Oxytocin induction of short-latency maternal behavior in nulliparous, estrogen-primed female rats
Abstract
This study was designed to test whether intracerebroventricular (icv) administration of oxytocin can shorten the latency of estrogen-treated virgin rats to respond to foster pups with maternal care. A secondary goal was a description of the behavioral effects of icv oxytocin in rats. Forty-eight hours before pup presentation female rats (Sprague-Dawley strain, obtained from Zivic-Miller Laboratories, Inc.) with chronic lateral ventricle cannulae were ovariectomized and treated with 100 micrograms/kg body wt estradiol benzoate (EB). Immediately before pup presentation either 400 ng oxytocin or the normal saline vehicle was infused. A second control group of noncannulated animals received the same surgery, EB treatment, and behavior tests without any icv infusion. Maternal behavior was scored on a scale from 0 to 5, one point each being given for licking pups, carrying pups, grouping pups, crouching over pups, and nest building. At the end of 1 hr of pup exposure 65% of the oxytocin-infused animals received scores of 4 or 5, while only 25% of the control animals attained these scores. Maternal behavior appeared as a unit in both spontaneously maternal and oxytocin-treated animals, with fewer than 10% in either group receiving scores of 1, 2, or 3. The oxytocin group also spent significantly more time grooming. In a second experiment in which oxytocin or normal saline was administered icv to oil-treated animals, this grooming effect was shown to be estrogen independent while the induction of maternal behavior required prior treatment with estrogen. Finally, a slight, transient hyperthermic effect of oxytocin on body temperature was observed in this test paradigm. These data suggest a role for oxytocin, acting with estrogen, in the onset of maternal behavior in rats.
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The transition from juvenile to adult patterns of alloparental behavior in female prairie voles does not appear to be related to changes in sex hormones.
“The transition from juvenile to adult patterns of alloparental behavior in females does not appear to be related to changes in sex hormones [40].”
From Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior (2009) · cites this paper as [40]
As female prairie voles reach puberty, only about 50% will spontaneously retrieve, lick/groom, and hover over pups presented to them, with the remainder either ignoring or attacking pups.
“However, as females reach puberty, only about 50% of the females will spontaneously retrieve, lick/groom, and hover over pups presented to them, with the remainder of the females either ignoring or attacking pups [38-40].”
From Oxytocin and the Neural Mechanisms Regulating Social Cognition and Affiliative Behavior (2009) · cites this paper as [40]
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“Central OT administration reduces the latency of female rats to show maternal behavior when exposed to pups (Pedersen and Prange, 1979; Pedersen et al., 1982; Fahrbach et al., 1984) and increases maternal behavior in mice (McCarthy, 1990).”
BackgroundCentral mechanisms underlying the neural and neuroendocrine determinants of maternal behaviour
Keverne, E. B. (1988) · Psychoneuroendocrinology · doi:10.1016/0306-4530(88)90010-8 · Cited by 78 · see citing works
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Neuroendocrine control of maternal behavior in non-human and human mammals
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Expression and Region-Specific Regulation of the Oxytocin Receptor Gene in Rat Brain
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The importance of vaginal-cervical stimulation for maternal behaviour in the rat
Yeo, J. A. G., & Keverne, E. B. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90378-1 · Cited by 74 · see citing works
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A comparative systems model of the regulation of maternal motivation in mammals
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Oxytocin and vasopressin enhance responsiveness to infant stimuli in adult marmosets
Taylor, J. H., & French, J. A. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.10.002 · Cited by 68 · see citing works
“…rat, Francis et al., 2000; macaque, Maestripieri et al., 2009), and females that would not ordinarily engage in parental behavior can be induced to do so with exogenous OT infusions (rat, Fahrbach et al., 1984; sheep, Kendrick et al., 1987; mouse, McCarthy et al., 1986; rat, Pedersen et al., 1982).”
