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Partner Preference Development in Female Prairie Voles Is Facilitated by Mating or the Central Infusion of Oxytocina
Abstract
Results of these experiments indicate that females given at least 24 hours of cohabitation with a male develop a social preference for the familiar partner versus a stranger. Mating is not essential for the development of partner preferences, but clearly facilitates the onset of preferences. Females given six hours of cohabitation showed partner preferences only if they mated with the partner during cohabitation (Experiment 2) or if they received oxytocin (Experiment 3). Females that continued to mate during preference tests (Experiment 2, n = 4) mated exclusively with the partner. Oxytocin infusions, even in the absence of mating or estrogen priming, facilitated the development of partner preferences.
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“Centrally administered OT facilitates contact-seeking, attachment bond formation, and social memory in rodents (Ferguson et al., 2000; Williams et al., 1992; Witt et al., 1992).”
From Effects of intranasal oxytocin on social anxiety in males with fragile X syndrome (2012) · cites this paper as Williams et al., 1992
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Cited by
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Neuropeptidergic regulation of affiliative behavior and social bonding in animals
Lim, M. M., & Young, L. J. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2006.06.028 · Cited by 624
“Indeed, oxytocin infused i.c. v. into both male and female prairie voles facilitates pair bond formation in the absence of mating (Cho et al., 1999; Williams et al., 1992).”
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The neurobiology of pair bonding: Insights from a socially monogamous rodent
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“following cohabitation with a male without mating, although this requires longer time periods (Williams et al., 1992).”
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“For example, oxytocin (OT) modulates spontaneous alloparental behavior and plays a central role in the formation of partner preferences (PP), the laboratory proxy of pair bonds, in female prairie voles (Williams et al., 1992; Insel and Hulihan, 1995; Olazábal and Young, 2006a).”
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“The length of cohabitation required to form partner preferences is reduced in female prairie voles if the pair mates (Williams et al., 1992; Insel et al., 1995) or if exogenous OT is infused into the brain (Winslow et al., 1993b; Williams et al., 1994; Insel and Hulihan, 1995).”
InfluentialIntranasal 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
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“In the laboratory, pair bond formation is reflected through formation of a robust and enduring preference for the mating partner relative to a novel opposite sex individual, referred to as a “partner preference” (Williams et al., 1992a).”
BackgroundGobrogge, K. L., Liu, Y., Jia, X., & Wang, Z. (2007) · Journal of Comparative Neurology · doi:10.1002/cne.21364 · Cited by 178
“…systems, including AVP, OXT, DA, GABA, and glutamate, have been implicated in partner preference formation in male and female prairie voles (Williams et al., 1992a; Winslow et al., 1993; Carter et al., 1995; Aragona et al., 2003; Liu and Wang, 2003; Lim et al., 2004a; Curtis and Wang,…”
BackgroundCampbell, D. B., Datta, D., Jones, S. T., Batey Lee, E., Sutcliffe, J. S., Hammock, E. A. D., & Levitt, P. (2011) · Journal of Neurodevelopmental Disorders · doi:10.1007/s11689-010-9071-2 · Cited by 170
“Moreover, OXT signaling facilitates social preferences between adult monogamous rodents (Williams et al. 1992; Williams et al. 1994).”
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Keebaugh, A. C., & Young, L. J. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.07.018 · Cited by 154
“In a partner preference test, the experimental female is placed in a neutral chamber of a three-chambered apparatus, in which the male “partner” is tethered to one side of the chamber and a novel “stranger” male is tethered in the other (Williams et al., 1992).”
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
“All animals then underwent a 3- hour partner preference test as described previously (Williams et al., 1992).”
MethodBredewold, R., Smith, C. J. W., Dumais, K. M., & Veenema, A. H. (2014) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2014.00216 · Cited by 164
“Given the well-known role of OXT in facilitating pro-social behaviors (Williams et al., 1992; Feldman et al., 2007; Kojima and Alberts, 2011; Feldman, 2012) and reducing anxiety-like behaviors (Windle et al., 1997; Ring et al., 2006; Blume et al., 2008), we expected to find a facilitating effect of…”
BackgroundThe role of oxytocin in male and female reproductive behavior
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“Prairie voles, in particular, have been useful in revealing OT’s role in human sociality largely because they share with humans the tendency toward forming selective preferences for familiar conspecifics (Williams et al., 1992).”
