The DOI matches its Crossref record; 88 of the 88 references it cites were found in a registry or an index.
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“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]
The cited source says what the claim attributes to it.
In the citing paper
“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]
In the citing paper
“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]
In the citing paper
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Meaney, M. J. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1161 · Cited by 2,708
(1973) · Cited by 2,004
Nongenomic Transmission Across Generations of Maternal Behavior and Stress Responses in the Rat
Francis, D., Diorio, J., Liu, D., & Meaney, M. J. (1999) · Science · doi:10.1126/science.286.5442.1155 · Cited by 1,965
Oxytocin, vasopressin, and the neurogenetics of sociality
Donaldson, Z. R., & Young, L. J. (2008) · Science · doi:10.1126/science.1158668 · Cited by 1,645
The neurobiology of pair bonding.
Young, L. J., & Wang, Z. (2004) · Nature Neuroscience · doi:10.1038/nn1327 · Cited by 1,523 · cited 10×
“Virgins of both sexes are highly social and exhibit spontaneous nurturing (or alloparental) care toward unrelated pups; adults form selective social attachments (or pair bonds) between mates; and breeding pairs usually display robust biparental (BP) care of offspring (Getz et al., 1981, 1993; Carter et al., 1995; Lons…”
InfluentialCaldji, C., Tannenbaum, B., Sharma, S., Francis, D., Plotsky, P. M., & Meaney, M. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.9.5335 · Cited by 1,437
Kleiman, D. G. (1977) · The Quarterly Review of Biology · doi:10.1086/409721 · Cited by 1,436
Maternal care, hippocampal synaptogenesis and cognitive development in rats
Liu, D., Diorio, J., Day, J. C., Francis, D. D., & Meaney, M. J. (2000) · Nature Neuroscience · doi:10.1038/77702 · Cited by 1,195
A role for central vasopressin in pair bonding in monogamous prairie voles
Winslow, J. T., Hastings, N., Carter, C. S., Harbaugh, C. R., & Insel, T. R. (1993) · Nature · doi:10.1038/365545a0 · Cited by 948 · cited 1×
“Arginine vasopressin (AVP), acting through the vasopressin 1a receptor (V1aR), shows similar effects, predominately in males (Winslow et al., 1993; Wang et al., 1994).”
Lim, M. M., Wang, Z., Olazábal, D. E., Ren, X., Terwilliger, E. F., & Young, L. J. (2004) · Nature · doi:10.1038/nature02539 · Cited by 628
Cited by
Sorted by citations
Oxytocin-dependent consolation behavior in rodents
Burkett, J. P., Andari, E., Johnson, Z. V., Curry, D. C., de Waal, F. B. M., & Young, L. J. (2016) · Science · doi:10.1126/science.aac4785 · Cited by 692
Feldman, R., Gordon, I., Schneiderman, I., Weisman, O., & Zagoory-Sharon, O. (2010) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.01.013 · Cited by 638
Feldman, R., Gordon, I., & Zagoory‐Sharon, O. (2011) · Developmental Science · doi:10.1111/j.1467-7687.2010.01021.x · Cited by 486
Oxytocin and the development of parenting in humans
Gordon, I., Zagoory-Sharon, O., Leckman, J. F., & Feldman, R. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.02.005 · Cited by 469
Exogenous and evoked oxytocin restores social behavior in the Cntnap2 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
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)
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
