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The role of the endocrine system in baboon maternal behavior.

BACKGROUND: Human mothers display a wide range of parenting skills, and although we have gathered a large body of evidence on a variety of factors affecting maternal behavior, we still know relatively little about the physiologic correlates of variation in parental behavior in primates. METHODS: Excreted gonadal and adrenal steroids were measured across parturition in a large sample (n = 89) of group-living female baboons. Maternal behavior data were collected during the first 2 months of infants' life. RESULTS: We found that changes in the excreted sex steroid hormones and cortisol were associated with baboon mothers' infant-directed behaviors. Mothers who displayed more stress-related behaviors, who were also prone to maintain less contact with their infants, had higher postpartum cortisol levels, higher prepartum pregnanediol-3-glucoronide (PdG) levels, and lower postpartum PdG levels. Mothers with higher prepartum cortisol levels showed higher levels of infant-directed affiliative behaviors. CONCLUSIONS: These results point toward the importance of the whole endocrine system as a functional unit in terms of enhancing maternal care in primates. The dramatic physiologic changes occurring across parturition may act, in coordination with the cognitive-experiential system, to help the mother cope with the additional challenges imposed by the newborn.

Animals↗

Endocrine communication between conceptus and mother: placental lactogen stimulation of maternal behavior.

The possible role of the conceptus in stimulating the onset of maternal behavior through its secretion of placental lactogens and their passage into the brain was investigated in female rats. In the first study, significant mitogenic activity in the Nb2 lymphoma cell bioassay was detected in cerebrospinal fluid (CSF) samples collected by push-pull perfusion from rats on days 12-21 of pregnancy, coincident with the establishment of placental function. In contrast, mitogenic activity was absent from CSF in lactating and gonadectomized, virgin females. In a second study the mitogenic activity in day 12 pregnant samples was neutralized 71% with antibodies to rat placental lactogen-I (rPL-I) and > 90% with a combination of antibodies to rPL-I plus rPL-II. In contrast, activity on day 21 of pregnancy, 1 day prepartum, was reduced by antibodies to rPL-II (> 85%), but not by antibodies to rPL-I, indicating that the predominant lactogen in the CSF prepartum is rPL-II. The behavioral actions of placental secretions were assessed in the third experiment by infusing recombinant rPL-I and purified rPL-II directly into the medial preoptic area of the brain of steroid-primed, nulliparous rats. Latencies to respond maternally to foster young were significantly reduced in rPL-I- and rPL-II-treated rats (2- to 3-day latencies) when compared with latencies in control females (5- to 6-day latencies). Thus, the conceptus through its secretion of rPLs which apparently gain access to the CSF helps to prime the pregnant female's brain to respond maternally at the end of gestation. This endocrine communication between the developing conceptus and pregnant female appears to be an important part of the biological system which helps to establish successful maternal care.

Animals↗

Intracellular preoptic and striatal monoamines in pregnant and lactating rats: possible role in maternal behavior.

In many mammals, hormonal fluctuations during pregnancy and parturition produce neurochemical events that are necessary for the transition from a non-maternal state to a maternal state that occurs when infants are born. However, the nature of these events is mostly unknown. We investigated whether changes in dopamine (DA) and serotonin (5-HT) activity within the preoptic area (POA) and striatum, neural sites important for some maternal behaviors, could be part of this process. Female rats were sacrificed as either diestrus virgins, on pregnancy day 10 or 20, on the day of parturition, or on day 7 or 17 of lactation. Bilateral tissue punches from the POA, dorsolateral striatum (ST(dl)), and nucleus accumbens (NA) were obtained and levels of intracellular DA and 5-HT analyzed with high-performance liquid chromatography with electrochemical detection (HPLC-EC). In the POA, DA was high in virgins and during early pregnancy, lowest on the day of parturition, and very high during lactation. Although there were no changes in the DOPAC to DA ratio (i.e., turnover), DOPAC levels also followed this pattern. 5-HT turnover in the POA was lower in virgins compared to other groups. In the ST(dl), DA turnover was highest during late pregnancy and on the day of parturition, while no changes in 5-HT measures were found. No significant effects were found in the NA. Therefore, decreased DAergic activity in the POA and increased DAergic activity in the ST(dl) occurs around parturition, the time when maternal behavior emerges, and may influence its onset.

Animals↗

The capacity to develop maternal behavior is enhanced during aging in rats.

