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Neural mediation of nursing and related maternal behaviors.

Nursing is the behavioral concomitant of lactation and the most generalizable maternal behavior across mammals. In lactating rats nursing often occurs in the kyphotic (upright crouched) posture; like the neuroendocrine determinants of milk synthesis and release, kyphosis requires suckling by the young. The dam's active pronurturant behaviors, such as retrieval and licking of pups, requires perioral somatosensory stimulation, which is often a precursor of kyphosis as well, and is inhibited by suckling. The sequential nature of maternal behaviors and the dissociations in their somatosensory regulation are critical to understanding their neural mediation, as exemplified by our recent work in lactating rats. We found that the caudal lateral and ventrolateral midbrain periaqueductal gray (cPAGl,vl) is a sensorimotor integration site for the kyphotic nursing posture. Destruction of the cPAGl,vl, or increased activity of the inhibitory neurotransmitter GABA within it, severely reduced kyphosis, increased nursing in more atypical postures, and had little or no effect on pronurturance. Various forebrain sites are known to mediate retrieval and licking of pups. Inhibition of dopaminergic activity in the nucleus accumbens of dams via microinfusions of a mixed D1/D2 dopamine receptor antagonist, cis-flupenthixol (FLU), dose-dependently reduced these active behaviors, while increasing nursing duration. Retrieval was inhibited, however, only by infusions of FLU that included the nucleus accumbens shell, which is reciprocally connected with other sites implicated in retrieval of pups. Thus, maternal behavior is not a unitary process but rather a complex category consisting of sequential behavioral components that have their own sensory and neural determinants.

Animals↗

Duration of daily test pup exposure in adult, nulliparous rats alters maternal behavior induction rates: implications for animal use numbers.

Testing for the induction of maternal behavior in rats involves the use of adult nulliparous experimental females, lactating donor dams, and their pups. In the present study, the effects of reducing the daily pup exposure from 23 h to 1 h on maternal induction latencies were assessed. In addition, because a 1-h daily exposure would reduce the non-nutritive period and potential discomfort in the pups, the effect of the reduction in pup exposure on animal use numbers was compared under these two conditions. Exposure to test young for 23 h daily for 15 days significantly increased the proportion of test animals that became maternal compared with 1 h of exposure (92% versus 35%). Moreover, animals in the 23-h group that became maternal had shorter latencies (5 days versus 11 days) and responded faster to the pups on the first day that maternal behavior was displayed than did the 1-h exposure group. A mathematical comparison of numbers of rats required to induce maternal behavior in 30 nulliparous rats under both exposure conditions revealed that the 1-h group requires 2.6 times more animals. These findings indicate that compared with the 1-h scheme, the 23-h exposure protocol is significantly more efficient in both inducing maternal care as well as reducing the overall use of animals. Therefore, when selecting an animal testing protocol, one must consider the effect of reducing potential pup discomfort in light of the implications on the number of animals used and the behavioral outcome in a given test paradigm.

Animal Husbandry↗

The relationship of maternal perception and maternal behavior: a study of normal mothers and their infants.

Normal mothers of nine-month-olds generally perceived their infants' behavior accurately. However, where maternal perceptual distortions did occur, they were associated with less maternal responsiveness and greater interference. These correlated with the mothers' anxiety level and with infant sleep problems. Maternal expectations thus seemed to be translated into specific maternal behavior which may be of significance in the child's psychosocial adjustment.

Adult↗

A neural circuitry analysis of maternal behavior in the rat.

This article reviews work that shows that the medial preoptic area of the hypothalamus plays a crucial role in controlling the occurrence of maternal behavior in rats. A primary goal of this report is to fit the medial preoptic area into a larger neural circuitry, examining its critical inputs and outputs. Lesions of the medial preoptic area disrupt maternal behavior and estradiol and prolactin injections into this region activate maternal behavior. The medial amygdala, which is located in the limbic telencephalon, sends a neural projection to the preoptic region. Research indicates that this projection influences maternal behavior by relaying olfactory input to the medial preoptic area. The output of the preoptic area influences maternal behavior through descending projections to the brain stem. One of the influences of such projections might be to regulate neural circuits involved in controlling specific maternal responses, such as retrieval (carrying of pups) behavior.

