 · Cited by 88
“Pregnancy was confirmed by extracting embryos from pregnant females and subsequently categorizing pregnancy status by average neonatal weight of the embryos (Curtis, 2010; Resendez et al., 2012)”
Self-citationSocial 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 76
Loth, M. K., & Donaldson, Z. R. (2020) · Endocrinology · doi:10.1210/endocr/bqaa223 · Cited by 80
“It is also worth noting that Resendez et al demonstrated an increase in NAc MOR mRNA during bond formation, a time associated with increased NAc OXT release, although whether this increase is OXT-dependent has not been directly tested (42, 55, 56).”
BackgroundModulation of 5-HT release by dynorphin mediates social deficits during opioid withdrawal
Pomrenze, M. B., Pinto, D. F. C., Neumann, P. A., Llorach, P., Tucciarone, J., Morishita, W., Eshel, N., Heifets, B. D., & Malenka, R. C. (2022) · Neuron · doi:10.1016/j.neuron.2022.09.024 · Cited by 79
The opioid system and the social brain: implications for depression and suicide
Lutz, P., Courtet, P., & Calati, R. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24269 · Cited by 53
“…formation and maintenance of pair bonds relies on both MOR and KOR signaling (Resendez and Aragona 2013; Resendez et al. 2013; Resendez et al. 2016; Resendez et al. 2012), in the nucleus accumbens where these receptors are thought to mediate reinforcing interactions with the preferred partner…”
BackgroundRobles, C. F., McMackin, M. Z., Campi, K. L., Doig, I. E., Takahashi, E. Y., Pride, M. C., & Trainor, B. C. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.01.003 · Cited by 67
“Furthermore, treatment with KOR antagonists decrease male resident-intruder aggression in prairie voles (Resendez et al., 2012).”
BackgroundCarp, S. B., Rothwell, E. S., Bourdon, A., Freeman, S. M., Ferrer, E. E., & Bales, K. L. (2015) · American Journal of Primatology · doi:10.1002/ajp.22450 · Cited by 63
“…and opioid systems in mediating pair bond formation inmonogamous prairie voles [Burkett et al., 2011; Cho et al., 1999; Gingrich et al., 2000; Resendez et al., 2012; Williams et al., 1994; Young et al., 2001], and it has also been used to study social preferences in non-monogamous rodents…”
MethodAversive motivation and the maintenance of monogamous pair bonding
Resendez, S. L., & Aragona, B. J. (2013) · Reviews in the Neurosciences · doi:10.1515/revneuro-2012-0068 · Cited by 58
Self-citationThe Neurobiology of Love and Pair Bonding from Human and Animal Perspectives
Blumenthal, S. A., & Young, L. J. (2023) · Biology · doi:10.3390/biology12060844 · Cited by 59
Sex differences in effects of dopamine D1 receptors on social withdrawal
Campi, K. L., Greenberg, G. D., Kapoor, A., Ziegler, T. E., & Trainor, B. C. (2014) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.09.026 · Cited by 55
“Infusion of the KOR antagonist norbinaltorphimine (nor-BNI) into the NAc shell of pair-bonded prairie voles reduces aggressive behavior (Resendez et al., 2012).”
Naltrexone alters the processing of social and emotional stimuli in healthy adults
Wardle, M. C., Bershad, A. K., & de Wit, H. (2015) · Social Neuroscience · doi:10.1080/17470919.2015.1136355 · Cited by 52
“suggesting that kappa antagonism reduces aversive social motivation (Resendez & Aragona, 2013; Resendez et al., 2012) in addition to exerting more general anxiolytic effects (Falcon, Maier, Robinson,”
BackgroundDynorphin and its role in alcohol use disorder
Karkhanis, A. N., & Al-Hasani, R. (2020) · Brain Research · doi:10.1016/j.brainres.2020.146742 · Cited by 47
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 54
Hinde, K., Muth, C., Maninger, N., Ragen, B., Larke, R. H., Jarcho, M. R., Mendoza, S. P., Mason, W. A., Ferrer, E. E., Cherry, S. R., et al. (2016) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2016.00221 · Cited by 46
“…receptors (Ragen et al., 2015a). κ opioid receptors are associated with negative affect and the dysphoria of social separation in vole and titi monkeys (Resendez et al., 2012; Resendez and Aragona, 2013; Ragen et al., 2015b). κ opioid receptors are also present in titi monkey LS (Ragen et al.,…”
BackgroundPerkeybile, A. M., & Bales, K. L. (2017) · Journal of Experimental Biology · doi:10.1242/jeb.142182 · Cited by 43
“, 2013), while the dysphoric effects of separation are mediated by kappa opioid receptors (Ragen et al., 2015a,b; Resendez and Aragona, 2013; Resendez et al., 2012).”
