The DOI matches its Crossref record; 33 of the 34 references it cites were found in a registry or an index.
Cohabitation alters vasopressin innervation and paternal behavior in prairie voles (Microtus ochrogaster)
Abstract
The density of vasopressin-immunoreactive (AVP-ir) fibers in the lateral septum and lateral habenular nucleus is lower in prairie vole fathers--which display paternal behavior under natural conditions-than in sexually naive males. To see if these changes occur before or after the birth of pups, and whether they are related to changes in paternal behavior, we tested paternal responsiveness and measured AVP-ir fiber density in the lateral septum, lateral habenular nucleus, medial preoptic area, and paraventricular nucleus of the thalamus of sexually naive males and females (0P) and breeding pairs that were sacrificed shortly after mating (3P); during early (13P); or late gestation (21P); or after the birth of pups (6PP). Paternal responsiveness was increased in 3P males and reached a plateau in 13P males. AVP-ir fiber density did not change in the medial preoptic area and the paraventricular nucleus of the thalamus. The fiber density in the lateral septum and lateral habenular nucleus was affected differently in males and females. Among males, 3P animals had the lowest fiber density, while 13P and 6PP animals had an intermediate, and 0P and 21P animals the highest fiber density, whereas among females, no differences in fiber density were found. A second experiment showed that the decrease in fiber density in 3P males could be induced by cohabitation with an unfamiliar female but not by an unfamiliar male nor by relocation to a novel cage. The changes in AVP-ir fiber density shortly after mating suggest that these fibers may be involved in paternal responsiveness as well as in various other social behaviors that change after mating.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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?
In the citing paper
“Early comparative studies discovered that in prairie voles, cohabitation with a female resulted in a decrease in AVP content in the lateral septum (likely reflecting a release of AVP from neuronal fibers in the region), which was coincident with an increase in paternal responsiveness.”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [36]
In the citing paper
“This phenomenon was not observed in meadow voles [36, 37].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [36]
Citations
Cites
The Physiology of Reproduction
Legendre, M., & Jalabert, B. (1988) · Annals of Internal Medicine · doi:10.7326/0003-4819-109-2-176_1 · Cited by 7,876
The Physiology of Reproduction
Blandau, R. J. (1988) · JAMA · doi:10.1001/jama.1988.03410200127050 · Cited by 3,000
Oxytocin induces maternal behavior in virgin female rats
Pedersen, C. A., Ascher, J. A., Monroe, Y. L., & Prange, A. J. (1982) · Science · doi:10.1126/science.7071605 · Cited by 770
The vasopressinergic innervation of the brain in normal and castrated rats
DeVries, G. J., Buijs, R. M., van Leeuwen, F. W., Caffé, A. R., & Swaab, D. F. (1985) · Journal of Comparative Neurology · doi:10.1002/cne.902330206 · Cited by 522
Getz, L. L., Carter, C. S., & Gavish, L. (1981) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00299829 · Cited by 466
Role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster).
Wang, Z., Ferris, C. F., & De Vries, G. J. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.1.400 · Cited by 381
The biparental care system of the California mouse, Peromyscus californicus.