The induction of maternal behavior (MB) in response to stimulation by pups was studied in aged rats (19-20 months old). We used virgin female rats, neonatally androgenized female rats and male rats. Both groups of female rats showed a constant estrous vaginal smear. Maternal responsiveness was compared with that of young rats (3-4 months old). Normal and androgenized female aged rats showed a very high percentage of immediate maternal responsiveness and 100% of the rats were fully maternal within 24 hr of testing. The percentage of cyclic and androgenized young rats showing MB were significantly lower. Chronic ovariectomy performed 17 months before testing but not acute ovariectomy abolished MB. Estrogen treatment (5 micrograms 15 hours before pup presentation) to chronically ovariectomized aged rats was not sufficient to reestablish significantly the capacity of the normal female aged rats to become short-latency maternal. Young and aged male rats showed no difference in maternal responsiveness to the presence of foster pups. The percentage of maternal aged male rats was significantly lower than that of the normal and androgenized aged female rats, whereas young male and female rats showed a similar level of MB, indicating a sex difference in the development of MB with age. In conclusion the high percentage of rats becoming maternal and the short-latency maternal responsiveness in aged female rats appears to be the result of a prolonged estrogen and/or prolactin stimulation.

Aging↗

Exposure to PCB 77 affects the maternal behavior of rats.

Polychlorinated biphenyls are environmental contaminants known to affect neurobehavioral development in many laboratory studies using different animal models. Because of their bioaccumulation and long half-life they are a serious concern for our own species. The dioxin-like PCB congener 3,4,3',4'-tetrachlorobiphenyl (PCB 77) has estrogenic and anti-estrogenic properties, and has been shown to affect brain chemistry and behavior of developing rats when administered during gestation. Since many developmental outcomes in mammals depend upon the type of maternal care provided by the dams, we investigated the effects of two doses of PCB 77 (2 and 4 mg/kg administered during gestational days 6-18) on the maternal behavior of the treated dams. Both doses of PCB 77 reduced the amount of nursing time in which the dams displayed the high-crouch posture over postnatal days 1-6. In addition, the high dose increased the amount of maternal licking and grooming of the litters and the amount of time the dams spent on the nest. The high dose also increased pup mortality, and both doses reduced the weight gain of the litters during the first 6 days of life. These results document effects of PCB 77 on maternal behavior and serve to raise questions about the importance of maternal contributions to the developmental effects of this and similar contaminants.

Age Factors↗

The relationship between social support and maternal behaviors and attitudes: a meta-analytic review.

Used meta-analysis to analyze 66 studies that evaluated the relationship between social support available to the mother and maternal behaviors and attitudes. Investigators sampled relatively homogeneous populations of white, middle-class, married mothers of young children without physical or mental disabilities. A variety of instruments were used to assess key study variables. Significant correlations existed between both emotional and material support and maternal behaviors. Implications of these findings for funding of family support programs and for professionals working with mothers are discussed.

Attitude↗

Initiation of maternal behavior in the rat: possible involvement of limbic norepinephrine.

The dorsal norepinephrine (NE) fiber system was manipulated in pregnant female rats. Brainstem lesions of the dorsal bundle, depleting NE in cortex and hippocampus, resulted in deficits in maternal-behavior onset in primiparous rats. Similarly, fornix-bundle transections, depleting only hippocampal NE, were associated with an absence of pup care. Hypothalamic NE levels, as well as dopamine and serotonin concentrations in cortex, hippocampus and hypothalamus, were not significantly affected by these manipulations. The data are discussed in terms of behavioral specificity, possible hormonal involvement and interactions with diencephalic mechanisms controlling the onset of maternal behavior in the female rat.

Animals↗

Intracerebral oxytocin is important for the onset of maternal behavior in inexperienced ewes delivered under peridural anesthesia.

Measurement of cerebrospinal concentrations of oxytocin (OT) in intact and peridural-anesthetized ewes showed that central release of OT during parturition is inhibited by this anesthesia. Also, observations of maternal behavior and attraction to amniotic fluid (AF) in inexperienced peridural-anesthetized parturient ewes after intracerebroventricular injections of either OT (2 x 10 micrograms) or saline showed that OT infusions increased the proportion of maternal females (2/17 vs. 10/20; p = .01) and attraction to AF. This study confirms that in sheep vaginocervical stimulation activates the oxytocinergic system, which induces the onset of maternal behavior, and that this action is not limited to maternally experienced females.

Anesthesia, Epidural↗

Prenatal stress impairs maternal behavior in a conflict situation and reduces hippocampal benzodiazepine receptors.