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Effects of intranasal oxytocin on social anxiety in males with fragile X syndrome
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“Centrally administered OT facilitates contact-seeking, attachment bond formation, and social memory in rodents (Ferguson et al., 2000; Williams et al., 1992; Witt et al., 1992).”
Wessells, H., Gralnek, D. R., Dorr, R. T., Hruby, V. J., Hadley, M. E., & Levine, N. (2000) · Urology · doi:10.1016/s0090-4295(00)00680-4 · Cited by 137
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κ-Opioid Receptors within the Nucleus Accumbens Shell Mediate Pair Bond Maintenance
Resendez, S. L., Kuhnmuench, M., Krzywosinski, T., & Aragona, B. J. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.5779-11.2012 · Cited by 110
“Initial pair bond formation involves prosocial behaviors that are reliably assayed with the partner preference test (Williams et al., 1992).”
Ahern, T. H., Hammock, E. A. D., & Young, L. J. (2011) · Developmental Psychobiology · doi:10.1002/dev.20498 · Cited by 113
Oxytocin and same-sex social behavior in female meadow voles
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A brief history of oxytocin and its role in modulating psychostimulant effects
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“…evidence that centrally administered OT could facilitate monogamous pair-bond formation in prairie voles and later that centrally administered OT could modulate social interaction, aggression, and sexual satiety in prairie voles (Carter et al., 1992; Williams et al., 1992; Witt et al., 1990, 1992).”
BackgroundAlgoe, S. B., Kurtz, L. E., & Grewen, K. (2017) · Psychological Science · doi:10.1177/0956797617716922 · Cited by 108
“Specifically, rather than focus on global evaluations of the relationship, we took a cue from original work (Williams et al., 1992) that examined proximal mechanisms for bonding, and we focused on the specific affective and relationship constructs involved in that process; in the future, such an approach may help addr…”
BackgroundResultInfluentialA Conserved Role for Serotonergic Neurotransmission in Mediating Social Behavior in Octopus
Edsinger, E., & Dölen, G. (2018) · Current Biology · doi:10.1016/j.cub.2018.07.061 · Cited by 104
Young, K. A., Liu, Y., Gobrogge, K. L., Wang, H., & Wang, Z. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4275-13.2014 · Cited by 99
“induces PP formation in female prairie voles (Williams et al., 1992; Insel and Hulihan, 1995).”
BackgroundOxytocin inhibits ethanol consumption and ethanol‐induced dopamine release in the nucleus accumbens
Peters, S., Bowen, M. T., Bohrer, K., McGregor, I. S., & Neumann, I. D. (2016) · Addiction Biology · doi:10.1111/adb.12362 · Cited by 101
“2009) with centrally administered OXT facilitating monogamous pair bond formation in prairie voles (Williams et al. 1992).”
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“Motivation, the dorsal striatum, and partner preference formation Partner preference formation in prairie voles is facilitated by mating (Williams et al., 1992), and the present study demonstrates that blockade of neural systems that mediate this behavior, such as the endogenous opioid system…”
BackgroundResultInfluentialSalubrious 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
“…relationships (reviewed in Dunbar, 2010), the neuroendocrine systems that regulate these bond-promoting behavior such as the oxytocin system (e.g., Williams et al., 1992; Winslow et al., 1993; Williams et al., 1994; Insel and Hulihan, 1995; Cho et al., 1999; Ross et al., 2009; Smith et al., 2010;…”
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Oxytocin receptor dynamics in the brain across development and species
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“In addition to maternal care, OXT modulates sexual behavior, social recognition, and affiliative behaviors (Caldwell et al., 1986; Insel and Winslow, 1991; Williams et al., 1992; Ferguson et al., 2001; Neumann and Landgraf, 2012).”