Algorithms↗

The effects of medial preoptic area and amygdala lesions on maternal behavior in the juvenile rat.

The present study was designed to determine whether the medial preoptic area (MPOA) and the amygdala (AMYG) are involved in the expression of "maternal" behavior in juvenile rats as they are in the adult. Juveniles show many behaviors that are similar to the maternal behaviors shown by the postpartum female rat. Whether these behaviors are social in function, as opposed to parental, and hence mediated by different mechanisms from those regulating adult maternal behavior is not known. To test the roles of the MPOA and AMYG in mediating these behaviors, 21-day-old female juvenile rats received MPOA, AMYG, or SHAM (MPOA/AMYG) lesions and were tested at 22 days of age for maternal and other responses to pups. Major findings demonstrate that MPOA lesions disrupt components of maternal behavior, including retrieving and nest building, while AMYG lesions facilitate these behaviors. These findings indicate striking similarities between the juvenile and rat brain for parental responding.

Amygdala↗

Maternal behavior is impaired by methamphetamine administered during pre-mating, gestation and lactation.

Previous studies demonstrated that stimulant drugs, such as cocaine or amphetamine, administered during gestation or lactation may attenuate maternal behavior in rats. The effect of methamphetamine (MA), a drug whose usage has increased lately, on maternal behavior has not yet been investigated. The present study tested the effect of MA (5 mg/kg daily) administered prior to, during and after gestation on maternal behavior. Regularity of the estrous cycle, the incidence of impregnation, and the weight gain was compared between groups (control, saline- and MA-treated). Maternal behavior was examined using two tests: Observation test (without disturbance of the mother and pups) and Retrieval test (with short separation of pups from the mother). All tests were conducted prior to dosing each day. In the Observation test, MA decreased the blanket position of active nursing, while increasing passive nursing. There were no MA-induced changes in other maternal activities such as mother being in the nest, in contact with pups, or grooming pups. MA increased some non-maternal activities, such as drinking, eating, and sleeping, while decreasing stereotypic behavior (sniffing and rearing) when compared to controls. In the Retrieval test, MA-treated mothers were slower in retrieving the first pup, returning the first pup into the nest, and returning all pups into the nest. Interestingly, there were differences in maternal behavior also in saline-treated mothers relative to controls. Saline-treated mothers spent more time in the nest and groomed pups more than controls or MA-treated mothers. In conclusion, the present study demonstrates a novel finding that MA administered during pre-mating, gestational and lactational periods has a negative effect on maternal behavior toward pups.

Animals↗

Prevalence of selected maternal behaviors and experiences, Pregnancy Risk Assessment Monitoring System (PRAMS), 1999.