BackgroundSocial selectivity and social motivation in voles
Beery, A. K., Lopez, S. A., Blandino, K. L., Lee, N. S., Bourdon, N. S., & Ahern, T. H. (2021) · eLife · doi:10.7554/elife.72684 · Cited by 53
Inagaki, T. K., Hazlett, L. I., & Andreescu, C. (2019) · Journal of Experimental Psychology General · doi:10.1037/xge0000674 · Cited by 38
Social withdrawal and gender differences: Clinical phenotypes and biological bases
Masi, G., Berloffa, S., Milone, A., & Brovedani, P. (2021) · Journal of Neuroscience Research · doi:10.1002/jnr.24802 · Cited by 45
Ragen, B. J., Freeman, S. M., Laredo, S. A., Mendoza, S. P., & Bales, K. L. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.01.023 · Cited by 37
Matuskey, D., Dias, M., Naganawa, M., Pittman, B. P., Henry, S. E., Li, S., Gao, H., Ropchan, J. R., Nabulsi, N., Carson, R. E., et al. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0379-7 · Cited by 39
Neuroendocrine regulation of long-term pair maintenance in the monogamous zebra finch
Prior, N. H., & Soma, K. K. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.04.014 · Cited by 39
Ragen, B., Maninger, N., Mendoza, S. P., Jarcho, M. R., & Bales, K. L. (2013) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2013.05.009 · Cited by 39
“The current study replicates findings in prairie voles that did not find an effect of opioid blockade on affiliative behaviors (Shapiro et al., 1989; Burkett et al., 2011; Resendez et al., 2012).”
InfluentialInvestigational drugs under development for the treatment of PTSD
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“These drugs have been used in rodents and nonhuman primates with little to no side effects [124,132,133].”
BackgroundSocial housing and alcohol drinking in male-female pairs of prairie voles (Microtus ochrogaster)
Hostetler, C. M., Anacker, A. M. J., Loftis, J. M., & Ryabinin, A. E. (2012) · Psychopharmacology · doi:10.1007/s00213-012-2836-4 · Cited by 35
“However, prairie voles display normal social behavior toward, and form partner preferences with, a gonadectomized partner (DeVries and Carter 1999) and will form and maintain pair bonds in the absence of mating (Cho et al. 1999; Resendez et al. 2012; Winslow et al. 1993).”
BackgroundFamiliarity and Mate Preference Assessment with the Partner Preference Test
Beery, A. K. (2021) · Current Protocols · doi:10.1002/cpz1.173 · Cited by 39
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Putnam, P. T., & Chang, S. W. C. (2022) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2021.0050 · Cited by 34
Comparative role of reward in long-term peer and mate relationships in voles
Goodwin, N. L., Lopez, S., Lee, N. S., & Beery, A. K. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2018.10.012 · Cited by 35
Inoue, K., Burkett, J. P., & Young, L. J. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.03.035 · Cited by 33
“Our findings and those of Resendez et al. (2012) now suggest some interesting locations where MOR and KOR intersect, which may provide clues as to a mechanism of cross-talk between these behavioral systems.”
BackgroundResultInfluentialDynorphins regulate the strength of social memory
Bilkei‐Gorzó, A., Mauer, D., Michel, K., & Zimmer, A. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.10.023 · Cited by 31
“Recently the contribution of dynorphin signalling in pair bonding maintenance was also suggested: Pharmacological manipulation of its receptor, the kappa opioid receptor (KOR), altered aversive social motivation in prairie vole (Resendez et al., 2012).”