BackgroundNeuroscience: The hard science of oxytocin
Shen, H. H. (2015) · Nature · doi:10.1038/522410a · Cited by 80
Social bonding: regulation by neuropeptides
Lieberwirth, C., & Wang, Z. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00171 · Cited by 86
“…OT seems to be gender-specific as OT administration does not result in partner preference formation and selective OTR antagonist administration does not block partner preference formation in males (Williams et al., 1992a; Winslow et al., 1993; Insel and Hulihan, 1995; but see Cho et al., 1999).”
BackgroundInfluentialAntisocial oxytocin: Complex effects on social behavior
Beery, A. K. (2015) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2015.11.006 · Cited by 74
The neurobiology of pair bond formation, bond disruption, and social buffering
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A neuronal signature for monogamous reunion
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Oxytocin and the salience of social cues
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“ogamous prairie vole [30,31].”
Biological Contribution to Social Influences on Alcohol Drinking: Evidence from Animal Models
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“Oxytocin facilitates partner preference formation in female prairie voles [92], and has a number of addiction-related effects similar to vasopressin,”
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A Neuroscientist’s Guide to the Vole
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Comparative Assessment of Familiarity/Novelty Preferences in Rodents
Beery, A. K., & Shambaugh, K. L. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.648830 · Cited by 50
“In early descriptions, partner preferences became evident in the 2nd hour and remained stable thereafter (Williams et al., 1992a).”
BackgroundDay length and estradiol affect same-sex affiliative behavior in the female meadow vole
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“This contrasts to results obtained in opposite-sex prairie voles, where social behavior in LD is always high, but changes from non-specific to specific affiliation with increased housing time or sexual activity (Williams et al., 1992).”
ResultGillera, S. E. A., Marinello, W. P., Horman, B. M., Phillips, A. L., Ruis, M. T., Stapleton, H. M., Reif, D. M., & Patisaul, H. B. (2019) · Neurotoxicology and Teratology · doi:10.1016/j.ntt.2019.106840 · Cited by 48
“This length of time is sufficient to induce a pair bond even if mating does not occur (Williams et al., 1992).”
BackgroundMethodInfluentialNovel treatments for autism spectrum disorder based on genomics and systems biology
Baribeau, D. A., & Anagnostou, E. A. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2021.107939 · Cited by 51
BDNF-TrkB signaling in oxytocin neurons contributes to maternal behavior
Maynard, K. R., Hobbs, J. W., Phan, B. N., Gupta, A., Rajpurohit, S., Williams, C. A., Rajpurohit, A., Shin, J. H., Jaffe, A. E., & Martinowich, K. (2018) · eLife · doi:10.7554/elife.33676 · Cited by 47
Sexual dimorphism of oxytocin and vasopressin in social cognition and behavior
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“Facing opposite-sex cage mates, prairie voles exhibit familiar-partner preference in both males 30 – 32 and females 19,33,34 with OT injections intracranially.”
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A sexual arousability model involving steroid effects at the plasma membrane
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“A standardized partner preference test is widely used in the study of rodent monogamy, which has allowed comparisons across laboratories, across time, and across species [Williams et al., 1992, 1994; Millan & Bales, 2013], and this test uses similar parameters.”
Zilcha‐Mano, S., Goldstein, P., Dolev‐Amit, T., & Shamay‐Tsoory, S. (2021) · Journal of Consulting and Clinical Psychology · doi:10.1037/ccp0000619 · Cited by 39
“Based on accumulating studies, it has been argued that OT serves as a biological mechanism by which bonds are formed and strengthened in various species (Algoe et al., 2017; Josef et al., 2019; Williams et al., 1992).”
BackgroundLipopolysaccharide facilitates partner preference behaviors in female prairie voles
Bilbo, S. D., KLEIN, S., DEVRIES, A., & Nelson, R. J. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(99)00154-7 · Cited by 37
“Some labs report pair bonding in females within 3 h [18,19], although others report that females require >24 h for partner preferences to be expressed in the absence of mating [20, 21 ,35,36].”
