The DOI matches its Crossref record; 69 of the 69 references it cites were found in a registry or an index.
Oxytocin receptors in the nucleus accumbens facilitate “spontaneous” maternal behavior in adult female prairie voles
Abstract
Oxytocin and the nucleus accumbens have been extensively implicated in the regulation of maternal behavior, and the processing of pup-related stimuli relevant for this behavior. Oxytocin receptor density in the nucleus accumbens is highly variable in virgin female prairie voles, as is their behavioral response to pups, ranging from neglecting and infanticidal to full maternal behavior. We hypothesized that oxytocin receptor in the nucleus accumbens facilitates the expression of "spontaneous" maternal behavior in prairie voles. Forty sexually-naive adult females were exposed to pups for the first time and tested for maternal behavior. Oxytocin receptor binding in the nucleus accumbens and other brain regions was later determined using autoradiography. Females that showed maternal behavior (lick and groom the pups and hover over them for at least 30 s, n=24) had higher oxytocin receptor density in the nucleus accumbens (shell subregion) (P<0.05) than females that did not show maternal behavior or attacked the pups (n=16). No differences were found in other brain regions (medial preoptic area, septum, prelimbic cortex). In a second experiment, we tested whether infusions of the oxytocin receptor antagonist (d(CH2)5(1),Tyr(Me)2,Orn8)-AVT into the nucleus accumbens would block "spontaneous" maternal behavior. As a control region, oxytocin receptor antagonist was also infused into the caudate putamen. Ten females were infused bilaterally into the nucleus accumbens or caudate putamen with either 2 ng/0.5 microl of oxytocin receptor antagonist or CSF (vehicle). While five of 10 nucleus accumbens CSF-infused animals showed maternal behavior, none of the nucleus accumbens oxytocin receptor antagonist-infused subjects did (0/10; chi2, P<0.01). Nucleus accumbens oxytocin receptor antagonist-infused females recovered the next day and were not different from controls. Animals infused with CSF or oxytocin receptor antagonist into the caudate putamen did not differ (four/10, four/10). This is the first study to show that the nucleus accumbens is involved in the regulation of "spontaneous" maternal behavior and that oxytocin receptor in this brain region facilitates maternal responses.
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
“Prairie voles are highly nurturing, and virgin females can display spontaneous levels of maternal care depending on density of nucleus accumbens oxytocin receptors”
From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Olazábal & Young 2006
In the citing paper
“When administered intranasally to human subjects, OT stimulates behaviors consistent with an enhancement of interpersonal trust during economic games [99].”
From Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior (2009) · cites this paper as [99]
In the citing paper
“For example, among virgin female prairie voles, a cooperative breeding species, alloparent behavior was positively correlated with oxytocin receptor density (Olazabal and Young, 2006) and when given an oxytocin receptor antagonist, adult female alloparent behavior was completely absent.”
From The evolved nest, oxytocin functioning, and prosocial development (2023) · cites this paper as Olazabal and Young (2006)
In the citing paper
“For example, among virgin female prairie voles, a cooperative breeding species, alloparent behavior was positively correlated with oxytocin receptor density (Olazabal and Young, 2006) and when given an oxytocin receptor antagonist, adult female alloparent behavior was completely absent.”
From The evolved nest, oxytocin functioning, and prosocial development (2023) · cites this paper as Olazabal and Young (2006)
In the citing paper
“Oxytocin transmission and oxytocin receptors in the NAc seem to facilitate maternal behavior in female voles [546].”
From Reward circuitry dysfunction in psychiatric and neurodevelopmental disorders and genetic syndromes: animal models and clinical findings (2012) · cites this paper as [546]
In the citing paper
“Further, an infusion OTR antagonist into the NAcc prevents the display of spontaneous maternal behavior [33].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [33]
In the citing paper
“Approximately 60% of adult females display spontaneous maternal nurturing toward novel pups, while 40% either ignore or attack pups [33–35].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [33]
In the citing paper
“For example, virgin female prairie voles that display maternal behavior have higher densities of OTR in the NAcc than non-maternal females [33, 34].”
From The prairie vole: An emerging model organism for understanding the social brain (2010) · cites this paper as [33]
Citations
Cites
What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?