BackgroundRagen, B., Maninger, N., Mendoza, S. P., & Bales, K. L. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.11.053 · Cited by 31
Stress impairs new but not established relationships in seasonally social voles
Anacker, A. M. J., Reitz, K. M., Goodwin, N. L., & Beery, A. K. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.01.004 · Cited by 32
Sadino, J. M., Bradeen, X., Kelly, C. J., Brusman, L. E., Walker, D. M., & Donaldson, Z. R. (2023) · eLife · doi:10.7554/elife.80517 · Cited by 29
“Steroid and opioid signaling have been extensively implicated in pair bonding ( Resendez et al., 2016 ; Resendez et al., 2012 ; Loth and Donaldson, 2021 ; Inoue et al., 2013 ; Stetzik et al., 2018 ; Carter and Perkeybile, 2018 ; Lei et al., 2010 ; Cushing et al., 2008 ).”
BackgroundInfluentialNeural 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
Mother–Pup Interactions: Rodents and Humans
Lucion, A. B., & Bortolini, M. C. (2014) · Frontiers in Endocrinology · doi:10.3389/fendo.2014.00017 · Cited by 33
“, OXT, vasopressin, serotonin, noradrenaline), cytokines (14), opioids (15, 16), and dopamine (17), as well as epigenetic (18) and environmental factors (19).”
BackgroundManinger, N., Hinde, K., Mendoza, S. P., Mason, W. A., Larke, R. H., Ragen, B., Jarcho, M. R., Cherry, S. R., Rowland, D. J., Ferrer, E. E., et al. (2017) · Neuroscience · doi:10.1016/j.neuroscience.2017.02.028 · Cited by 27
“Also likely involved are µ and ĸ opioid receptors, which are involved in pair bond regulation in both prairie voles (Resendez et al., 2012, Resendez et al., 2013) and titi monkeys (Ragen et al., 2013, Ragen et al., 2015b).”
Sex differences in the reward value of familiar mates in prairie voles
Vahaba, D. M., Halstead, E. R., Donaldson, Z. R., Ahern, T. H., & Beery, A. K. (2022) · Genes Brain & Behavior · doi:10.1111/gbb.12790 · Cited by 29
“Opioid signaling is also necessary for partnership maintenance, and interacts with dopamine signaling within the nucleus accumbens.(11,12) Behaviorally, prairie voles show a conditioned preference for cues associated with mates in socially conditioned place preference tests,(13,14) although unfamiliar opposite-sex con…”
BackgroundFisher‐Phelps, M., Mendoza, S. P., Serna, S. N., Griffin, L. L., Schaefer, T. J., Jarcho, M. R., Ragen, B., Goetze, L. R., & Bales, K. L. (2015) · American Journal of Primatology · doi:10.1002/ajp.22483 · Cited by 26
“Laboratory simulations of territorial encounters have been used frequently in the study of socially monogamous rodents (primarily prairie voles, Microtus ochrogaster) in order to examine both the neurobiological basis of mate-guarding (although often not in the presence of the mate), and to pharmacologically manipulat…”
Kowalczyk, A. S., Davila, R., & Trainor, B. C. (2018) · Hormones and Behavior · doi:10.1016/j.yhbeh.2017.12.010 · Cited by 25
“In pair-bonded male and female prairie voles, KOR activation in the nucleus accumbens facilitates aggression towards same-sex intruders (Resendez et al., 2012).”
BackgroundMethodSerotonin 1A agonism decreases affiliative behavior in pair-bonded titi monkeys
Larke, R. H., Maninger, N., Ragen, B., Mendoza, S. P., & Bales, K. L. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.10.001 · Cited by 21
“…2009; Williams et al., 1994), vasopressin (Lim et al., 2004; Lim and Young, 2004; Pitkow et al., 2001), dopamine (Aragona and Wang, 2009; Hostetler et al., 2011; Resendez et al., 2016), and opioid systems (Burkett et al., 2011; Resendez et al., 2013; Resendez et al., 2016; Resendez et al., 2012).”
