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Using c-Fos immunocytochemistry to identify forebrain regions that may inhibit maternal behavior in rats.

Evidence indicates there is a neural system that inhibits maternal behavior in virgin rats. It has been suggested that pregnancy hormones promote the onset of maternal behavior by reducing the behavioral influence of this system. The authors used c-Fos immunocytochemistry to identify brain regions more activated by pup exposure in nonmaternal rats than in maternal rats. Previous experiments indicated that some of these regions, such as the posterodorsal medial amygdala and several medial hypothalamic sites, inhibit maternal behavior. For others, such as the ventral lateral septum, dorsal premammillary nucleus, and principal bed nucleus of the stria terminalis, this is the first indication that they could also inhibit maternal responding. These regions have previously been implicated in promoting defensive behaviors, consistent with the finding that nonmaternal rats actively avoid pups. These findings suggest the existence of a neural circuit through which pup exposure could promote defensive responses in virgin rats, and how pregnancy hormones could reduce such activity to stimulate maternal behavior.

Animals↗

Hospital units as social contexts: effects on maternal behavior.

This paper examines the impact of different styles of nursing in maternity units on maternal behavior. These styles are found to be independent of the units' formal organizational characteristics and to vary depending on specific nursing tasks. The degree to which unit management affords opportunities for individualized patient teaching probably has the greatest impact on maternal behavior. Forty-five mothers, closely matched on ethnicity, age, marital status, socioeconomic status and parity, who delivered in three different hospital units, were observed systematically while feeding their infants. The investigators' observations, supplemented by measures of nurse task conceptions and perceptions of work structure, were used to characterize each unit. Analyses of variance, in which each hospital represented a fixed level of treatment, showed that mothers in the moderately supportive unit were significantly more affectionate and responsive towards their infants, and behaved less passively towards them, than mothers in units where nursing work was highly routinized or where zeal for innovation predominated. The moderately supportive unit also significantly diminished the effects of social class and of prior experience with children on affectionate maternal behavior. The threat to validity posed by self-selection of mothers into hospital units was accounted for by the selection of hospitals owned by one prepaid group plan, each serving socioeconomically similar populations in different catchment areas, and by data from the mothers which showed that plan membership and hospital selection were governed by financial considerations and geographical convenience. The findings provide evidence that the social context of the hospital unit--particularly the opportunity for individualized interaction between nurse and patient--may have an effect on early maternal behavior which is independent of the mother's own characteristics.

California↗

Hysterectomy-induced maternal behavior during pregnancy in the rat.

Hysterectomies were performed between the 10th and 19th day of pregnancy, and females were tested with pups for the onset of maternal behavior starting 0,24, 48, or 72 hr after surgery. Pups remained with the females overnight, and testing was repeated daily with fresh pups until females exhibited maternal behavior. Latencies for the onset of maternal behavior were shorter after hysterectomy on the 10th and 16th days of pregnancy than in intact pregnant females at the same stages of pregnancy; latencies became shorter, the later the termination of pregnancy. When the ovaries were removed along with hysterectomy during pregnancy, short-latency maternal behavior no longer was exhibited. Pregnant females were tested during the last 40 hr of pregnancy: nest building began at 34 hr prepartum and retrieving at 28 hr prepartum. The effect of hysterectomy during pregnancy on ovarian secretion of estrogen and progesterone is reviewed, and it is concluded that the rise in estrogen secretion, which follows hysterectomy during pregnancy, is most likely the cause of the rapid onset of maternal behavior after hysterectomy. A similar proposal is made for the prepartum onset of maternal behavior in intact pregnant females.

Animals↗

Nonhormonal basis of maternal behavior in the rat.

Rats were tested for induction of maternal behavior by exposing them to young pups continously for 10 to 15 days. Nonpregnant intact, ovariecto-mized. and hypophysectomized females were studied, as well as intact and castrated males. Nearly all the animals exhibited the four main items of maternal behavior and there were only minor differences in the latencies for the onset of maternal behavior among the various groups. It is concluded that all rats have a basic level of maternal responsiveness which is independent of hormonal stimulation.

Analysis of Variance↗

Lesions of the hypothalamic paraventricular nucleus disrupt the initiation of maternal behavior.

