The oxytocin system promotes resilience to the effects of neonatal isolation on adult social attachment in female prairie voles
Open accessAbstract
Genes and social experiences interact to create variation in social behavior and vulnerability to develop disorders of the social domain. Socially monogamous prairie voles display remarkable diversity in neuropeptide receptor systems and social behavior. Here, we examine the interaction of early-life adversity and brain oxytocin receptor (OTR) density on adult social attachment in female prairie voles. First, pups were isolated for 3 h per day, or unmanipulated, from postnatal day 1–14. Adult subjects were tested on the partner preference (PP) test to assess social attachment and OTR density in the brain was quantified. Neonatal social isolation impaired female PP formation, without affecting OTR density. Accumbal OTR density was, however, positively correlated with the percent of time spent huddling with the partner in neonatally isolated females. Females with high accumbal OTR binding were resilient to neonatal isolation. These results are consistent with the hypothesis that parental nurturing shapes neural systems underlying social relationships by enhancing striatal OTR signaling. Thus, we next determined whether early touch, mimicking parental licking and grooming, stimulates hypothalamic OT neuron activity. Tactile stimulation induced immediate-early gene activity in OT neurons in neonates. Finally, we investigated whether pharmacologically potentiating OT release using a melanocortin 3/4 agonist, melanotan-II (10 mg kg−1 subcutaneously), would mitigate the social isolation-induced impairments in attachment behavior. Neonatal melanotan-II administration buffered against the effects of early isolation on partner preference formation. Thus, variation in accumbal OTR density and early OT release induced by parental nurturing may moderate susceptibility to early adverse experiences, including neglect.
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Repeated neonatal social isolations disrupt adult pair-bonding in voles with low accumbens receptor density but not in those with high receptor density.
“Repeated neonatal social isolations (modeling neglect) disrupt adult pair-bonding in voles with low accumbens receptor density but not in those with high receptor density, suggesting that accumbens oxytocin signaling promotes resilience to early-life neglect (Barrett et al. 2015).”
From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Barrett et al. 2015
In Experiment 1 (Results), early-isolated females with low accumbens oxytocin receptor binding did not show a partner preference, whereas those with high binding did. The claim says “voles” without specifying females; the Discussion calls the male data inconclusive, so the finding cannot be extended to males. (LLM, conf=0.86)
Experimental — accuracy not yet measuredAccumbens oxytocin signaling promotes resilience to early-life neglect.
“suggesting that accumbens oxytocin signaling promotes resilience to early-life neglect (Barrett et al. 2015).”
From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Barrett et al. 2015
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 [39]
Prairie vole females that experienced early-life separation from parents and littermates for 3 h per day for the first two weeks of life displayed an impairment in the ability to form pair bonds as adults.
“As adults, females that experienced this early-life separation, modeling parental neglect, displayed an impairment in the ability to form pair bonds.”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [66]
Some females were resilient to early-life neglect and formed bonds normally, while others were susceptible and unable to form bonds.
“Interestingly, not all females responded in the same way to this early neglect; some were resilient, forming bonds normally, while others were susceptible and unable to form bonds.”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [66]
Females with the highest density of oxytocin receptors in the nucleus accumbens were resilient to early-life neglect and formed bonds, while those with lower OXTR density were impaired in pair bond formation.
“Further investigation revealed that those females with the highest density of OXTR in the NAc were resilient to early-life neglect and formed bonds, while those with lower OXTR density were impaired in pair bond formation.”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [66]
Prairie voles with high nucleus accumbens oxytocin receptor levels show resilience to early life stress.
“and resilience to early life stress (23).”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [23]
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 [23]
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 [23]
MC4R agonists interact with other neurochemical systems relevant to behaviour.
“Although MC4R agonists show promise for eliciting OT-mediated behaviours, they also interact with other behaviourally relevant neurochemical systems (23) and thus are not useful tools for isolating OT function.”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [23]
MC4R agonists cannot isolate OT function.
“Although MC4R agonists show promise for eliciting OT-mediated behaviours, they also interact with other behaviourally relevant neurochemical systems (23) and thus are not useful tools for isolating OT function.”
From Comparative Perspectives on Oxytocin and Vasopressin Receptor Research in Rodents and Primates: Translational Implications (2016) · cites this paper as [23]
Variation in nucleus accumbens OXTR density is correlated with individual differences in monogamy-related behavior in male prairie voles in naturalistic settings.