Berridge, K. C., & Robinson, T. E. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(98)00019-8 · Cited by 4,127
Ikemoto, S., & Panksepp, J. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00023-5 · Cited by 1,450
Uvnäs-Moberg, K. (1998) · Psychoneuroendocrinology · doi:10.1016/s0306-4530(98)00056-0 · Cited by 966
Pedersen, C. A., & Prange, A. J. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.12.6661 · Cited by 841
Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles
Insel, T. R., & Shapiro, L. E. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.13.5981 · Cited by 833
Salamone, J. D., & Correa, M. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00282-6 · Cited by 817
Kelley, A. E. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.016 · Cited by 788
Nonhormonal basis of maternal behavior in the rat
Rosenblatt, J. S. (1967) · Science · doi:10.1126/science.156.3781.1512 · Cited by 721
Champagne, F., Diorio, J., Sharma, S., & Meaney, M. J. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.221224598 · Cited by 707
Berridge, K. C. (2003) · Brain and Cognition · doi:10.1016/s0278-2626(03)00014-9 · Cited by 701
The Neurobiology of Parental Behavior
(2003) · Hormones, Brain, and Behavior · doi:10.1007/b97533 · Cited by 684
Liu, Y., & Wang, Z. X. (2003) · Neuroscience · doi:10.1016/s0306-4522(03)00555-4 · Cited by 580
Cho, M. M., DeVries, A. C., Williams, J. R., & Carter, C. S. (1999) · Behavioral Neuroscience · doi:10.1037/0735-7044.113.5.1071 · Cited by 529
Cellular Mechanisms of Social Attachment
Young, L. J., Lim, M. M., Gingrich, B., & Insel, T. R. (2001) · Hormones and Behavior · doi:10.1006/hbeh.2001.1691 · Cited by 523
Self-citationFrancis, D. D., Champagne, F. C., & Meaney, M. J. (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00599.x · Cited by 496
Insel, T. R. (1992) · Psychoneuroendocrinology · doi:10.1016/0306-4530(92)90073-g · Cited by 487
Pedersen, C. A., Caldwell, J. D., Walker, C., Ayers, G., & Mason, G. A. (1994) · Behavioral Neuroscience · doi:10.1037/0735-7044.108.6.1163 · Cited by 475
Getz, L. L., Carter, C. S., & Gavish, L. (1981) · Behavioral Ecology and Sociobiology · doi:10.1007/bf00299829 · Cited by 466
Neumann, Wigger, Torner, Holsboer, & Landgraf (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00442.x · Cited by 452
Francis, D. D., Young, L. J., Meaney, M. J., & Insel, T. R. (2002) · Journal of Neuroendocrinology · doi:10.1046/j.0007-1331.2002.00776.x · Cited by 415
Self-citationWindle, R. J., Kershaw, Y. M., Shanks, N., Wood, S. A., Lightman, S. L., & Ingram, C. D. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.3432-03.2004 · Cited by 408
Champagne, F. A., Chretien, P., Stevenson, C. W., Zhang, T. Y., Gratton, A., & Meaney, M. J. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5322-03.2004 · Cited by 398
Limbic-Striatal Memory Systems and Drug Addiction
Robbins, T. W. (2002) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2002.4103 · Cited by 379
Developmental consequences of oxytocin
Carter, C. S. (2003) · Physiology & Behavior · doi:10.1016/s0031-9384(03)00151-3 · Cited by 367
Chapter 29 The nucleus accumbens: gateway for limbic structures to reach the motor system?
Groenewegen, H. J., Wright, C. I., & Beijer, A. V. J. (1996) · Progress in brain research · doi:10.1016/s0079-6123(08)61883-x · Cited by 344
Anxiety and stress responses in female oxytocin deficient mice
Amico, J. A., Mantella, R. C., Vollmer, R. R., & Li, X. (2004) · Journal of Neuroendocrinology · doi:10.1111/j.0953-8194.2004.01161.x · Cited by 327
van Leengoed, E., Kerker, E., & Swanson, H. H. (1987) · Journal of Endocrinology · doi:10.1677/joe.0.1120275 · Cited by 300
Keer, S. E., & Stern, J. M. (1999) · Physiology & Behavior · doi:10.1016/s0031-9384(99)00116-x · Cited by 250
Hansen, S., Bergvall, Å. H., & Nyiredi, S. (1993) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(93)90523-v · Cited by 247
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
Forebrain expression of c-fos due to active maternal behaviour in lactating rats
