Physiological Regulation of Maternal Behavior in Heifers: Roles of Genital Stimulation, Intracerebral Oxytocin Release, and Ovarian Steroids

Department of Animal Science, Iowa State University, Ames, Iowa, United States
Biology of Reproduction (Impact Factor: 3.32). 07/2001; 65(1):295-300. DOI: 10.1095/biolreprod65.1.295
Source: PubMed


We tested the hypotheses that 1) epidural anesthesia at parturition would block both peripheral and central release of oxytocin and eliminate the development of maternal behavior in primiparous heifers and 2) estradiol priming, genital stimulation, and appropriate neonatal stimuli would induce maternal behavior in nulliparous heifers. In experiment 1, primiparous crossbred heifers (n = 13) with cannulas in the third cerebroventricle (IIIV) were assigned randomly to receive epidural treatments of saline (SAL; n = 6) or lidocaine HCl (EPI; n = 7) at the onset of labor induced between Days 270 and 280 of gestation. Epidural anesthesia blocked (P < 0.001) both central and peripheral release of oxytocin and markedly reduced (P < 0.05) or eliminated licking behaviors during a 3-h period following parturition as compared with SAL. Following approximately 1 wk of controlled daily suckling, during which calves were permitted access only to the inguinal region of their dams (three times daily for 10 min each time), a second maternal behavior test was performed. Although licking behavior remained markedly reduced (P < 0.001) in the EPI compared with the SAL groups, all heifers accepted their calf at the udder. In experiments 2-4, neither estradiol priming in ovariectomized heifers nor estradiol plus progesterone in intact heifers resulted in an induction of maternal behaviors following genital stimulation and presentation of a neonate wetted with amniotic fluid. Pelvic sensory deficits apparently block oxytocin release and disturb both short-latency and long-term maternal behaviors but do not result ultimately in rejection of the calf. Combinations of hormonal, sensory, olfactory, and visual cues observed previously to induce maternal behavior in nulliparous ewes do not appear adequate for induction of maternal behavior in nulliparous heifers.

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    • "Oxytocin is released e.g. during teat stimulation while suckling as well as during vaginocervical stimulation as is the case when giving birth [12] [13]. A relationship between oxytocin levels and maternal and/or bonding behavior has been detected in various species such as cattle [14], sheep [11], rats [15], and primates [16], including humans [17]. We therefore hypothesized that saliva oxytocin levels either alone or in combination with parameters indicative of stress may serve as a biomarker for maternal behavior in cattle. "
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    ABSTRACT: The objectives of the present study were to evaluate the suitability of potential biomarkers for maternal ability in cattle, and in addition to test the hypothesis that dairy cows have a less pronounced motherliness than beef cows. Therefore, maternal behavior of 20 Simmental beef-type (S) and 20 German Black Pied (dairy-type) Cattle (BP) was assessed on the 2nd and again on the 3rd day of the calf's life. Measurements included the frequency of interactions between cow and calf, the cow's willingness to defend her calf, the overall maternal behavior, saliva cortisol, saliva oxytocin, heart rate, and thermal images of the eye (ET). Mixed model analysis revealed that BP had significantly (P<0.05) higher oxytocin (88.6±9.2 vs. 62.8±9.2pg/ml saliva) and cortisol (1.3±0.1 vs. 1.0±0.1ng/ml saliva) levels, but lower heart rates (80.0±2.0 vs. 95.8±2.0bpm) than S cows. Simmental (beef) cows showed more defensive behavior (3.5±0.2 vs. 2.7±0.2 scores), but fewer total interactions between cow and calf (8.1±1.4 vs. 13.8±1.4), compared to BP (dairy). However, with the exception of heart rate and overall maternal behavior, breed differences tended to diminish from the 2nd to the 3rd day of the calf's life. Repeatabilities ranged from 9±23% (ET) to 77±7% (maternal behavior measured on a visual analogue scale), and correlations between physiological parameters and behavior differed between breeds and were generally at a low level. In conclusion, beef cows do not seem to be per se more maternal compared to dairy cows, and the assessed parameters are of limited use as biomarkers for maternal behavior. Copyright © 2014 Elsevier Inc. All rights reserved.
    Full-text · Article · Nov 2014 · Physiology & Behavior
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    • "In experimental animals, it has been shown that oxytocin strongly influences maternal care, and the prosocial effects of oxytocin have been widely recognized (Francis et al., 2000; Williams et al., 2001; Caldwell and Young, 2006). However, the neuroendocrinological research of mother-infant relations in humans is now being progressively undertaken, although it remains unclear how oxytocin links mother-infant relationship and post-growth offspring. "
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    ABSTRACT: Mother-infant bonding is universal to all mammalian species. In this review, we describe the manner in which reciprocal communication between the mother and infant leads to mother-infant bonding in rodents. In rats and mice, mother-infant bond formation is reinforced by various social stimuli, such as tactile stimuli and ultrasonic vocalizations (USVs) from the pups to the mother, and feeding and tactile stimulation from the mother to the pups. Some evidence suggests that mother and infant can develop a cross-modal sensory recognition of their counterpart during this bonding process. Neurochemically, oxytocin in the neural system plays a pivotal role in each side of the mother-infant bonding process, although the mechanisms underlying bond formation in the brains of infants has not yet been clarified. Impairment of mother-infant bonding, that is, deprivation of social stimuli from the mother, strongly influences offspring sociality, including maternal behavior toward their own offspring in their adulthood, implying a "non-genomic transmission of maternal environment," even in rodents. The comparative understanding of cognitive functions between mother and infants, and the biological mechanisms involved in mother-infant bonding may help us understand psychiatric disorders associated with mother-infant relationships.
    Full-text · Article · Jan 2012 · Frontiers in Human Neuroscience
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    • "Parturition induces physiological changes within several brain areas. OT concentrations are greatly increased in the cerebrospinal fluid of ewes within the first few minutes after expulsion of the neonate (Kendrick et al., 1986) but not in animals that have an epidural anesthesia (Levy et al., 1992; Williams et al., 2001). OT synthesis increases at parturition in the paraventricular nucleus of the hypothalamus (PVN), and in the supraoptic nucleus (SON) of the hypothalamus, two main sources of OT projections in the brain (Broad et al., 1993b). "
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    ABSTRACT: Across mammalian species, sheep are unique in showing maternal care together with a specialized form of rapid olfactory learning producing recognition of individual young. These two behavioral processes are synchronized at parturition by vaginocervical stimulation (VCS) induced by the expulsion of the neonate. Olfactory cues from amniotic fluid are a prerequisite for the initial approach to the neonate and selectivity is strictly dependent on the learning of the individual olfactory signature. At a physiological level, central oxytocin (OT), supported by estrogens, the opoid peptides and cortico‐releasing hormone (CRH) is the key factor for maternal responsiveness. At the neural level, the control of maternal responsiveness is mainly hypothalamic and has little in common with the circuitry involved in selectivity, which mainly concerns olfactory processing regions but also cholinergic and noradrenergic systems. Maternal responsiveness, a common behavioral trait of altricial and precocial species, is mediated in sheep by endocrine factors that are similar to those found in altricial species, such as rats. In the majority of mammalian species, steroids, VCS, and OT play a role in the development of maternal response to the young although the relative importance of each may vary. A role of olfaction is clearly established for the onset of both maternal responsiveness and selectivity at suckling. Amniotic fluid is necessary for the initial approach to the young and mothers learn the individual olfactory signature of their own neonate to discriminate them from alien lambs.
    Full-text · Article · Dec 2008 · Advances in the Study of Behavior
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