PROBLEM/CONDITION: Various maternal behaviors and experiences before, during, and after pregnancy (e.g., unintended pregnancy, late entry into prenatal care, cigarette smoking, not breast-feeding) are associated with adverse health outcomes for both the mother and the infant. Information regarding maternal behaviors and experiences is needed to monitor trends, to enhance the understanding of the relations between behaviors and health outcomes, to plan and evaluate programs, to direct policy decisions, and to monitor progress toward Healthy People 2000 and 2010 objectives. REPORTING PERIOD COVERED: This report covers data from 1993 through 1999. DESCRIPTION OF SYSTEM: The Pregnancy Risk Assessment Monitoring System (PRAMS) is an ongoing, state- and population-based surveillance system designed to monitor selected self-reported maternal behaviors and experiences that occur before, during, and after pregnancy among women who deliver a live-born infant. PRAMS employs a mixed-mode data collection methodology; up to three self-administered surveys are mailed to a sample of mothers, and nonresponders are followed up with a telephone interview. Self-reported survey data are linked to selected birth certificate data and weighted for sample design, nonresponse, and noncoverage to create annual PRAMS analysis data sets. PRAMS generates statewide estimates of various perinatal health topics among women delivering a live infant. Data for 1999 from 17 states are examined. In addition, trend data are examined for 12 states that had at least 3 years of data during 1993-1999. RESULTS: In 1999, the prevalence of unintended pregnancy resulting in a live birth ranged from 33.7% to 52% across the 17 states. During 1993-1999, only one state reported a decreasing trend in the prevalence of unintended pregnancy. Women aged <20 years, black women, women with less than or equal to a high school education, and women receiving Medicaid were more likely to report unintended pregnancy. The prevalence of late or no entry into prenatal care ranged from 16.1% to 29.9%. The prevalence of late or no entry into prenatal care significantly decreased over time in seven of the 12 states with trend data. In general, women aged <20 years, black women, women with less than a high school education, and women receiving Medicaid were more likely to report late or no entry into prenatal care. The prevalence of smoking during the last 3 months of pregnancy ranged from 6.2% to 27.2%, and the prevalence decreased in five states from 1993 to 1999. Overall, smoking during the last 3 months of pregnancy was associated with younger age (<25 years), non-Hispanic ethnicity, having less than or equal to a high school education, receiving Medicaid, and delivering a low birthweight infant. The prevalence of physical abuse by a husband or partner during pregnancy ranged from 2.1% to 6.3%. No trends were observed for physical abuse from 1996 to 1999, the only years for which these data were available. Across the 17 states, only Medicaid status was consistently associated with experiencing physical abuse during pregnancy. The prevalence of breast-feeding initiation ranged from 48% to 89%. Ten of 12 states with trend data reported increases in the prevalence of breast-feeding initiation. Overall, women aged <20 years, women with less than or equal to a high school education, and women receiving Medicaid were less likely to breast-feed. The prevalence of breast-feeding duration for at least 4 weeks ranged from 34.9% to 78.1%. From 1993 to 1999, increases in levels of breast-feeding for at least 4 weeks were observed in eight states. Women aged <25 years, black women, women with less than or equal to a high school education, and women receiving Medicaid were generally less likely to breast-feed for at least 4 weeks. The prevalence of back sleep position for infants ranged from 35.1% to 74.6%. Increases in the use of the back sleep position were observed in all 12 states with trend data from 1996 to 1999. Black race and having less than or equal to a high school education were consistently associated with not using the back sleep position. INTERPRETATION: For surveillance during 1993-1999, the majority or all states observed increases in breast-feeding initiation, breast-feeding for at least 4 weeks, and back sleep position. Approximately one half of the states observed decreases for late or no entry into prenatal care and smoking during the last 3 months of pregnancy. Little or no progress was observed in the prevalence of unintended pregnancy or physical abuse during pregnancy. With few exceptions, the 17 states failed to meet the Healthy People 2000 objectives for the seven reported behaviors in 1999. Certain de

Adolescent↗

Olfactory basis for the delayed onset of maternal behavior in virgin female rats: experimential effects.

A previous study showed that intranasal zinc sulfate (ZnSO4) treatment shortens the latencies for the onset of maternal behavior in nonpregnant rats. The aim of this study was to see whether after recovery from the effects of ZnSO4 treatment, the latencies for maternal behavior increased. In Experiment 1 nonpregnant females were intranasally infused with ZnSO4 or air or were left untreated and exposed to pups starting 48 hr later. Olfactory discrimination tests using chocolate bits were done simultaneously. The ZnSO4 treatment resulted in short latency maternal behavior (1.1 days) compared with latencies of control females (3.8 days), but neither group showed any loss of olfactory discrimination. Three weeks later- ZnSO4-treated females showed increased latencies for all but retrieving, while control groups showed decreased latencies for all maternal behaviors. In Experiment 2, intranasal ZnSO4- and air-treated females were given olfactory discrimination tests under food deprivation, using chocolate bits and guinea pigs pellets. Choice of guinea pig pellets was more severely affected than choice of chocolate bits, but recovery of the discriminations was complete in 4-5 days. The effects of ZnSO4 on maternal behavior and on olfactory discrimination in nonpregnant females were discussed.