BackgroundFamiliarity and Mate Preference Assessment with the Partner Preference Test
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Oxytocin: A citation network analysis of 10 000 papers
Leng, G., & Leng, R. (2021) · Journal of Neuroendocrinology · doi:10.1111/jne.13014 · Cited by 34
How prior pair-bonding experience affects future bonding behavior in monogamous prairie voles
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“…voles will prefer to affiliate with their partner, display selective aggression towards non-partner individuals, and exhibit robust and organized biparental care ( Williams, 1992 ; Getz et al., 1981 ; Williams et al., 1992 ; Insel and Young, 2001 ; Carter et al., 1995 ; Winslow et al., 1993 ).”
BackgroundDrinking alcohol has sex-dependent effects on pair bond formation in prairie voles
Anacker, A. M. J., Ahern, T. H., Hostetler, C. M., Dufour, B. D., Smith, M. L., Cocking, D. L., Li, J., Young, L. J., Loftis, J. M., & Ryabinin, A. E. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1320879111 · Cited by 28
“Extensive literature implicates oxytocin and AVP in regulation of PP (28, 39, 40), and although we found some effects of alcohol or sex on these neuropeptide levels in a few brain regions (Table S1), there were no significant interactions to indicate a role for either of these neuropeptides in the sex-specific effects…”
BackgroundMethodNeural 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
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Genetics of Aggression in Voles
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Gene Regulation as a Modulator of Social Preference in Voles
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The role of oxytocin and vasopressin in conditioned mate guarding behavior in the female rat
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“whenmale/female prairie voles mate guard the first mate they copulated with [5].”
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Social stimuli cause changes of plasma oxytocin and behavior in guinea pigs
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Alcohol’s Effects on Pair-Bond Maintenance in Male Prairie Voles
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“Partner Preference Test Partner preference test was used as a standard way to test pair bonding in prairie voles (36, 37).”
MethodBaribeau, D. A., & Anagnostou, E. A. (2014) · Europe PMC (PubMed Central) · Cited by 19
Exploring the role of intra-nasal oxytocin on the partner preference effect in humans
Liu, J. C., Guastella, A. J., & Dadds, M. R. (2012) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2012.07.009 · Cited by 19
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“Cohabitation with or without mating induces partner preference in females (Williams et al. 1992), but the effect of cohabitation on partner preference in males is unknown.”
Oxytocin and vasopressin in non-human primates
Ragen, B., & Bales, K. L. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9781139017855.019 · Cited by 18
Oztan, O., Zyga, O., Stafford, D. E. J., & Parker, K. J. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104870 · Cited by 18
“, 1987), and subsequently, pair bond formation in female prairie voles (Williams et al., 1992).”
BackgroundSex, 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
“…such as corticotrophin releasing factor (CRF), steroid hormones, 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…”
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
“, 1993), or when male/female prairie voles mate guard the first mate they copulated with (Williams et al., 1993).”
Emerging Frontiers in Social Neuroendocrinology and the Study of Nonapeptides
Ondrasek, N. R. (2016) · Ethology · doi:10.1111/eth.12493 · Cited by 19
Froemke, R. C., & Carcea, I. (2017) · Principles of Gender-Specific Medicine · doi:10.1016/b978-0-12-803506-1.00037-1 · Cited by 20
Romantic Love Is Associated with Enhanced Inhibitory Control in an Emotional Stop-Signal Task
Song, S., Zou, Z., Song, H., Wang, Y.-M., Uquillas, F. D., Wang, H., & Chen, H. (2016) · Frontiers in Psychology · doi:10.3389/fpsyg.2016.01574 · Cited by 18
“Studies show a critical role for oxytocin (OT) in promoting pair-bonding formation, and OT has been shown to modulate social interaction and sexual satiety in prairie voles (Carter, 1992; Williams et al., 1992; Witt et al., 1992).”
BackgroundEstrous phase alters social behavior in a polygynous but not a monogamous Peromyscus species
Karelina, K., Walton, J. C., Weil, Z. M., Norman, G. J., Nelson, R. J., & DeVries, A. C. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.03.022 · Cited by 15
“following exogenous administration of OT) induces a pro-social behavioral phenotype (Cho et al., 1999; Williams et al., 1992; Witt et al., 1992), thus, elevated endogenous OT prior to and during social interaction potentially contributed to increased affiliative social contact in P.”