Electrolytic lesions of the paraventricular nucleus (PVN) of the hypothalamus were found to disrupt the initiation but not the maintenance of maternal behavior in primiparous Sprague-Dawley rats. Following lesions performed on Day 15 of gestation, measures of maternal behavior (grouping, crouching, and nest building), pup retrieval, and pup weight gain were all impaired, but only if the lesion included the most rostral and medial aspects of the PVN. Lesions sparing these regions and sham surgery were generally ineffective. In a separate experiment, PVN lesions performed on Day 4 postpartum had relatively little effect on maternal behavior. As females lesioned prepartum showed changes in open-field behavior as well as maternal behavior, the PVN may be important for modulating responses not only to pups but to several kinds of novel stimuli. These results may also further implicate oxytocin, which is synthesized in the PVN, in the initiation of maternal behavior.

Animals↗

A potential role for thalamocingulate circuitry in human maternal behavior.

BACKGROUND: Little is known about the regional brain basis of human maternal behavior. To understand this better, we have been examining brain activity in mothers listening to infant cries. METHODS: We measured functional Magnetic Resonance Imaging brain activity in healthy, breastfeeding first-time mothers with young infants while they listened to infant cries, white noise control sounds, and a rest condition. Based on the thalamocingulate theory of maternal behavior and pilot work, we hypothesized that the cingulate, medial thalamus, medial prefrontal cortex, and right orbitofrontal cortex would display more activity with infant cries than with white noise (comparison 1) and would uniquely activate with the cries, meaning that these regions would display activity with cry minus rest but not with white noise minus rest (comparison 2). RESULTS: In hypothesized regions, the group displayed more activity in the medial thalamus, medial prefrontal and right orbitofrontal cortices with both comparisons. The anterior and posterior cingulate cortex displayed more activity only with comparison 1. In non-hypothesized brain regions, several other structures thought important in rodent maternal behavior displayed activity with both comparisons including the midbrain, hypothalamus, dorsal and ventral striatum, and vicinity of the lateral septal region. CONCLUSIONS: Our results partially support our hypotheses and are generally consistent with neuroanatomical studies of rodent maternal behavior.

Adult↗

Early postnatal diazepam exposure facilitates maternal behavior in virgin female rats.

Virgin female rats do not display maternal behavior if they are not exposed to the pups during several days. This exposure is called induction. In this work we have studied the effects of early postnatal (PO-P16) diazepam (DZ) administration (1 and 2.5 mg/kg, SC) on the display of maternal behavior of virgin female rats when adults. Although we did not find statistically significant differences between P0-P16 DZ treated and control females with respect to the latency of retrieval, P0-P16 DZ administration resulted in a statistically significant increase of the percentage of female rats that became maternal, showing retrieval behavior. This early postnatal treatment with DZ also increased other variables that are currently measured in maternal behavior tests, such as: time of physical contacts, grooming, crouching, and nest building quality. No statistically significant differences were found in the body weight of treated versus control animals during development, nor during adulthood. Our results provide further evidence that the GABAA-BDZ-Cl- receptor complex is implicated in the development of maternal behavior in female rats.

Analysis of Variance↗

The relationship of developmental variables to maternal behavior.

Developmental differences in self-concept, personality integration, flexibility, empathy, and temperament, and the relationship of these variables to maternal behavior, were investigated using three age groups of first-time mothers. The age groups also were tested for change in self-concept and personality integration from 1 to 3 days postpartum to 8 months postbirth. The longitudinal study included 60 mothers aged 15-19 years, 138 aged 20-29 years, and 90 aged 30-42 years. Self-completed instruments were used to measure the personality variables, and an interviewer-rated instrument measured maternal behavior. Personality integration and flexibility increased significantly and correlated significantly with age indicating that both are developmental constructs. Empathy and temperament traits did not increase with age, although teenage scores were significantly lower in empathy, self-concept, several temperament traits, and maternal behavior. The two older groups' self-concept decreased significantly the first eight months of motherhood. In the teenage group personality integration, empathy, activity level, intensity and threshold to stimulus were significantly correlated with maternal behavior. In the 20-29 year-old group, self-concept, personality integration, flexibility, rhythmicity, adaptability, intensity and mood quality correlated significantly with maternal behavior. In the older group, self-concept, flexibility, approach/withdrawal, adaptability, intensity, and mood quality correlated significantly with maternal behavior.