“Variation in NAcc OXTR density is correlated with individual differences in monogamy-related behavior in males in naturalistic settings (40).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [40]
The study confirms a genetic contribution of naturally occurring OXTR density differences to individual variation in social behavior.
“Here, we confirm a genetic role for naturally occurring OXTR density differences that contribute to individual variation in social behavior (36, 40).”
From Variation in the Oxytocin Receptor Gene Predicts Brain Region–Specific Expression and Social Attachment (2016) · cites this paper as [40]
Female prairie voles with low densities of OTR in the NAc who also experienced neglect failed to form partner preferences.
“those females with low densities of OTR in the NAc who also experienced neglect failed to form partner preferences”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Barrett et al. 2015
As adults, female but not male prairie voles subjected to 3 h daily social isolation from days 1-14 displayed significant impairment in pair bond formation even after 48 h of cohabitation with a male partner.
“As adults (e.g., ~90 days of age), female, but not male, prairie voles displayed a significant impairment in pair bond formation even after 48 h of cohabitation with a male partner”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Barrett et al. 2015
Female prairie voles with naturally high densities of OTR binding in the NAc were resilient to disruptions in early-life attachment behaviors and formed partner preferences as adults normally.
“those females with naturally high densities of OTR binding in the NAc were resilient to disruptions in early-life attachment behaviors and formed partner preferences as adults normally”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Barrett et al. 2015
Pups experiencing neonatal social isolations injected with Melanotan II form normal social attachments as adults.
“Indeed, if pups experiencing the neonatal social isolations are injected with the OT system-stimulant Melanotan II (Barrett et al. 2015) they form normal social attachments as adults.”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Barrett et al. 2015
Neonatal social isolation did not influence OTR density in the NAc.
“Neonatal social isolation did not influence OTR density in the NAc”
From Oxytocin and Social Relationships: From Attachment to Bond Disruption (2017) · cites this paper as Barrett et al. 2015
Robust individual differences in the nucleus accumbens relate to individual variation in alloparental nurturing behavior, and resilience to early-life adversity with respect to later-life pair bonding.
“Robust individual differences in NAcc relate to individual variation in alloparental nurturing behavior, and resilience to early-life adversity with respect to later-life pair bonding (142, 143).”
From Oxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities (2022) · cites this paper as [142]
Striatal oxytocin receptor density predicts resiliency to early-life neglect with respect to adult social bonding.
“which predicts resiliency to early-life neglect with respect to adult social bonding [14].”
From Translational opportunities for circuit-based social neuroscience: advancing 21st century psychiatry (2021) · cites this paper as [14]
Huddling was used as an index for social attachment in the present study in accordance with a previous report.
“We used huddling as an index for social attachment in the present study in accordance with a previous report (Barrett et al., 2015).”
From Helping behavior in prairie voles: a model of empathy and the importance of oxytocin (2022) · cites this paper as Barrett et al., 2015
Individual variation in oxytocin receptor density in the nucleus accumbens predicts how early life social experiences shape later social attachment behaviors.
“Further, individual variation in OTR density in the NAcc predicts how early life social experiences shape later social attachment behaviors (Barrett et al. 2015).”
From A precision medicine approach to oxytocin trials (2017) · cites this paper as Barrett et al. 2015
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Self-citationProduction and Characterization of Monoclonal Antibodies
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The Neurobiology of Human Attachments
Feldman, R. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2016.11.007 · Cited by 839 · see citing works
Oxytocin, Neural Plasticity, and Social Behavior
Froemke, R. C., & Young, L. J. (2021) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-102320-102847 · Cited by 487 · see citing works
“Repeated neonatal social isolations (modeling neglect) disrupt adult pair-bonding in voles with low accumbens receptor density but not in those with high receptor density, suggesting that accumbens oxytocin signaling promotes resilience to early-life neglect (Barrett et al. 2015).”
BackgroundSelf-citationThe 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 · see citing works
Self-citationStatistical and Methodological Considerations for the Interpretation of Intranasal Oxytocin Studies
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“For example, melanocortin receptor agonists potentiate central OT release in the brain (37, 38), facilitate OT-dependent partner preferences in prairie voles (35, 37, 39, 40), and mimic the prosocial effects of OT in a mouse model of autism (41).”
BackgroundSelf-citationJohnson, Z. V., & Young, L. J. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.01.034 · Cited by 242 · see citing works
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“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).”