BackgroundSex Differences in Regional Brain Glucose Metabolism Following Opioid Withdrawal and Replacement
Santoro, G. C., Carrión, J., Patel, K. J., Vilchez, C., Veith, J., Brodie, J. D., & Dewey, S. L. (2017) · Neuropsychopharmacology · doi:10.1038/npp.2017.69 · Cited by 22
“Specifically, women are generally considered more susceptible to drug cravings and relapse (Fox et al, 2014; Hitschfeld et al, 2015; Kennedy et al, 2013; Kippin et al, 2005; Robbins et al, 1999; Rubonis et al, 1994).”
BackgroundLaman-Maharg, A., Copeland, T., Sanchez, E. O., Campi, K. L., & Trainor, B. C. (2017) · Behavioural Brain Research · doi:10.1016/j.bbr.2017.06.015 · Cited by 21
Selectivity and Sociality: Aggression and Affiliation Shape Vole Social Relationships
Lee, N. S., & Beery, A. K. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.826831 · Cited by 25
Duclot, F., Sailer, L. L., Koutakis, P., Wang, Z., & Kabbaj, M. (2020) · Biological Psychiatry · doi:10.1016/j.biopsych.2020.11.022 · Cited by 20
Alcohol’s Effects on Pair-Bond Maintenance in Male Prairie Voles
Walcott, A. T., & Ryabinin, A. E. (2017) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2017.00226 · Cited by 20
“These affiliative behaviors start to become directed specifically toward their partner once they formed a pair bond (18, 38, 42).”
BackgroundLahvis, G. P., Panksepp, J. B., Kennedy, B. C., Wilson, C. R., & Merriman, D. K. (2015) · Journal of comparative psychology · doi:10.1037/a0039435 · Cited by 20
Bales, K. L., & Rogers, F. D. (2022) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2021.0061 · Cited by 17
Sex, Drugs, and Violence: Neuromodulation of Attachment and Conflict in Voles
Gobrogge, K. L. (2013) · Current topics in behavioral neurosciences · doi:10.1007/7854_2013_264 · Cited by 16
“…GABA, glutamate, and opioids have also been implicated in pair-bonding behavior (Williams et al. 1992, 1994; Winslow et al. 1993; Carter et al. 1995; Wang et al. 1998; Liu et al. 2001; Aragona et al. 2003; Liu and Wang 2003; Lim and Young 2004; Curtis and Wang 2005b; Resendez et al. 2012).”
Conditioned mate-guarding behavior in the female rat
Holley, A., Shalev, S., Bellevue, S., & Pfaus, J. G. (2014) · Physiology & Behavior · doi:10.1016/j.physbeh.2014.04.034 · Cited by 18
Brain Systems Underlying Social Behavior
Weitekamp, C. A., & Hofmann, H. A. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-804042-3.00025-7 · Cited by 17
Martin, T. J., Sexton, T., Kim, S. A., Severino, A. L., Peters, C. M., Young, L. J., & Childers, S. R. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.10.047 · Cited by 13
“…kappa opioid receptors are more intimately involved in reinforcement systems in the prairie vole relatively to other typical laboratory rodent species, as has been suggested by the involvement of kappa opioid receptors in male-male aggression following pair bond formation (Resendez et al., 2012).”
InfluentialCone, A. L., Wu, K. K., Kravitz, A. V., & Norris, A. J. (2023) · iScience · doi:10.1016/j.isci.2023.107241 · Cited by 12
Borland, J. M. (2025) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2025.101175 · Cited by 13
Mate Selection, Sexual Orientation, and Pair Bonding
Balthazart, J., & Young, L. J. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397175-3.00048-x · Cited by 12
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 12
Alger, S. J., Stevenson, S. A., Vega, A. A., Kelm‐Nelson, C. A., Juang, C. V., & Riters, L. V. (2021) · Behavioral Neuroscience · doi:10.1037/bne0000494 · Cited by 12
Wright, E. C., Parks, T. V., Alexander, J. O., Supra, R., & Trainor, B. C. (2018) · Behavioural Brain Research · doi:10.1016/j.bbr.2018.05.011 · Cited by 13
“While activation of KOR has been linked to increased aggression, this effect was observed in the nucleus accumbens and in a specific context of pair bonding [72].”