Adaptation, Psychological↗

Projection sites of medial preoptic area and ventral bed nucleus of the stria terminalis neurons that express Fos during maternal behavior in female rats.

Medial preoptic area (MPOA) and ventral bed nucleus of the stria terminalis (VBST) neurons are involved in maternal behavior, but the neural sites to which the maternally relevant neurons project have not been determined. Since MPOA and VBST neurons express Fos during maternal behavior, we used a double-labeling immunocytochemical procedure to detect both Fos and a retrograde tracer, wheat germ agglutinin (WGA), in order to determine where these Fos neurons project. On Day 4 postpartum, fully maternal females were separated from their litters. On Day 5, WGA was iontophoretically injected into one of the following regions known to receive MPOA and/or VBST input: Lateral septum, medial hypothalamus at the level of the ventromedial nucleus, lateral habenula, ventral tegmental area, retrorubral field, or periaqueductal gray. On Day 7, females received a 2-h test with either pups or candy, after which they were perfused and their brains were processed for the detection of Fos and WGA. As expected, females tested with pups had more Fos-containing neurons in the MPOA and VBST than did females tested with candy. After WGA injections into several brain sites, the number of double-labeled cells observed in the MPOA and VBST was greater for the maternal females when compared to the non-maternal females. Therefore, these results pinpointed neural circuits that were activated during maternal behavior. For the maternal females, Fos-containing neurons in the MPOA projected most strongly to the medial hypothalamus at the level of the ventromedial nucleus and to the lateral septum, while Fos-containing neurons in the VBST projected most strongly to the retrorubral field, ventral tegmental area, and medial hypothalamus. Although relatively few MPOA and VBST neurons which expressed Fos during maternal behavior projected to the periaqueductal gray, these Fos-expressing neurons made up a relatively large proportion of the MPOA and VBST projection to the periaqueductal gray. This study suggests that MPOA and VBST efferents project to a variety of regions to promote full maternal responsiveness.

Animals↗

The content of dopamine, serotonin, and their metabolites in the neural circuit that mediates maternal behavior in juvenile and adult rats.

Continuous exposure of non-parturient rats to pups can induce maternal behavior similar in most aspects to that found in the postpartum rat. Surprisingly, young juvenile rats (20-24 days of age) only require 1-3 days of exposure to pups, while adults require 4-8 days before maternal behavior emerges. Dopamine (DA) and possibly serotonin (5-HT) may mediate the expression of adult maternal behavior. We hypothesize that postnatal changes in DA and 5-HT within the neural circuit that supports maternal behavior including the medial preoptic area (MPOA), medial and cortical amygdala (MCA), and nucleus accumbens (NAC), may underlie these differences in responsiveness across juveniles and adults. We measured DA, 5-HT, and their metabolites in postmortem samples of these regions in maternal and non-maternal juvenile and adult females. The only difference found across behavioral groups was that the MPOA of adults induced into maternal behavior by pup exposure had more DA than did that of isolated adult females or maternal juveniles. However, when adults versus juveniles were compared, the content of DA and 3,4-dihydroxyphenylacetic (DOPAC) was higher in the adult than in the juvenile NAC and MCA; the content of 5-HT and 5-hydroxyindoleacetic acid (5-HIAA) in these structures did not vary across the age groups. In contrast, higher levels of 5-HT and 5-HIAA were found in the MPOA in juveniles compared to adults. We propose that these region-specific age differences in DA and 5HT may underlie differences in juvenile-adult responses to pups.

Age Factors↗

Motivational systems and the neural circuitry of maternal behavior in the rat.

Jay Rosenblatt's approach-avoidance model of maternal behavior proposes that maternal behavior occurs when the tendency to approach infant stimuli is greater than the tendency to avoid such stimuli. Our research program has uncovered neural circuits which conform to such a model. We present evidence that the medial preoptic area (MPOA: located in the rostral hypothalamus) may regulate maternal responsiveness by depressing antagonistic neural systems which promote withdrawal responses while also activating appetitive neural systems which increase the attractiveness of infant-related stimuli. These MPOA circuits are activated by the hormonal events of late pregnancy. Preoptic efferents may suppress a central aversion system which includes an amygdala to anterior hypothalamic circuit. Preoptic efferents are also shown to interact with components of the mesolimbic dopamine (DA) system to regulate proactive voluntary maternal responses. We make a distinction between specific (MPOA neurons) and nonspecific motivational systems (mesolimbic DA system) in the regulation of maternal responsiveness.