Animals↗

Effects of small medial preoptic area lesions on maternal behavior: retrieving and nest building in the rat.

Previous studies in rats have demonstrated that large lesions in the medial preoptic area (MPOA) disrupt all aspects of maternal behavior. In the present study, small bilateral electrolyte lesions in the MPOA of lactating females abolished nest building and retrieving components of maternal behavior while crouching and nursing were unaffected. Animals which failed to show retrieval and nest building behaviors tended to have a greater area of lesion within the more dorsal part of the MPOA. Although the dorsal MPOA may play a role in the maintenance of the active components of maternal behavior, i.e. nest building and retrieving, another critical factor in determining which components of maternal behavior are disrupted may be the size of the lesion. As one increases the area of damaged tissue there is also an accompanying increase in the components of maternal behavior which are disrupted. No correlation was found between damage to the Sexually Dimorphic Nucleus of the preoptic area and retrieving and nest building.

Animals↗

Peripartum sex steroid profiles and endocrine correlates of postpartum maternal behavior in captive gorillas (Gorilla gorilla gorilla).

An association between pregnancy levels of estrogen and progesterone and maternal behavior has been demonstrated in several taxonomic orders of nonprimate and primate mammals, but has not so far been investigated in the gorilla. In this study we investigated whether prepartum titers of urinary estrone conjugates (E1C) or pregnanediol-3alpha-glucuronide (PdG) were related to postpartum maternal behavior in eight multiparous Western lowland gorilla females (Gorilla gorilla gorilla) housed in four zoological gardens. Urine samples were collected from each study animal for 14 days prepartum and 14 days postpartum, and measures of maternal responsiveness were scored during the first 15 days postpartum. Urine samples were assayed with radioimmunoassay for E1C and PdG. Results for the peripartum profiles of urinary E1C, as well as postpartum profiles of PdG, agree with previous findings for the gorilla, while results for late-pregnancy profiles of urinary PdG were inconclusive in confirming a prepartum increase or decrease. Neither prepartum levels of E1C or PdG, nor the E1C/PdG ratio were found to be related to measures of postpartum maternal behavior. This lack of association between late-pregnancy E1C titers per se and postpartum maternal behavior is contrary to findings in nonprimate and other primate species.

Animals↗

Maternal behavior of primiparous females in inbred strains of mice: a detailed descriptive analysis.

In the present study, we compared the maternal and non-maternal behaviors of primiparous females in both the light and dark phases during 3 weeks postpartum in five inbred strains of mice (BALB/c, CBA/Ca, C3H/He, C57BL/6, and DBA/2) to examine the strain differences in the behaviors in detail. Generally, nursing postures (arched-back, blanket, and supine) and pup lickings (anogenital and body) occurred more frequently in the light phase, whereas nest building occurred more frequently in the dark phase. As pups grew, arched-back and blanket nursing, anogenital and body licking, and nest building decreased, but supine nursing slightly increased. The present results revealed strain-specific variations in maternal behavior. In general, BALB did not engage in maternal behavior very vigorously, but the other four strains actively did. The patterns of strain differences were not parallel between the subcomponents of nursing posture or pup licking. CBA showed more arched-back and supine nursing, and DBA showed more blanket nursing. C57 and CBA showed more anogenital licking, while C3H and DBA showed more body licking. Strain differences were also found for the changes across postpartum days in almost all behaviors. These findings provide information to examine the effects of genetic and environmental factors on the development of maternal behavior in mice.

Analysis of Variance↗

Differential role of cholecystokinin receptor subtypes in opioid modulation of ongoing maternal behavior.