Gubernick, D. J., & Alberts, J. R. (1987) · Journal of comparative psychology · doi:10.1037/0735-7036.101.2.169 · Cited by 274
Parental care and mating system of the prairie vole, Microtus ochrogaster
Thomas, J. A., & Birney, E. C. (1979) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00293304 · Cited by 244
Social organization in free-living prairie voles, Microtus ochrogaster
Getz, L. L., & Hofmann, J. E. (1986) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00300004 · Cited by 239
Gonadal hormone actions on the morphology of the vasopressinergic innervation of the adult rat brain
De Vries, G. J., Buijs, R. M., & Sluiter, A. A. (1984) · Brain Research · doi:10.1016/0006-8993(84)91157-0 · Cited by 224
Research works printed but not linked: 3
- Årgen, 1976, Social and territorial behaviour in the Mongolian gerbil (Meriones unguiculatus) under seminatural conditions, Biol. Behav., 1, 267
- Dewsbury, 1981, An exercise in the prediction of monogamy in the field from laboratory data on 42 muroid rodents, Biologist, 63, 138
- Wang, 1993, The role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster), Soc. Neurosci. Abstr., 19, 1452
Cited by
Sorted by citations
Items 101–160 of 160
Kelly, A. M., & Goodson, J. L. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.09.006 · Cited by 38
Liu, Y., Donovan, M. L., Jia, X., & Wang, Z. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14550 · Cited by 38
EMERGING THEMES AND FUTURE CHALLENGES: FORGOTTEN RODENTS, NEGLECTED QUESTIONS
Tang‐Martínez, Z. (2003) · Journal of Mammalogy · doi:10.1644/ble-015 · Cited by 37
Lambert, K. G., Franssen, C. L., Hampton, J. E., Rzucidlo, A., Hyer, M. M., True, M., Kaufman, C., & Bardi, M. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.12.023 · Cited by 36
Fatherhood Alters Behavioural and Neural Responsiveness in a Spatial Task
Franssen, C. L., Bardi, M., Shea, E. A., Hampton, J. E., Franssen, R. A., Kinsley, C. H., & Lambert, K. G. (2011) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2011.02225.x · Cited by 36
Plasticity of the paternal brain: Effects of fatherhood on neural structure and function
Horrell, N. D., Acosta, M. C., & Wendy Saltzman, A. (2021) · Developmental Psychobiology · doi:10.1002/dev.22097 · Cited by 35
Vries, G. J. D., AL‐SHAMMA, H. A., & ZHOU, L. (1994) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1994.tb55789.x · Cited by 34
Sexual Dimorphism of Parental Care: From Genes to Behavior
Zilkha, N., Scott, N., & Kimchi, T. (2017) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-072116-031447 · Cited by 33
Social recognition in paired, but not single, male prairie voles
Blocker, T. D., & Ophir, A. G. (2015) · Animal Behaviour · doi:10.1016/j.anbehav.2015.07.003 · Cited by 30
Fish as a model in social neuroscience: conservation and diversity in the social brain network
Ogawa, S., Pfaff, D. W., & Parhar, I. S. (2021) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12689 · Cited by 32
Oxytocin 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
Vasopressin and developmental onset of flank marking behavior in golden hamsters
Ferris, C. F., Delville, Y., Brewer, J. A., Mansour, K., Yules, B., & Melloni, R. H. (1996) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199606)30:2 · Cited by 29
BAXTER, A. B., Anderson, M., Seelke, A. M. H., Kinnally, E. L., Freeman, S. M., & Bales, K. L. (2020) · Scientific Reports · doi:10.1038/s41598-020-74243-1 · Cited by 26
Ophir, A. G., Crino, O. L., Wilkerson-Vidal, Q. C., Wolff, J. O., & Phelps, S. M. (2007) · Brain Behavior and Evolution · doi:10.1159/000108609 · Cited by 26
Nonapeptides mediate trade-offs in parental care strategy
DeAngelis, R., Dodd, L., & Rhodes, J. S. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104717 · Cited by 24
Optimization of Laboratory Conditions for the Study of Social Behavior
Wersinger, S. R., & Martin, L. B. E. (2009) · ILAR Journal · doi:10.1093/ilar.50.1.64 · Cited by 24
Vasopressinergic Neurocircuitry Regulating Social Attachment in a Monogamous Species