Forero, S. A., Sailer, L. L., Girčytė, A., Madrid, J. E., Sullivan, N., & Ophir, A. G. (2023) · Hormones and Behavior · doi:10.1016/j.yhbeh.2023.105351 · Cited by 11
Forero, S. A., Liu, S., Shetty, N., & Ophir, A. G. (2024) · Genes Brain & Behavior · doi:10.1111/gbb.12906 · Cited by 9
Polzin, B. J., Heimovics, S., & Riters, L. V. (2021) · Brain, Behavior and Evolution · doi:10.1159/000521310 · Cited by 10
“…food and drugs [Mcbride et al., 1999; Alderson et al., 2001; Pecina, 2005; Van Der Plasse et al., 2012] and social reward related to pair bonding [Resendez et al., 2012, 2013], while the ACC plays a significant role in the approach to motivational stimuli and learning [Parkinson et al., 1999;…”
BackgroundCardiovascular control is associated with pair-bond success in male prairie voles
Lewis, R. J., Wilkins, B. A., Benjamin, B., & Curtis, J. T. (2017) · Autonomic Neuroscience · doi:10.1016/j.autneu.2017.10.002 · Cited by 8
“Similarly, Resendez et al. (2012) found that males from pairs with smaller pups in utero after two weeks of pairing did not display the stranger-directed aggression typical of pair-bonded males.”
Wang, Y., Yan, M., Zheng, G., He, L., & Yang, H. (2014) · Acta Pharmacologica Sinica · doi:10.1038/aps.2014.21 · Cited by 8
Loth, M. K., Schmidt, J. C., Gonzalez, C. A., Brusman, L. E., Sadino, J. M., Winther, K. E., Protter, D. S. W., & Donaldson, Z. R. (2025) · Scientific Reports · doi:10.1038/s41598-025-06367-1 · Cited by 8
Alger, S. J., Kelm‐Nelson, C. A., Stevenson, S. A., Juang, C., Gammie, S. C., & Riters, L. V. (2019) · Genes Brain & Behavior · doi:10.1111/gbb.12619 · Cited by 8
“neural mechanisms that function to maintain long-term, affiliative bonds.(9-11) Furthermore, most of the studies on pair bond mainte-”
BackgroundFreeman, S. M. (2021) · Methods in molecular biology · doi:10.1007/978-1-0716-1759-5_7 · Cited by 7
Wu, R., Xu, Z., Song, Z., & Tai, F. (2023) · Hormones and Behavior · doi:10.1016/j.yhbeh.2023.105366 · Cited by 4
Ford, C. L., McDonough, A. A., Horie, K., & Young, L. J. (2024) · Neuropharmacology · doi:10.1016/j.neuropharm.2024.109848 · Cited by 4
Tomaszycki, M. L., Schnelker, J. H., & Zatirka, B. P. (2014) · Behaviour · doi:10.1163/1568539x-00003234 · Cited by 4
Female-Paced Mating Does Not Affect Pair-Bond Expression byMicrotus ochrogaster(Prairie Vole) Males
McCracken, K., Lewis, R. J., & Curtis, J. T. (2015) · Northeastern Naturalist · doi:10.1656/045.022.0311 · Cited by 4
“The answer is found in the study by Resendez et al. (2012) which showed that the effects of pregnancy status on pair-bond expression are sexually dimorphic in prairie voles.”
BackgroundInfluentialZhang, L., Qu, Y., Young, L. J., Hou, W., Liu, L., Liu, J., Wang, Y., Li, L., Guo, X., Yin, L., et al. (2024) · eLife · doi:10.7554/elife.100292 · Cited by 5
“In addition, selective aggression toward a stranger was stopped by blocking D1R in the NAc ( Resendez et al., 2012 ).”