Amygdala↗

Estrogen implants in the medial preoptic area stimulate maternal behavior in male rats.

The present study investigated whether the medial preoptic area (MPOA) mediates estrogen stimulation of maternal behavior in the male as it does in the female. Previous studies have shown that lesions of the medial preoptic area prevent sensitization of maternal behavior in male rats and that in gonadectomized, hormonally primed males, systemically administered estradiol benzoate stimulates short-latency maternal behavior. These findings are similar to those found in females. In the present study adult males were gonadectomized and hormonally primed with subcutaneously implanted capsules of estradiol (Days 1-16) and progesterone (Days 3-15) and then were stereotaxically implanted bilaterally in the MPOA with implants containing 10% estradiol. Tests with young pups were started 48 h later and continued for 10 days (11 tests). Control groups were implanted in the MPOA with cholesterol or were injected subcutaneously with estradiol benzoate (100 microg/kg). Estradiol implanted males had shorter latencies for maternal behavior (retrieving, crouching, licking pups) than cholesterol implanted males, but their latencies were slightly longer than those of estradiol benzoate injected males. The medial preoptic area, therefore, mediates estrogen stimulation of maternal behavior in males as it does in females.

Animals↗

Early weaning deprives mouse pups of maternal care and decreases their maternal behavior in adulthood.

Weaning is one of the most important events in the early stage of life, and recently we have found that precocious weaning augments anxiety and aggressiveness in mice. Maternal behavior has been reported to be transmitted from one generation to the next; that is, female pups that received intensive maternal care showed higher maternal behavior in their adulthood. In the present study, the following three experiments were conducted to understand maternal behavior transmission in early-weaned mice that were separated from the dam on postnatal day 14. First, the maternal behavior observed from the postpartum day 15 to 21, which was deprived in the early-weaned mice, were analyzed. Mothers spent 3% of their time on licking/grooming and arched-back nursing of their pups on postpartum day 15, and the time spent on these behaviors was gradually decreased until postpartum day 21; however, they spent 50% of their time attending to their pups through postpartum days 15-21. Simultaneously, the behavior of the pups was monitored, and it was found that the early-weaned mice had higher activity and lower resting behavior over the period from postnatal day 15 to 21. Secondly, the early- and normally weaned female mice were subjected to an elevated plus maze test at the age of 8 weeks to assess their anxiety level. The early-weaned mice showed a lower frequency of entering the open arms, and a shorter duration of time spent within them, as compared to the normally weaned mice, suggesting that early-weaned females had a higher anxiety level. In the third experiment, the two groups of female mice were paired with adult male mice for 2 weeks, and the mother's maternal behavior was analyzed. The early-weaned female mice showed lower frequency of licking/grooming and arched-back nursing of their pups as compared to the normally weaned mice, whereas the time of mother-off pups and attending to pups were not different between groups. These results suggest that early-weaning manipulation deprives offspring of a certain level of maternal care, and as a consequence, the offspring show higher anxiety levels and lower maternal behavior in their own adulthood.

Analysis of Variance↗

Preoptic area and substantia nigra interact in the control of maternal behavior in the rat.

This study provides evidence that the preoptic region and the substantia nigra interact in the control of maternal behavior. In the first experiment, large electrolytic lesions of the substantia nigra were found to severely disrupt maternal behavior and cause stereotyped motor activity in postpartum lactating rats. In order to test the hypothesis that the preoptic region and the substantia nigra interact in the control of maternal behavior, a second experiment employed an asymmetrical lesion design. Postpartum lactating rats that received a unilateral knife cut severing the lateral connections of the medial preoptic area and a contralateral lesion of the substantia nigra showed larger deficits in maternal behavior than either sham females or females that received a unilateral preoptic knife cut paired with an ipsilateral substantia nigra lesion. Measurements of body weights, body temperatures, and stereotyped behavior indicated that the differences in maternal behavior between the ipsilateral and contralateral groups could not be explained on the basis of nonspecific effects.

Animals↗

Relationship of maternal behavioral style to the development of organically impaired mentally retarded infants.