Maternal behavior (pup retrieval) was assessed in prenatally stressed rats during control and conflict situations (having to pass through an airstream) when their pups were 4-5 days old. There was no difference in pup retrieval between experimental and control rats under normal conditions but only 52% of the former retrieved their pups during the conflict situation, compared with 96% of the controls. Catecholamine (CA) levels in the arcuate nucleus (Arc.n.) and noradrenaline in the medial preoptic nucleus (POM) were not altered in prenatally stressed females, but their dopamine levels in the POM tended to be lower (p less than 0.1). The number of benzodiazepine (BZ) receptors in the hippocampi of prenatally stressed females was significantly lower than in controls. We conclude from these results that random prenatal noise and light stress increases the vulnerability to stressful situations in the female offspring during adulthood, which may be accompanied by altered CA function in the hypothalamus and BZ binding in the hippocampus.

Animals↗

Induction of maternal behavior in incubating and non-incubating hens: influence of hormones.

Maternal responses and variations in plasma levels of prolactin and testosterone have been studied in incubating and in non-incubating, non-laying hens during forced adoption experiments. The results demonstrate the ability of incubating hens to display complete maternal behavior as early as the 10th day of incubation after being exposed to stimulation by chicks during one night. Maternal responses also emerged in non-laying hens but more gradually. In both groups, a decline in plasma testosterone occurred after the introduction of the chicks and, in the incubating hens, prolactin levels fell as they abandoned their nests.

Animals↗

The role of lactogenic hormones in maternal behavior in female rats.

Most mammals display an immediate onset of maternal care towards their offspring at parturition. In contrast, inexperienced, nulliparous females are often slow responders and show less intensity in their maternal responses. The transition from a slow responder in non-parous females to a rapid response at parturition is facilitated by the endocrine state of pregnancy. The present report reviews recent evidence from my laboratory demonstrating a role for prolactin in the stimulation of maternal behavior in the rat and presents new findings suggesting tht the conceptus, through its secretion of placental lactogens, helps prime the maternal brain (one site being the medial preoptic area) to respond maternally at parturition.

Animals↗

Induction of maternal behavior by mouse neonates: influence of dam parity and prenatal oxazepam exposure.

The aim of the present report was to investigate the influence of pup stimulus properties and female parity on mouse maternal behavior. Outbred CD-1 mouse pups, prenatally exposed to either the vehicle (VEH) or oxazepam (OX, 15 mg/kg twice/day on pregnancy days 12-16) and fostered to untreated dams at birth, were offered as a stimulus on postnatal days 4, 6, and 8 to four groups of females that differed in maternal experience: virgin, experienced virgin females, primiparae, and biparae. Maternal behavior was observed during a 15-min session each day. Virgin females were less involved in crouching behavior than primiparae. Pups, age, and prenatal oxazepam showed interactive effects on maternal care, particularly by increasing licking and nest-building activities and decreasing still-out behavior. Moreover, dams receiving younger pups showed high levels of both locomotor activity and rearing. The present findings point to the need for a better understanding of mother-pup interactions in studies aimed at characterizing drug and toxicant effects on both animal and human development.

Animals↗

Evidence from urinary cortisol that maternal behavior is related to stress in gorillas.

By studying western lowland gorillas (Gorilla gorilla gorilla, n = 8) in zoological gardens via ethological and non-invasive physiological techniques, we have demonstrated that their postpartum maternal behavior is related negatively to their postpartum urinary titers of cortisol. On the basis of this finding, it is proposed that postpartum stress contributes to disrupted maternal behavior in the gorilla in captivity. Morning urine samples were collected with a mean sampling interval of 1.6 days from Day 14 prepartum to Day 14 postpartum (n = 11 pregnancies). Creatinine-indexed (Cr) urinary cortisol titers declined significantly between Day 9 to 1 prepartum (0.634 +/- 0.014 microg/mg of Cr, mean +/- SEM) and Day 1 to 6 postpartum (0.396 +/- 0.030 microg/mg of Cr, mean +/- SEM; p < 0.01-0.001). For each pregnancy, the relative postpartum decline in urinary cortisol was calculated as (microg of cortisol/mg of Cr Day 1 to 4)/(microg of cortisol/mg of Cr Day -4 to -1). Values ranged from 0.35 to 1.12, were independent of absolute prepartum cortisol titers, and were interpreted as evidence of inter-female differences in postpartum hypothalamo-pituitary-adrenal axis activity and, therefore, postpartum stress. This postpartum stress index was negatively correlated with the amount of time (0-100%) that females carried and supported their 0-14 day-old infants in a ventral position during locomotion (r(s) = -0.68, p < 0.05) and tended to be negatively correlated with the total amount of time (0-100%) they spent in ventro-ventral contact with their infants (r(s) = -0.58; p < 0.10). This study provides the first physiological evidence that postpartum stress is an important etiologic factor in gorilla maternal failure in captive environments.