BackgroundMaternal Behavior among the Nonprimate Mammals
Rosenblatt, J. S., Mayer, A. D., & Siegel, H. I. (1985) · Springer eBooks · doi:10.1007/978-1-4684-4832-0_7 · Cited by 69 · see citing works
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“central release of the peptide hormone oxytocin (OXY) has been implicated both in the control of maternal behaviour in rats (1, 2) and sheep (3) and sexual receptivity in rats (4-7) and prairie voles (8), although the proposed role for OXY in controlling sexual receptivity in these two latter species is opposite.”
BackgroundNuman, M. J., FLEMING, A., & Lévy, F. (2006) · Elsevier eBooks · doi:10.1016/b978-012515400-0/50040-3 · Cited by 63 · see citing works
The role of lactogenic hormones in maternal behavior in female rats
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Chapter 4 Oxytocin: who needs it?
Insel, T. R., Gingrich, B., & Young, L. J. (2001) · Progress in brain research · doi:10.1016/s0079-6123(01)33005-4 · Cited by 62 · see citing works
Fahrbach, S. E., Morrell, J. I., & Pfaff, D. W. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90396-3 · Cited by 60 · see citing works
The habenular complex mediates hormonal stimulation of maternal behavior in rats.
Corodimas, K. P., Rosenblatt, J. S., & Morrell, J. I. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.5.853 · Cited by 59 · see citing works
McCarthy, M. M., Bare, J. E., & Saal, F. S. V. (1986) · Physiology & Behavior · doi:10.1016/0031-9384(86)90066-1 · Cited by 58 · see citing works
Rayner, V. C., Robinson, I. C., & Russell, J. A. (1988) · The Journal of Physiology · doi:10.1113/jphysiol.1988.sp016964 · Cited by 58 · see citing works
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“The distinction between the onset and maintenance periods of maternal behavior is particularly important because these two periods are apparently regulated by different underlying hormonal states (oxytocin is essential for the normal onset of maternal behavior but not essential for its maintenance once maternal behavi…”
BackgroundYuan, W., He, Z., Hou, W., Wang, L., Li, L., Zhang, J., Yang, Y., Jia, R., Qiao, H., & Tai, F. (2019) · Hormones and Behavior · doi:10.1016/j.yhbeh.2019.02.014 · Cited by 56 · see citing works
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Hormonal influences on the duration of postpartum maternal responsiveness in the rat
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The interplay of oxytocin and sex hormones
Quintana, D. S., Glaser, B. D., Kang, H., Kildal, E. S.-M., Audunsdottir, K., Sartorius, A. M., & Barth, C. (2024) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2024.105765 · Cited by 54 · see citing works
“…via intracerebroventricular oxytocin administration that effects on the onset of parenting behaviors were demonstrated in virgin rodents, which was dependent on the presence of estrogens (Fahrbach et al., 1984; Pedersen et al., 1982; Pedersen and Prange, 1979) and the environment (McCarthy, 1995).”
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
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 · see citing works
Harony, H., & Wagner, S. (2010) · Neurosignals · doi:10.1159/000321035 · Cited by 62 · see citing works
“Indeed, following priming with estrogen, virgin female rats centrally infused with OT display full maternal behavior [”
BackgroundInnate and learned aspects of pheromone-mediated social behaviours
Beny, Y., & Kimchi, T. (2014) · Animal Behaviour · doi:10.1016/j.anbehav.2014.09.014 · Cited by 50 · see citing works
“It has been suggested that oxytocin release in the brain might be part of an array of neuroendocrine events, mediated by the pup's odours, that together determine the initial aversion to pups observed in nulliparous females (Fahrbach, Morrell, & Pfaff,1984).”