Tickerhoof, M. C., & Smith, A. S. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00265 · Cited by 26
Bester‐Meredith, J. K., & Marler, C. A. (2012) · Brain Behavior and Evolution · doi:10.1159/000341899 · Cited by 23
Kelly, A. M., Hiura, L. C., & Ophir, A. G. (2018) · Brain Structure and Function · doi:10.1007/s00429-018-1640-2 · Cited by 23
McEwen (2004) · doi:10.1016/s1054-3589(04)50016-9 · Cited by 22
DiBenedictis, B. T., Cheung, H. K., Nussbaum, E. R., & Veenema, A. H. (2019) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2019.104462 · Cited by 21
Wang, J., Tai, F., & Lai, X. (2014) · Neuropeptides · doi:10.1016/j.npep.2013.10.016 · Cited by 20
Paternal behavior in the Mongolian gerbil, and its regulation by social factors, T, ERα, and AR
Martínez, A., Arteaga‐Silva, M., Bonilla‐Jaime, H., Cárdenas, M., Rojas‐Castañeda, J. C., Vigueras‐Villaseñor, R. M., Limón‐Morales, O., & Luis, J. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2018.12.001 · Cited by 20
Wang, L., Zhang, W., Wu, R., Kong, L., Feng, W., Cao, Y., Tai, F., & Zhang, X. (2014) · Developmental Psychobiology · doi:10.1002/dev.21202 · Cited by 19
Askew, A., González, F., Stahl, J. M., & Karom, M. C. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.08.001 · Cited by 19
Parker, K. J., & Lee, T. M. (2001) · Journal of comparative psychology · doi:10.1037/0735-7036.115.4.331 · Cited by 19
Terleph, T. A., Jean‐Baptiste, N., & Bamshad, M. (2004) · Journal of Mammalogy · doi:10.1644/bns-108.1 · Cited by 19
Lowrey, E. M., & Tomaszycki, M. L. (2014) · Behavioral Neuroscience · doi:10.1037/a0035416 · Cited by 17
Emerging Frontiers in Social Neuroendocrinology and the Study of Nonapeptides
Ondrasek, N. R. (2016) · Ethology · doi:10.1111/eth.12493 · Cited by 19
Cavanaugh, B. L., & Lonstein, J. S. (2010) · Physiology & Behavior · doi:10.1016/j.physbeh.2010.03.020 · Cited by 16
Intranasal administration of oxytocin alters sleep architecture
Braga, R. I., Panaitescu, A. M., Bădescu, S., Zăgrean, A., & Zăgrean, L. (2013) · Biological Rhythm Research · doi:10.1080/09291016.2013.797641 · Cited by 15
Chary, M., Cruz, J. P., Bardi, M., & Becker, E. A. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.05.013 · Cited by 13
Parental care in male degus (Octodon degus) is flexible and contingent upon female care
Aspillaga-Cid, A., Vera, D. C., Ebensperger, L. A., & Correa, L. A. (2021) · Physiology & Behavior · doi:10.1016/j.physbeh.2021.113487 · Cited by 13
Terleph, T. A. (2011) · Behaviour · doi:10.1163/000579511x600727 · Cited by 12
Social environment alters central distribution of estrogen receptor alpha in juvenile prairie voles
Ruscio, M. G., Sweeny, T. D., Gomez, A. M., Parker, K., & Carter, C. S. (2009) · Physiology & Behavior · doi:10.1016/j.physbeh.2009.06.005 · Cited by 12
Clark, M. M., & Galef, B. G. (2001) · Developmental Psychobiology · doi:10.1002/dev.1043 · Cited by 11
Paternal care in rodents: Ultimate causation and proximate mechanisms
Gromov, V. S. (2020) · Russian Journal of Theriology · doi:10.15298/rusjtheriol.19.1.01 · Cited by 10
Transcriptomic analysis of paternal behaviors in prairie voles
Duclot, F., Liu, Y., Saland, S. K., Wang, Z., & Kabbaj, M. (2022) · BMC Genomics · doi:10.1186/s12864-022-08912-y · Cited by 11
Parker, J. T., Rodriguez, N. A., Lawal, B., Delevan, C. J., & Bamshad, M. (2011) · Behavioural Processes · doi:10.1016/j.beproc.2011.08.010 · Cited by 10
Female tactile cues maximize paternal behavior in prairie voles
Simoncelli, L. A., Delevan, C. J., Al-Naimi, O. A. S., & Bamshad, M. (2010) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-010-0903-6 · Cited by 10
Association between parental behaviors and structural plasticity in the brain of male rodents
Inada, K., & Miyamichi, K. (2023) · Neuroscience Research · doi:10.1016/j.neures.2023.06.007 · Cited by 9
Jean‐Baptiste, N., Terleph, T. A., & Bamshad, M. (2008) · Ethology · doi:10.1111/j.1439-0310.2008.01577.x · Cited by 8