Lonstein, J. S., Simmons, D. A., Swann, J. M., & Stern, J. M. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00283-2 · Cited by 237
Olazábal, D. E., & Young, L. J. (2006) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.12.010 · Cited by 230
Self-citationSex differences in the parental behavior of rodents
Lonstein, J. S., & De Vries, G. J. (2000) · Neuroscience & Biobehavioral Reviews · doi:10.1016/s0149-7634(00)00036-1 · Cited by 226
Oxytocin and Vasopressin Receptors and Species-Typical Social Behaviors
Young, L. J. (1999) · Hormones and Behavior · doi:10.1006/hbeh.1999.1548 · Cited by 211
Self-citationMcGuire, B., & Novak, M. A. (1984) · Animal Behaviour · doi:10.1016/s0003-3472(84)80229-8 · Cited by 207
Central and peripheral effects of oxytocin administration in prairie voles (Microtus ochrogaster)
Witt, D. M., Carter, C. S., & Walton, D. M. (1990) · Pharmacology Biochemistry and Behavior · doi:10.1016/0091-3057(90)90042-g · Cited by 181
Lim, M. M., Murphy, A. Z., & Young, L. J. (2004) · Journal of Comparative Neurology · doi:10.1002/cne.10973 · Cited by 163
Self-citationNuman, M., Numan, M. J., Schwarz, J. M., Neuner, C. M., Flood, T. F., & Smith, C. D. (2004) · Behavioural Brain Research · doi:10.1016/j.bbr.2004.08.008 · Cited by 139
A Selective Oxytocin Antagonist Attenuates Progesterone Facilitation of Female Sexual Behavior
Witt, D. M., & Insel, T. R. (1991) · Endocrinology · doi:10.1210/endo-128-6-3269 · Cited by 138
Oxytocin antiserum delays onset of ovarian steroid-induced maternal behavior
Pedersen, C. A., Caldwell, J. D., Johnson, M. F., Fort, S. A., & Prange, A. J. (1985) · Neuropeptides · doi:10.1016/0143-4179(85)90108-8 · Cited by 137
Li, M., & Fleming, A. S. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(03)00135-9 · Cited by 136
Wang, Z., Liu, Y., Young, L. J., & Insel, T. R. (2000) · Journal of Neuroendocrinology · doi:10.1046/j.1365-2826.2000.00435.x · Cited by 134
Self-citationOntogeny of oxytocin receptors in rat forebrain: A quantitative study
Shapiro, L. E., & Insel, T. R. (1989) · Synapse · doi:10.1002/syn.890040312 · Cited by 131
Phelps, S. M., & Young, L. J. (2003) · Journal of Comparative Neurology · doi:10.1002/cne.10902 · Cited by 116
Self-citationThe role of oxytocin-dopamine interactions in cocaine-induced locomotor hyperactivity
Kovàcs, G. L., Sarnyai, Z., Babarczi, E., Szabó, G., & Telegdy, G. (1990) · Neuropharmacology · doi:10.1016/0028-3908(90)90095-9 · Cited by 101
Stern, J. M., & Taylor, L. A. (1991) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.1991.tb00323.x · Cited by 99
Chapter 19 Neural mediation of nursing and related maternal behaviors
Stern, J. M., & Lonstein, J. S. (2001) · Progress in brain research · doi:10.1016/s0079-6123(01)33020-0 · Cited by 98
Roberts, R. L., Miller, A. K., Taymans, S. E., & Carter, C. S. (1998) · Canadian Journal of Zoology · doi:10.1139/z98-156 · Cited by 95
Li, M., & Fleming, A. S. (2003) · Behavioral Neuroscience · doi:10.1037/0735-7044.117.3.426 · Cited by 90
Maternal motivation of lactating rats is disrupted by low dosages of haloperidol
Stern, J. M., & Keer, S. E. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00108-9 · Cited by 84
Familiarity and gender influence social preferences in prairie voles (Microtus ochrogaster)
DeVries, A. C., Johnson, C. L., & Carter, C. S. (1997) · Canadian Journal of Zoology · doi:10.1139/z97-037 · Cited by 84
Maternal behaviour in sheep and its neuroendocrine regulation
Keverne, B., & Kendrick, K. (1994) · Acta Paediatrica · doi:10.1111/j.1651-2227.1994.tb13265.x · Cited by 82
Ontogeny of maternal behavior in the laboratory rat: Early origins in 18‐ to 27‐day‐old young
Mayer, A. D., & Rosenblatt, J. S. (1979) · Developmental Psychobiology · doi:10.1002/dev.420120502 · Cited by 80
Effects of stress on parental care are sexually dimorphic in prairie voles
Bales, K. L., Kramer, K. M., Lewis‐Reese, A. D., & Carter, C. S. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.11.002 · Cited by 77
Lonstein, J. S. (2002) · Pharmacology Biochemistry and Behavior · doi:10.1016/s0091-3057(02)00952-8 · Cited by 68
Oxytocin and the molecular basis of monogamy.