BackgroundSelf-citationIn the search for integrative biomarker of resilience to psychological stress
Walker, F. R., Pfingst, K., Carnevali, L., Sgoifo, A., & Nalivaiko, E. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.05.003 · Cited by 211 · see citing works
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“Furthermore, variation in prairie vole NAc OXTR confers susceptibility or resilience to the effects of daily neonatal isolations, a model of neglect, in relation to the ability to form social attachments as adults (40).”
Self-citationOxytocin, Vasopressin, and Social Behavior: From Neural Circuits to Clinical Opportunities
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Self-citationOxytocin and Social Relationships: From Attachment to Bond Disruption
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Self-citationRoles of Oxytocin in Stress Responses, Allostasis and Resilience
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Touching the social robot PARO reduces pain perception and salivary oxytocin levels
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Oxytocin receptors modulate a social salience neural network in male prairie voles
Johnson, Z. V., Walum, H., Xiao, Y., Riefkohl, P. C., & Young, L. J. (2017) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.10.009 · Cited by 113 · see citing works
Self-citationRole of oxytocin in the control of stress and food intake
Onaka, T., & Takayanagi, Y. (2019) · Journal of Neuroendocrinology · doi:10.1111/jne.12700 · Cited by 98 · see citing works
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Early secure attachment as a protective factor against later cognitive decline and dementia
Walsh, E., Blake, Y., Donati, A., Stoop, R., & von Gunten, A. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00161 · Cited by 84 · see citing works
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Rebalancing the Addicted Brain: Oxytocin Interference with the Neural Substrates of Addiction
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Self-citationMother-newborn separation at birth in hospitals: A possible risk for neurodevelopmental disorders?
Császár-Nagy, N., & Bókkon, I. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.08.013 · Cited by 73 · see citing works
Early Life Experience Shapes Male Behavior and Social Networks in Drosophila
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Self-citationThalamic integration of social stimuli regulating parental behavior and the oxytocin system
Dobolyi, A., Cservenák, M., & Young, L. J. (2018) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2018.05.002 · Cited by 64 · see citing works
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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
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The 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 · see citing works
“In one study, prairie vole pups were isolated from their parents and littermates for 3 h per day for the first two weeks of life, then raised normally by both parents [66].”
MethodSelf-citationThe oxytocin system and early‐life experience‐dependent plastic changes
Onaka, T., & Takayanagi, Y. (2021) · Journal of Neuroendocrinology · doi:10.1111/jne.13049 · Cited by 60 · see citing works
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Oxytocin and excitation/inhibition balance in social recognition
Lopatina, O. L., Komleva, Y. K., Gorina, Y. V., Olovyannikova, R. Y., Труфанова, Л. В., Hashimoto, T., Takahashi, T., Kikuchi, M., Minabe, Y., Higashida, H., et al. (2018) · Neuropeptides · doi:10.1016/j.npep.2018.09.003 · Cited by 51 · see citing works
Pain, Parental Involvement, and Oxytocin in the Neonatal Intensive Care Unit
Filippa, M., Poisbeau, P., Mairesse, J., Monaci, M. G., Baud, O., Hüppi, P. S., Grandjean, D., & Kuhn, P. (2019) · Frontiers in Psychology · doi:10.3389/fpsyg.2019.00715 · Cited by 56 · see citing works
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“Oxytocin (OXT) and oxytocin receptor (OXTR) are one of the key neuromodulators and receptors mediating pair bond formation and maintenance in prairie voles (Donaldson and Young, 2008; Smith and Wang, 2014; Barrett et al., 2015; Bosch, et al., 2016; Johnson et al., 2016, 2017; Walum and Young, 2018).”