Clark, M. M., Johnson, J., & Galef, B. G. (2003) · Animal Behaviour · doi:10.1016/j.anbehav.2003.02.006 · Cited by 8
Rodriguez, N. A., Legzim, K. M., Aliou, F., Al-Naimi, O. A. S., & Bamshad, M. (2013) · Behavioural Processes · doi:10.1016/j.beproc.2013.10.002 · Cited by 7
Hiura, L. C., Lazaro, V. A., & Ophir, A. G. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2023.1172845 · Cited by 6
A stereotaxic atlas of the forebrain of the bank vole (Clethrionomys glareolus)
Vandebroek, I., Bouche, K., D'Herde, K. G. M. A., Caemaert, J., Roels, F., & Ödberg, F. O. (1999) · Brain Research Bulletin · doi:10.1016/s0361-9230(98)00137-3 · Cited by 6
The role of avpr1a microsatellite length on reproductive success of female Microtus ochrogaster
Harris, M. N., Alvarez, R. M., Keane, B., Talib, A. D., Eiswerth, M. J., & Solomon, N. G. (2014) · Behaviour · doi:10.1163/1568539x-00003178 · Cited by 5
Vasopressin: Roles in Modulating Social Behaviors
Williams, S. K., & Cymerblit‐Sabba, A. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00057-2 · Cited by 5
Lang, D.-L. Y., Bamshad, M., & Dorcely, R. (2019) · Brain Research · doi:10.1016/j.brainres.2019.02.023 · Cited by 4
Yamoah, D., Williams-Baginski, K., & Bamshad, M. J. (2008) · Canadian Journal of Zoology · doi:10.1139/z07-133 · Cited by 4
Neuroendocrinology, Neurochemistry, and Molecular Neurobiology of Affiliative Behavior
Hammock, E. A. D., & Young, L. J. (2006) · Springer eBooks · doi:10.1007/978-0-387-30405-2_6 · Cited by 4
Acland, E. L., Lidhar, N. K., & Martin, L. J. (2018) · Springer eBooks · doi:10.1007/978-3-319-78340-6_10 · Cited by 3
Lang, D.-L. Y., Laryea, W., Fassil, F., & Bamshad, M. (2013) · Current Zoology · doi:10.1093/czoolo/59.3.317 · Cited by 3
Nonapeptide mechanisms of avian social behavior and phenotypic diversity
Goodson, J. L. (2013) · Cambridge University Press eBooks · doi:10.1017/cbo9781139017855.010 · Cited by 2
Bales, K. L., Finnerty-Haggerty, A., Guan, J., Meckler, L., Saenz, J., Sosnowski, M. J., Afrakhteh, S., Hung, C. L., Purewal, R. A., Oliinyk, S. L., et al. (2026) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2026.1779750 · Cited by 1
Behavioral Alterations in Prairie Voles (Microtus ochrogaster) after Parent-Pup Separation
Yamamoto, M. (2023) · ScholarWorks@UMassAmherst (University of Massachusetts Amherst) · doi:10.7275/872107 · Cited by 1
Sex Differences in Neurotransmitters Systems; Vasopressin as an Example
Vries, G. J. D. (2006) · Springer eBooks · doi:10.1007/978-0-387-30405-2_12
Assessing parental experience in a socially monogamous songbird
Bell, B. A. (2017) · doi:10.7282/t3sq936t
Luis, J., & Romero‐Morales, L. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-33657-7.00015-4
Wang (1996) · doi:10.1002/(sici)1096-9861(19960318)366:4
Metadata
- Authors
- Bamshad, M., Novak, M. A., & de Vries, G. J.
- Affiliations
- University of Massachusetts Amherst (US)
- ORCID
- Novak, Melinda A.
- Venue
- Physiology & Behavior
- Publisher
- Elsevier BV
- Published
- 1994-10
- Volume
- 56
- Issue
- 4
- Pages
- 751-758
- ISSN
- 0031-9384 (ISSN-L)
- OpenAlex
- W1991358167
- Cited by
- 162
- References
- 34
- Citations by year
- 2026: 2 · 2023: 3 · 2022: 2 · 2021: 3 · 2020: 4 · 2019: 3 · 2018: 5 · 2017: 7 · 2016: 9 · 2015: 5 · 2014: 8 · 2013: 7 · 2012: 3
- FWCI
- 9.71
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Physiology & Behavior (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (RO1 MH47538)
- 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
- vasopressin, cohabitation, paternal behavior, Microtus ochrogaster, lateral septum, lateral habenula, social behavior, mating, gestation, sex differences, neuroendocrine regulation
- MeSH terms
- Amygdala, Animals, Arginine Vasopressin, Brain, Brain Mapping, Arvicolinae, Female, Immunoenzyme Techniques, Male, Nerve Fibers, Neural Pathways, Pair Bond, Paraventricular Hypothalamic Nucleus, Paternal Behavior, Pregnancy, Preoptic Area, Septum Pellucidum, Thalamic Nuclei
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