Cholecystokinin (CCK) can have effects opposite those of opioids. The present study was undertaken to determine whether peripheral injections of antagonists of the CCK1 receptor (lorglumide) and the CCK2 receptor (L-365,260) can influence the effects of morphine on maternal behavior during lactation. A total of 110 female Wistar rats were tested on days 5 and 6 postpartum. Groups were randomly assigned to morphine vehicle (MV-SC) + saline (S-IP), MV + lorglumide (LOR: 1.0 or 10.0 mg/kg), MV + L-365,260 (10 mg/kg), morphine chlorhydrate (MC: 7.0 mg/kg) + S, MC + LOR (1.0 or 10.0 mg/kg), and MC + L-365,260 (1.0 or 10 mg/kg). Maternal behavior testing was started 30 min after the injections, at which time pups were placed in the home cage of their mother. Latencies for retrieval, grouping, and crouching responses were scored. The results show that both lorglumide and L-365,260 potentiated the MC-induced inhibition of maternal behavior. In addition L-365,260 treatment alone inhibited maternal behavior. Blockade of both the CCK1 and CCK2 receptors potentiated the morphine-induced disruption of maternal behavior, while CCK2 antagonism alone also inhibited this behavior. The results suggest that CCK antagonism of opioid-induced disruption of maternal behavior occurs due to the action of CCK on both CCK1 and CCK2 receptor subtypes.

Animals↗

Effects of ethanol consumption on maternal behavior in the female rat.

Female rats consuming 30% ethanol (v/v) for 30 days prior to and during gestation, and during the post-partum period were tested for maternal behavior with either their own pups or pups provided by normal foster mothers. When tested with their own pups, ethanol consuming females displayed significant deficits in maternal behavior. However, when a second group of ethanol consuming females were tested with normal pups, the females displayed maternal behavior comparable to that of control females. These data suggest that gestational ethanol consumption per se does not produce a deficit in the ability to display maternal behavior. Possibly, due to ethanol related changes in the pup's own characteristics, they became a less attractive stimulus in eliciting the display of maternal behaviors from their mothers.

Alcohol Drinking↗

Intact neurons of the lateral habenular nucleus are necessary for the nonhormonal, pup-mediated display of maternal behavior in sensitized virgin female rats.

Our research has demonstrated that the lateral habenular nucleus (Lhb) is necessary for the hormonal onset but not the postpartum maintenance of maternal behavior in the rat (K. P. Corodimas, J. S. Rosenblatt, & J. I. Morrell, 1992; K. P. Corodimas, J. S. Rosenblatt, M. E. Canfield, & J. I. Morell, 1993; T. Matthews-Felton, K. P. Corodimas, J. S. Rosenblatt, & J. I. Morell, 1995). To test the role of the Lhb in the nonhormonal onset of maternal behavior, we used the sensitization model in which the continual exposure of females to pups induces maternal behavior. Ovariectomized females received bilateral cytotoxic lesions of neurons of either the Lhb or the dorsal medial cingulate cortex-hippocampus, or they were unoperated. Maternal behavior, activity, and oromotor carrying capability were tested. Complete lesions of the neurons of the Lhb induced significant deficits in pup retrieval and nest building. Sniffing, licking, and crouching behaviors were unaltered. Activity and carrying ability were normal. These results indicate a role for the Lhb that extends to the nonhormonally dependent onset of maternal behavior, but they also indicate a more limited role than in the mediation of the hormonal onset of the behavior.

Animals↗

Effects of stress during pregnancy on maternal behavior in mice.

The effects of stress experienced during pregnancy and raising stressed offspring on maternal behavior were investigated in Swiss-Webster mice. Dams were either stressed or not stressed during pregnancy, and raised either prenatally stressed or nonstressed cross-fostered pups. Maternal behaviors such as grooming, nursing, pup retrieval and maternal aggression were assessed during the first 4 days after birth. Nonstressed dams raising stressed pups and stressed dams raising nonstressed pups groomed and nursed their pups significantly less than did control dams (stressed dams raising stressed pups and nonstressed dams raising nonstressed pups). Nonstressed dams raising stressed pups were also the slowest to retrieve both the first and last pup in retrieval tests. Nonstressed dams raising nonstressed pups were significantly less aggressive than other dams. In contrast, stressed dams raising stressed pups exhibited high levels of nursing and grooming, retrieved their pups rapidly and were very aggressive towards an intruder. These results indicate that raising stressed pups, or experiencing stress during a pregnancy can have significant effects on maternal behaviors. Stressed dams raising stressed pups exhibit maternal care comparable to that of nonstressed dams raising nonstressed pups at least for nesting/nurturing behaviors, and show increased levels of aggression and pup retrieval.