BackgroundMaternal care boosted by paternal imprinting in mammals
Creeth, H., McNamara, G. I., Tunster, S. J., Boqué-Sastre, R., Allen, B., Sumption, L. A., Eddy, J. B., Isles, A. R., & John, R. M. (2018) · PLoS Biology · doi:10.1371/journal.pbio.2006599 · Cited by 49 · see citing works
Oxytocin—a social peptide? Deconstructing the evidence
Leng, G., Leng, R., & Ludwig, M. (2022) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2021.0055 · Cited by 48 · see citing works
Role of oxytocin in parental behaviour
Olazábal, D. E. (2018) · Journal of Neuroendocrinology · doi:10.1111/jne.12594 · Cited by 47 · see citing works
A Role for Nonapeptides and Dopamine in Nest‐Building Behaviour
Hall, Z. J., Healy, S. D., & Meddle, S. (2014) · Journal of Neuroendocrinology · doi:10.1111/jne.12250 · Cited by 45 · see citing works
“oxytocin infusions induce maternal behaviour in rats and mice [23,24] and oxytocin signalling appears to be involved in nest-building behaviour in rodents [25,26].”
Johnson, A. E. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb34367.x · Cited by 43 · see citing works
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 · see citing works
Kojima, S., & Alberts, J. R. (2011) · Hormones and Behavior · doi:10.1016/j.yhbeh.2011.08.003 · Cited by 39 · see citing works
“, 2000; Popik and van Ree, 1998), pair bonding (Carter, 1998; Young and Wang, 2004), and maternal behavior (Fahrbach et al., 1984; Keverne and Kendrick, 1992; Pedersen, 1997; Pedersen and Boccia, 2003) in rodents and ungulates, as well as love (Bartels and Zeki, 2004), trust (Kosfeld et al.”
BackgroundKlatt, J. D., & Goodson, J. L. (2013) · Hormones and Behavior · doi:10.1016/j.yhbeh.2013.10.001 · Cited by 38 · see citing works
Liu, Y., Donovan, M. L., Jia, X., & Wang, Z. (2019) · European Journal of Neuroscience · doi:10.1111/ejn.14550 · Cited by 38 · see citing works
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Zinni, M., Colella, M., Novais, A. R. B., Baud, O., & Mairesse, J. (2018) · Frontiers in Neurology · doi:10.3389/fneur.2018.00229 · Cited by 35 · see citing works
“Indeed, the authors demonstrated that intracerebral administration of OTX to virgin female rats reduced the latency to develop maternal care in response to exposure to forest pups (75, 76).”
BackgroundAlterations in supraoptic nucleus ultrastructure of maternally behaving virgin rats
Salm, A. K., Modney, B. K., & Hatton, G. I. (1988) · Brain Research Bulletin · doi:10.1016/0361-9230(88)90209-2 · Cited by 34 · see citing works
- Authors
- FAHRBACH, S.
- Affiliations
- Rockefeller University (US)
- Corresponding author
- FAHRBACH, S
- ORCID
- FAHRBACH, S
- Venue
- Hormones and Behavior
- Publisher
- Elsevier BV
- Published
- 1984-09
- Volume
- 18
- Issue
- 3
- Pages
- 267-286
- ISSN
- 0018-506X (ISSN-L)
- OpenAlex
- W2018132730
- Cited by
- 187
- References
- 33
- Citations by year
- 2026: 4 · 2025: 1 · 2024: 5 · 2023: 4 · 2022: 5 · 2021: 1 · 2020: 19 · 2019: 4 · 2018: 6 · 2017: 5 · 2016: 3 · 2015: 3 · 2014: 5 · 2013: 7 · 2012: 3
- FWCI
- 11.67
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Hormones and Behavior (publishedVersion)
- PubMed (publishedVersion)
- Funders
- University of Arizona
- Topics
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuropeptides and Animal Physiology
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- oxytocin, maternal behavior, estrogen, estradiol benzoate, nulliparous rats, intracerebroventricular administration, pup licking, grooming, body temperature, hyperthermia
- MeSH terms
- Animals, Brain, Estradiol, Female, Grooming, Injections, Intraventricular, Maternal Behavior, Motor Activity, Nesting Behavior, Oxytocin, Rats, Inbred Strains, Reaction Time, Rats
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