Mapping Kappa Opioid Receptor Binding in Titi Monkeys with [ 11 C]GR103545 PET
Almeida, A. J. D., Hobson, B. A., Savidge, L. E., Manca, C., Paulus, J. P., Bales, K. L., & Chaudhari, A. J. (2025) · Molecular Imaging · doi:10.1177/15353508251341082 · Cited by 5
Zhang, L., Qu, Y., Young, L. J., Hou, W., Liu, L., Liu, J., Wang, Y., Li, L., Guo, X., Yin, L., et al. (2025) · eLife · doi:10.1101/2024.07.24.604911 · Cited by 3
The transient joys of others—neural ensembles encode social approach in bonded voles
Phelps, S. M., & Gustison, M. L. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2006307117 · Cited by 3
Effects of a D2 receptor antagonist on repeated pair bond formation in the male prairie vole
Herschberger, M. R., & Perkeybile, A. M. (2022) · Hormones and Behavior · doi:10.1016/j.yhbeh.2022.105149 · Cited by 1
López-Gutiérrez, M. F., Valera-Marín, G., Alcauter, S., & Portillo, W. (2023) · Neuromethods · doi:10.1007/978-1-0716-3234-5_2 · Cited by 1
Castro, A. E., López-Quiroz, M. A., Ávila‐González, D., Camacho, F., Paredes, R. G., Díaz, N. F., & Portillo, W. (2025) · PLoS ONE · doi:10.1371/journal.pone.0335626 · Cited by 1
Nowicki, J. P., Pratchett, M. S., Walker, S. P. W., Coker, D. J., & O’Connell, L. A. (2017) · King Abdullah University of Science and Technology Repository (King Abdullah University of Science and Technology) · doi:10.1101/214759 · Cited by 1
Simmons, T. C., Rothwell, E. S., Savidge, L. E., Razo, R. A., & Bales, K. L. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-809633-8.90712-x · Cited by 1
Interactions Between Social and Drug Reward on Stimulated Dopamine Release in Male Prairie Voles
Austin, C. J. (2013) · Deep Blue (University of Michigan)
The Overlap Between Romantic Love And Addiction
Barends, A. J. (2014) · Utrecht University Repository (Utrecht University)
Targeting Opioid Receptors for Innovative Antidepressant Therapies: Rediscovering the Opioid Cure
Darcq, E., Chung, P. C. S., Kieffer, B. L., & Lutz, P.-É. (2016) · Springer eBooks · doi:10.1007/978-81-322-2803-5_38
Energetic metabolism, stress, and immunity—development of population physiology
Moshkin, M. P., & Gerlinskaya, L. A. (2016) · Biology Bulletin · doi:10.1134/s1062359016110108
“For example, in monogamous prairie voles, the activation of κ-opioid receptors stimulates the formation of aversive motivations aimed at unknown intruders (Resendez et al., 2012).”
(2016) · Royal Society of Chemistry eBooks · doi:10.1039/bk9781782621348-00198
Metadata
- Authors
- Resendez, S. L., Kuhnmuench, M., Krzywosinski, T., & Aragona, B. J.
- Affiliations
- University of Michigan (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2012-05-16
- Volume
- 32
- Issue
- 20
- Pages
- 6771-6784
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6622186
- OpenAlex
- W2005581416
- Cited by
- 110
- References
- 152
- Citations by year
- 2026: 4 · 2025: 7 · 2024: 5 · 2023: 6 · 2022: 6 · 2021: 7 · 2020: 4 · 2019: 6 · 2018: 6 · 2017: 11 · 2016: 10 · 2015: 12 · 2014: 11 · 2013: 12 · 2012: 3
- FWCI
- 18.28
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (0953106)
- Florida State University
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- kappa opioid receptor, pair bond maintenance, Microtus ochrogaster, nucleus accumbens shell, mate guarding, endogenous opioids, nor-binaltorphimine, mu-opioid receptor, CTAP, social motivation, social monogamy, ventral pallidum
- MeSH terms
- Aggression, Animals, Autoradiography, Brain, Corticosterone, Arvicolinae, Dose-Response Relationship, Drug, Female, Male, Microinjections, Naloxone, Naltrexone, Nucleus Accumbens, Pair Bond, Peptide Fragments, Sex Characteristics, Somatostatin, Testosterone, Receptors, Opioid, mu, Receptors, Opioid, kappa
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