Aggression↗

Long-term effects of preoptic area knife cuts on the maternal behavior of postpartum rats.

Knife cuts severing the lateral connections of the medial preoptic area disrupt maternal behavior in postpartum rats. In these studies the knife cuts were produced 1-2 days prior to behavioral testing. The present study examined whether preoptic area knife cuts produce long-term deficits in maternal behavior. Nulliparous Charles River CD rats received knife cuts severing the lateral connections of the medial preoptic area or sham cuts. Approximately 2 weeks later they were mated. All females delivered young 22-23 days after mating, and litter size did not differ between the groups. Females with preoptic knife cuts cleaned their young, built nests (albeit of inferior quality), crouched over their young in a nursing posture, and lactated. The major deficit shown was the near total elimination of retrieval behavior. Females with preoptic knife cuts, however, were capable of performing the oral-motor responses associated with hoarding behavior. These results show that severing the lateral connections of the medial preoptic area does produce long-term deficits in maternal behavior, particularly with respect to maternal retrieving.

Animals↗

Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin.

Oxytocin produces uterine contractions and milk ejection, functions related to parturition and nuturing. Studies were conducted to determine if this peptide, native to the brain and the posterior pituitary gland, plays a role in the induction of maternal behavior. Intact virgin female rats were given 0.4 mug of oxytocin, 0.4 mug of [Arg(8)]vasopressin, or saline through lateral ventricular cannulae. Forty-two percent of intact rats receiving oxytocin displayed full maternal behavior towards foster pups. None of the saline- or vasopressin-treated animals displayed full maternal behavior. Criteria in five behavioral categories had to be fulfilled by an animal within 2 hr of injection for its behavior to be considered fully maternal. When partial maternal responses were considered, oxytocin was significantly more effective than saline and marginally more effective than vasopressin. Five animals responding fully maternally after oxytocin injection were allowed to stay with pups for 10 days. All five continued to display full maternal behavior during this time. Nearly all animals that responded fully maternally to oxytocin injection were in the last day of diestrus or in proestrus or estrus. This suggested that elevated or recently elevated levels of estrogen may be necessary for the induction of full maternal behavior by oxytocin. Twenty-seven virgin female rats were ovariectomized and given either 100 mug of estradiol benzoate per kg in oil subcutaneously or oil alone immediately after operation. Forty-eight hours later, all animals received 0.4 mug of oxytocin intracerebroventricularly. Eleven of 13 estrogen-primed animals became fully maternal; none of 14 nonprimed animals became fully maternal.

Animals↗

Opiate regulation of maternal behavior in the rat.

The effects of the opiate agonist morphine, the opiate antagonist naloxone and the weak opiate nonanalgesic dextrorphan on the expression of maternal behavior were investigated in a series of three experiments. In the first experiment treatment of rats with morphine (5 mg/kg, subcutaneously) after ovariectomy and hysterectomy on day 17 of gestation resulted in a disruption in the onset and quality of maternal responsiveness in the homecage and in a T-maze test. The duration of morphine's acute disruptive action was 2-4 hours. In the second experiment concurrent treatment of morphine-injected rats with naloxone prevented the disruptive effects of morphine in both the homecage and T-maze tests. The effects of morphine did not appear to result from a severe alteration in activity levels as measured in an open-field test, although morphine did increase activity slightly by the fifth day of treatment. In the third experiment treatment of rats after ovariectomy plus hysterectomy on day 17 of gestation with dextrorphan failed to disrupt maternal behavior. These results indicate that morphine disrupts maternal behavior through an opiate receptor mechanism, and suggests to us that endogenous opiates may mediate the expression of maternal behavior under certain physiological conditions.

Animals↗