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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)
Open accessAbstract
Early social attachments lie at the heart of emotional and social development in many mammals, including humans. In nature, monogamous prairie voles (Microtus ochrogaster) experience considerable natural variation in early social attachment opportunities due to differences in family structure [e.g., single-mothers (SM), solitary breeding pairs, and communal groups]. We exploited some of this natural variation in family structure to examine the influence of early social environment on the development of adult social behavior. First, we characterized the parental care received by pups reared biparentally (BP) or by SM in the laboratory. Second, we examined whether BP- and SM-reared offspring differed in adult nurturing, bonding, and emotional behaviors. Finally, we investigated the effects of rearing condition on neuropeptide systems that regulate adult social behavior [oxytocin (OT), vasopressin, and corticotropin-releasing factor, (CRF)]. Observations revealed that SM-reared pups were exposed more frequently (P < 0.01), licked and groomed less (P < 0.01), and matured more slowly (P < 0.01) than BP-reared pups. In adulthood, there were striking socio-behavioral differences: SM-reared females showed low spontaneous, pup-directed alloparental behavior (P < 0.01) and both males and females from the SM-reared condition showed delayed partner preference formation. While rearing did not impact neuropeptide receptor densities in the ventral forebrain as we predicted, SM-reared animals, particularly females, had increased OT content (P < 0.01) and greater dorsal raphe CRF2 densities (P < 0.05) and both measures correlated with licking and grooming experienced during the first 10 days of life. These results suggest that naturalistic variation in social rearing conditions can introduce diversity into adult nurturing and attachment behaviors.
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“As mentioned previously, prairie voles raised with biparental care, compared to those raised by a mother alone, form more pronounced pair bonds in adulthood.”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [64]
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“Manipulation of OT/AVP levels via direct exposures to exogenous hormones, agonists, or alteration of the social environment can significantly modify the number of OT, AVP, and TH neurons in the PVN, thereby resulting in anxiety-like behavior and alterations of prototypical male and female sociosexual behavior (123–127).”
From Endocrine Disruption of Vasopressin Systems and Related Behaviors (2017) · cites this paper as [125]
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“In adulthood, these same animals are slower to form a preference for their partner, despite normal mating behavior.”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [64]
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“Voles raised by their mother alone, compared to those raised under biparental care, receive less parental nurturing in the form of licking/grooming early in development [64].”
From The Neurobiology of Love and Pair Bonding from Human and Animal Perspectives (2023) · cites this paper as [64]
In the citing paper
“There is now growing evidence that the quality of early life nurturing received can have life-long consequences on adult social behavioral tendencies.”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [39]
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“Varying the family structure also altered the number of OT neurons in the paraventricular nucleus of hypothalamus.”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [39]
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“The single mother-reared pups received less parental nurturing (e.g. licking and grooming) than biparentally-reared pups.”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [39]
In the citing paper
“In addition, females raised in single mother units were less likely to display alloparental behavior and both male and female offspring from this group required longer cohabitation periods than biparentally reared offspring to form partner preferences [39].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [39]
In the citing paper
“In addition, females raised in single mother units were less likely to display alloparental behavior and both male and female offspring from this group required longer cohabitation periods than biparentally reared offspring to form partner preferences [39].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [39]
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Metadata
- Authors
- Ahern, T. H.
- Affiliations
- Emory University (US)
- Corresponding author
- Ahern, Todd H
- ORCID
- Ahern, Todd H
- Venue
- Frontiers in Behavioral Neuroscience
- Publisher
- Frontiers Media SA
- Published
- 2009
- Volume
- 3
- Pages
- 17-17
- ISSN
- 1662-5153 (ISSN-L)
- PMC
- PMC2742665
- OpenAlex
- W1991733912
- Cited by
- 239
- References
- 86
- Citations by year
- 2026: 9 · 2025: 6 · 2024: 7 · 2023: 18 · 2022: 30 · 2021: 14 · 2020: 21 · 2019: 13 · 2018: 13 · 2017: 15 · 2016: 13 · 2015: 22 · 2014: 10 · 2013: 13 · 2012: 11
- FWCI
- 15.17
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Behavioral Neuroscience (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Science Foundation (9876754)
- National Institutes of Health (IBN-9876754, RR‐00165)
- National Institute of Mental Health (K02MH064692, MH064692, MH77776, MH0732505, R01MH077776)
- National Center for Research Resources (P51RR000165)
- 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 › Agricultural and Biological Sciences › Animal Science and Zoology › Human-Animal Interaction Studies
- Keywords
- Microtus ochrogaster, family structure, social attachment, parental care, oxytocin, vasopressin, corticotropin-releasing factor, mate preferences, social bonding, licking and grooming, neuropeptide receptors, dorsal raphe nucleus, monogamy, early life experience, social development (developmental psychology)
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