BackgroundSelf-citationTranslational opportunities for circuit-based social neuroscience: advancing 21st century psychiatry
Ford, C. L., & Young, L. J. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.11.007 · Cited by 46 · see citing works
Self-citationInoue, K., Ford, C. L., Horie, K., & Young, L. J. (2022) · Journal of Comparative Neurology · doi:10.1002/cne.25382 · Cited by 45 · see citing works
Self-citationA neuroendocrine account of facial mimicry and its dynamic modulation
Kraaijenvanger, E. J., Hofman, D., & Bos, P. A. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2017.03.006 · Cited by 46 · see citing works
Birth signalling hormones and the developmental consequences of caesarean delivery
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Additive effects of oxytocin receptor gene polymorphisms on reward circuitry in youth with autism
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Effects of Stroking on Salivary Oxytocin and Cortisol in Guide Dogs: Preliminary Results
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Self-citationA precision medicine approach to oxytocin trials
Andari, E., Hurlemann, R., & Young, L. J. (2017) · Current Topics in Behavioral Neurosciences · doi:10.1007/7854_2017_29 · Cited by 40 · see citing works
Self-citationSocial buffering of stress – Physiological and ethological perspectives
Wu, A. (2021) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2021.105325 · Cited by 39 · see citing works
Brain functional networks associated with social bonding in monogamous voles
López-Gutiérrez, M. F., Gracia-Tabuenca, Z., Ortiz, J. J., Camacho, F., Young, L. J., Paredes, R. G., Díaz, N. F., Portillo, W., & Alcauter, S. (2021) · eLife · doi:10.7554/elife.55081 · Cited by 40 · see citing works
Self-citationJeste, D. V., Malaspina, D., Bagot, K. S., Barch, D. M., Cole, S. W., Dickerson, F., Dilmore, A. H., Ford, C. L., Karcher, N. R., Luby, J. L., et al. (2023) · Schizophrenia Bulletin · doi:10.1093/schbul/sbad031 · Cited by 38 · see citing works
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Helping behavior in prairie voles: a model of empathy and the importance of oxytocin
Kitano, K., Yamagishi, A., Horie, K., Nishimori, K., & Sato, N. (2022) · iScience · doi:10.1016/j.isci.2022.103991 · Cited by 31 · see citing works
Oxytocin, vasopressin and social behavior in the age of genome editing: a comparative perspective
Boender, A. J., & Young, L. J. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104780 · Cited by 30 · see citing works
Self-citationOxytocin Neurons Exhibit Extensive Functional Plasticity Due To Offspring Age in Mothers and Fathers
Kelly, A. M., Hiura, L. C., Saunders, A. G., & Ophir, A. G. (2017) · Integrative and Comparative Biology · doi:10.1093/icb/icx036 · Cited by 30 · see citing works
Bridging the gap between rodents and humans: The role of non‐human primates in oxytocin research
Putnam, P. T., Young, L. J., & Gothard, K. M. (2018) · American Journal of Primatology · doi:10.1002/ajp.22756 · Cited by 28 · see citing works
“This variation in density has been linked to individual differencesinalloparentalbehavior (Olazábal& Young,2006a,2006b), pair-bonding (King et al., 2016; Ross, Cole, et al., 2009; Ross, Freeman, et al., 2009), and resilience to early-life social neglect (Barrett, Arambula, & Young, 2015).”
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Self-citation
- Authors
- Barrett, C. E., Arambula, S. E., & Young, L. J.
- Affiliations
- Emory University (US)
- Corresponding author
- Barrett, C E
- Venue
- Translational Psychiatry
- Published
- 2015-07-21
- Volume
- 5
- Issue
- 7
- Pages
- e606-e606
- ISSN
- 2158-3188 (ISSN-L)
- PMC
- PMC5068726
- OpenAlex
- W1033049088
- Cited by
- 115
- References
- 114
- Citations by year
- 2026: 6 · 2025: 3 · 2024: 7 · 2023: 8 · 2022: 11 · 2021: 13 · 2020: 9 · 2019: 12 · 2018: 12 · 2017: 16 · 2016: 12 · 2015: 6
- FWCI
- 25.09
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Translational Psychiatry (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Science Foundation
- Autism Speaks
- National Institutes of Health (P51OD011132)
- Yerkes National Primate Research Center, Emory University (P51OD11132, /OD P51OD11132)
- National Institute of Mental Health (R01MH096983, P50MH100023)
- National Institute of General Medical Sciences (R01GM085391)
- National Institute of Neurological Disorders and Stroke (T32NS096050)
- Office of Research Infrastructure Programs, National Institutes of Health
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- oxytocin receptor, neonatal isolation, social attachment, mate preferences, Microtus ochrogaster, childhood adversity, melanotan II, social monogamy, female social behavior
- MeSH terms
- alpha-MSH, Animals, Animals, Newborn, Arvicolinae, Female, Object Attachment, Oxytocin, Peptides, Cyclic, Social Behavior, Social Isolation, Vasopressins, Gene Expression, Receptors, Oxytocin, Receptors, Melanocortin, Resilience, Psychological
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