BackgroundInfluentialSex differences of oxytocin and vasopressin in social behaviors
Lu, Q., & Hu, S. (2021) · Handbook of clinical neurology · doi:10.1016/b978-0-12-820107-7.00005-7 · Cited by 19
Chronic central oxytocin infusion impairs sociability in mandarin voles
Du, P., He, Z., Cai, Z., Hao, X., Dong, N., Yuan, W., Hou, W., Yang, J., Jia, R., & Tai, F. (2017) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2017.09.006 · Cited by 14
“to a stranger in female prairie voles (Williams et al., 1992).”
InfluentialKrentzel, A. A., Kimble, L. C., Dorris, D. M., Horman, B. M., Meitzen, J., & Patisaul, H. B. (2021) · Hormones and Behavior · doi:10.1016/j.yhbeh.2021.105019 · Cited by 14
Partner separation rescues pair bond-induced decreases in hypothalamic oxytocin neural densities
Fricker, B. A., Roshko, V. C., Jiang, J., & Kelly, A. M. (2023) · Scientific Reports · doi:10.1038/s41598-023-32076-8 · Cited by 15
Everyday co-presence with a romantic partner is associated with lower C-reactive protein
Jolink, T. A., Way, B. M., Younge, A. N., Oveis, C., & Algoe, S. B. (2022) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2022.09.007 · Cited by 13
Walcott, A. T., & Ryabinin, A. E. (2019) · Alcohol and Alcoholism · doi:10.1093/alcalc/agz041 · Cited by 12
“PPT has been described previously (Williams et al., 1992; Ahern et al., 2009).”
The Role of Early Life Experience and Species Differences in Alcohol Intake in Microtine Rodents
Anacker, A. M. J., Ahern, T. H., Young, L. J., & Ryabinin, A. E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039753 · Cited by 13
“[8,9,10,11,12].”
Gillera, S. E. A., Marinello, W. P., Nelson, M. A., Horman, B. M., & Patisaul, H. B. (2022) · Toxics · doi:10.3390/toxics10050268 · Cited by 11
Dumais, K. M., & Veenema, A. H. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-802114-9.00011-1 · Cited by 11
Wallace, K. J., Chun, E. K., Manns, J. R., Ophir, A. G., & Kelly, A. M. (2023) · Hormones and Behavior · doi:10.1016/j.yhbeh.2023.105362 · Cited by 9
“Like studies before (Williams et al., 1992; Winslow et al., 1993; Young et al., 2008), we found that non-bonded males were more pro-social across all contexts than pair bonded males, whereas pair bonded males were more aggressive.”
Oxytocin and object preferences in the male prairie vole
Madularu, D., Athanassiou, M., Yee, J. R., Kenkel, W. M., Carter, C. S., & Mumby, D. G. (2014) · Peptides · doi:10.1016/j.peptides.2014.08.015 · Cited by 11
Metadata
- Authors
- WILLIAMS, J. R., CARTER, C. S., & INSEL, T.
- Affiliations
- University of Maryland, College Park (US)
- National Institutes of Health (US)
- Venue
- Annals of the New York Academy of Sciences
- Publisher
- Wiley
- Published
- 1992-06
- Volume
- 652
- Issue
- 1
- Pages
- 487-489
- ISSN
- 0077-8923 (ISSN-L)
- 1749-6632
- OpenAlex
- W2047822585
- Cited by
- 147
- References
- 4
- Citations by year
- 2026: 4 · 2025: 2 · 2024: 3 · 2023: 8 · 2022: 7 · 2021: 12 · 2020: 5 · 2019: 8 · 2018: 8 · 2017: 8 · 2016: 8 · 2015: 12 · 2014: 11 · 2013: 4 · 2012: 6
- FWCI
- 0.00
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Annals of the New York Academy of Sciences (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Keywords
- mate preferences, Microtus ochrogaster, oxytocin, mating, female social behavior, cohabitation, social bonding, estradiol, monogamy
- MeSH terms
- Animals, Arvicolinae, Estradiol, Estrus, Female, Injections, Intraventricular, Male, Ovariectomy, Oxytocin, Pair Bond, Sexual Behavior, Animal, Time Factors
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