Insel, T. R., Winslow, J. T., Wang, Z., Young, L. J., & Hulihan, T. J. (1995) · PubMed · Cited by 65
Self-citationFahrbach, S. E., Morrell, J. I., & Pfaff, D. W. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90396-3 · Cited by 60
Olazábal, D. E., & Young, L. J. (2005) · Developmental Psychobiology · doi:10.1002/dev.20077 · Cited by 58
Self-citationLonstein, J. S., & Vries, G. J. D. (2001) · Journal of comparative psychology · doi:10.1037/0735-7036.115.1.53 · Cited by 55
Mayer, A. D., & Rosenblatt, J. S. (1975) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0077045 · Cited by 52
Speculations Concerning the Physiological Significance of Central Oxytocin in Maternal Behavior
McCarthy, M. M., Kow, L., & Pfaff, D. W. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb34347.x · Cited by 50
Oxytocin decreases corticosterone and nociception and increases motor activity in OVX rats
Petersson, M., Eklund, M., & Uvnäs‐Moberg, K. (2004) · Maturitas · doi:10.1016/j.maturitas.2004.10.005 · Cited by 44
Oxytocin and mothering behavior in the rat
Pedersen, C. A., & Prange, A. J. (1985) · Pharmacology & Therapeutics · doi:10.1016/0163-7258(85)90056-7 · Cited by 40
Corticosterone release is heightened in food or water deprived oxytocin deficient male mice
Mantella, R. C., Vollmer, R. R., & Amico, J. A. (2005) · Brain Research · doi:10.1016/j.brainres.2005.07.062 · Cited by 36
Affect and nurturance: Mechanisms mediating maternal behavior in two female mammals
Fleming, A. S., & Anderson, V. N. (1987) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/0278-5846(87)90049-2 · Cited by 30
Uvnäs-Moberg, K., Eklund, M., Hillegaart, V., & Ahlénius, S. (2000) · Regulatory Peptides · doi:10.1016/s0167-0115(99)00112-3 · Cited by 26
Pubertal decline in maternal responsiveness in Long-Evans rats: Maturational influences
Stern, J. M. (1987) · Physiology & Behavior · doi:10.1016/0031-9384(87)90136-3 · Cited by 26
Comparisons of nipple attachment and incisor growth among four species of voles (Microtus)
Salo, A. L., Shapiro, L. E., & Dewsbury, D. A. (1994) · Developmental Psychobiology · doi:10.1002/dev.420270506 · Cited by 25
Olazábal, D. E., & Morrell, J. I. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.4.1097 · Cited by 17
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Assessment of positive emotions in animals to improve their welfare
Boissy, A., Manteuffel, G., Jensen, M. B., Moe, R. O., Spruijt, B., Keeling, L. J., Winckler, C., Forkman, B., Dimitrov, I., Langbein, J., et al. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.02.003 · Cited by 1,486
Oxytocin: The Great Facilitator of Life
Lee, H.-J., Macbeth, A. H., Pagani, J., & Young, W. S. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.04.001 · Cited by 1,037
Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior
Ross, H. E., & Young, L. J. (2009) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2009.05.004 · Cited by 856
“There is a remarkable amount of individual variation in OTR density in the nucleus accumbens (NAcc) in prairie voles, and OTR density in the NAcc is significantly correlated with the display of alloparental behavior in both juvenile and adult virgin females [43,44].”
BackgroundSelf-citationAdult attachment predicts maternal brain and oxytocin response to infant cues.
Strathearn, L., Fonagy, P., Amico, J., & Montague, P. R. (2009) · Neuropsychopharmacology · doi:10.1038/npp.2009.103 · Cited by 773
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
Self-citation
Metadata
- Authors
- Olazábal, D. E., & Young, L. J.
- Affiliations
- Emory University (US)
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2006
- Volume
- 141
- Issue
- 2
- Pages
- 559-568
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W2071523320
- Cited by
- 289
- References
- 69
- Citations by year
- 2026: 8 · 2025: 12 · 2024: 6 · 2023: 15 · 2022: 7 · 2021: 20 · 2020: 23 · 2019: 10 · 2018: 16 · 2017: 19 · 2016: 29 · 2015: 24 · 2014: 11 · 2013: 18 · 2012: 14
- FWCI
- 13.77
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (K02MH064692, MH064692, MH 56538, R01MH056538)
- National Center for Research Resources (RR-00 165, P51RR000165)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Keywords
- oxytocin receptor, nucleus accumbens, maternal behavior, Microtus ochrogaster, oxytocin receptor antagonist, caudate-putamen, infanticide
- MeSH terms
- Animals, Animals, Newborn, Behavior, Animal, Arvicolinae, Dose-Response Relationship, Drug, Female, Iodine Isotopes, Maternal Behavior, Nucleus Accumbens, Protein Binding, Radioligand Assay, Time Factors, Vasotocin, Chi-Square Distribution, Receptors, Oxytocin
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