Animals↗

Neuropsychology of maternal behavior in the rat: c-fos expression during mother-litter interactions.

This series of studies used the pattern of nuclear Fos-like immunoreactivity (Fos-lir) to map the functional pathways in the brain that mediate the onset and retention of maternal behavior. In the first two experiments, parturient rat dams were exposed to either pups or to other stimuli on Day 1 postpartum. Dams interacting with pups were either intact or sustained ventral somatosensory, olfactory, or combined desensitizations. Results showed that 1) all intact pup-interacting dams showed elevated levels of Fos-lir in the medial preoptic area (MPOA) and the medial and cortical amygdala as compared to control groups, and 2) olfactory and ventral somatosensory desensitization, either alone or in combination, did not decrease Fos-lir in the MPOA. However, olfactory desensitizations did decrease Fos-lir in the medial amygdala and the combined desensitizations significantly reduced Fos-lir in both the basolateral and central amygdala. In the third study, dams were either exposed to pups or to other stimuli and were subsequently reexposed to pups or to pup cues. Regardless of prior maternal experience, females who were able to interact with pups upon reexposure showed increased Fos-lir in the MPOA, the basolateral and central nuclei of the amygdala, and the nucleus accumbens when compared to females which did not interact with pups. Taken together, these studies suggest that the neuroanatomy of maternal behavior is a complex one, involving multiple systems that interconnect with the MPOA and that mediate the many behavioral processes activated when an animal responds maternally.

Amygdala↗

Effects of dopamine receptor antagonists on ongoing maternal behavior in rats.

The effects of different peripheral doses of four dopamine (DA) receptor antagonists on general activity and maternal behavior were examined in lactating female rats. Administration of the classic D1-like and D2-like DA receptor blocker haloperidol (0.1 and 0.05 mg/kg) disrupted pup retrieval and nest-building behaviors and reduced motor activity. Pimozide (0.5 and 0.2 mg/kg), which has more affinity for DA D2-like receptors, mildly disrupted pup retrieval while showing no significant influence on open-field behaviors. The putative DA D(4) receptor blocker, clozapine (1.5 and 1.0 mg/kg) reduced motor activity significantly, while only 1.0 mg/kg dose significantly decreased percent of rats displaying nest building. The DA D1-like receptor blocker SKF-83566 (0.2 and 0.1 mg/kg) significantly reduced pup retrieval, nest building and motor activity. These results suggest a role for DA receptors in ongoing maternal behavior that correlates directly with general activity.

Adult↗

Amphetamine and maternal behavior: dose response relationships.

Primiparous rats received 0.05, 0.25, 0.50, or 1.50 mg d-amphetamine/kg body weight, injected IP, when offspring reached 3-4 and 10-11 days of age. A multidimensional analysis of their maternal behavior revealed that at doses as low as 0.25 mg/kg, amphetamine had a disruptive effect on mother-pup intercontact interval, retrieval latency, inter-retrieval interval, number of pup retrieved and number of corners to which they were retrieved, time nest building, number of paper strips used, nursing time, time in motion, and number of squares entered. Disruption was dose-dependent for all the preceding except number of corners and time nest building. Amphetamine had no effect on the rate of maternal locomotion. The impact of amphetamine on nursing was significantly greater at pup ages of 3-4 days than at 10-11 days. Drug-induced augmentation of arousal exceeding optimal levels for adequate care-giving and locomotor stimulation incompatible with elements of maternal behavior may account for dose-dependent impairment in the range of 0.25 to 1.50 mg/kg d-amphetamine.

Aging↗

Gene targeting approaches to neuroendocrinology: oxytocin, maternal behavior, and affiliation.

Transgenic technology affords exciting new opportunities in the field of behavioral neuroendocrinology. We have extended our research into the behavioral function of oxytocin in maternal and social behavior using two transgenic approaches: (i) targeted deletion of the oxytocin gene in mice and (ii) augmented oxytocin receptor expression in the brain. Mice genetically deficient in oxytocin can mate, give birth, and display normal maternal behavior; however, milk ejection and certain aspects of social behavior are affected. Comparative studies of oxytocin receptors have led to the observation that species differences in social organization are associated with differences in receptor distribution. Specifically, monogamous prairie voles and nonmonogamous, asocial montane voles exhibit different patterns of OT receptor expression in the brain. Transgenic mice have been created with a reporter gene driven by the prairie vole oxytocin receptor gene promoter. Analysis of the expression pattern suggests that it should be possible to manipulate receptor expression in the vole brain in order to examine the effects of receptor distribution on behavior.

Animals↗