The relationship of maternal behavioral style to the cognitive developmental status of 60, 1-, 2-, and 3-year-old organically impaired, mentally retarded children was investigated. Eighteen global maternal behaviors and four child behaviors were rated on a 10-minute video tape of mother-child play. A factor analysis of the maternal behavioral items revealed three major parameters of behavior. Child-Oriented/Maternal Pleasure was related positively, whereas Quantity of Stimulation and Control were related negatively to Children's Bayley Mental Development scores. Maternal behavioral style was not related to either the ratings of the children's behavior or to the children's current health status and family SES, but was related to the amount of time children had been in intervention programs. Findings were discussed in terms of their implications for intervention with mothers and their retarded infants.

Age Factors↗

Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors.

Naturally occurring variations in maternal licking/grooming influence neural development and are transmitted from mother to female offspring. We found that the induction of maternal behavior in virgin females through constant exposure to pups (pup sensitization) was significantly shorter in the offspring of High compared with Low licking/grooming mothers, suggesting differences in maternal responsivity. In randomly selected females screened for individual differences in maternal responsivity and subsequently mated, there was a significant and negative correlation (r = -0.73) between the latency to exhibit maternal behavior in the pup sensitization paradigm and the frequency of pup licking/grooming during lactation. Females that were more maternally responsive to pups and that showed increased levels of pup licking/grooming also showed significantly higher oxytocin receptor levels in the medial preoptic area, the lateral septum, the central nucleus (n.) of the amygdala, the paraventricular n. of the hypothalamus, and the bed n. of the stria terminalis. Intracerebroventricular administration of an oxytocin receptor antagonist to mothers on postpartum day 3 completely eliminated the differences in pup licking/grooming, suggesting that differences in oxytocin receptor levels are functionally related to maternal behavior. Finally, estrogen treatment of virgin females significantly increased oxytocin receptor binding in the medial preoptic area and lateral septum of female offspring of High, but not Low, licking/grooming mothers. These findings suggest that maternal licking/grooming influences the development of estrogen sensitivity in brain regions that regulate maternal behavior, providing a potential mechanism for the intergenerational transmission of individual differences in maternal behavior.

Animals↗

Maternal behavior of beef cows at parturition.

Over an 11-yr period maternal behavior, calf birth weight and calf condition were recorded within 24 h for 2,684 parturitions. Maternal behavior was rated on a scale from 1 to 11, where 1 indicated extreme aggressiveness and 11 indicated no maternal attentiveness. Birth condition was rated on a scale from 1 to 9, with 9 being fattest and 1 thinnest. Respective breed means of Hereford, Angus, Charolais and Red POll were 6.2, 5.3, 6.0, and 5.7 for maternal behavior rating; 30.6, 27.3, 39.2 and 32.6 kg for birth weight, and 5.5, 4.7, 5.6 and 5.5 for birth condition. Heritability estimates for maternal rating, birth weight and birth condition were .06 +/- .01, .48 +/- .02 and .19 +/- .01, respectively. Genetic correlations between maternal rating and birth weight and condition were .04 +/- .05 and -.02 +/- .06, respectively. These results suggest that, in the population of cows studied, nongenetic influences were the primary cause of differences in aggressiveness of cows at parturition.

Aggression↗

Effects of prenatal stress on maternal behavior in the rat.

Some authors reported a link between maternal stress and disturbances in their infants. Because of difficulties due to human research, the effects of prenatal stress have to be examined in animal models. Our approach was original in that the stressor was an ecological one and was applied at a given gestational day. Indeed, the stressor was a cat and the effects of stress on maternal behavior were investigated in five groups of 10 female rats: two groups were composed of females which were acutely stressed either at the 10th or the 14th gestational day; two other groups were composed of females which were repeatedly stressed either at the 10th or the 14th gestational day; the fifth group comprised non-stressed females. Plasma corticosterone concentrations measured in blood samples collected from dams just after stress were significantly higher than in controls showing that cat represents an efficient stressor for rats. Maternal behavior was recorded during 30 min at the 2nd, 4th, and 6th postnatal days. In all cases, stressed dams' activities directly directed towards the pups (retrieving, sniffing and licking), those non-directly directed towards the pups (carrying its tail and digging the sawdust), and those directed towards themselves (eating, drinking and resting) were altered to different degrees. These alterations in maternal behavior can explain, at least in part, the mortality and the low growth rate observed in pups born from stressed dams.

Animals↗