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PubMed1986

Identification of medial preoptic neurons that concentrate estradiol and project to the midbrain in the rat.

Fluorescent dye retrograde tracing was combined with steroid hormone autoradiography to study the midbrain projections of the estrogen-concentrating neurons in the preoptic region of the rat brain. Microinjections of the dyes DAPI, true blue, or a mixture of DAPI and primuline were made into the ventral tegmental area and into the midbrain central gray of ovariectomized, adrenalectomized 2-3-month-old female rats; 3 or 4 days later these animals were injected with [3H]estradiol; the brains were then processed for autoradiography. After exposures of from 3 to 12 months, the autoradiograms were developed and examined for reduced silver grains under cell nuclei (indicating binding of [3H]estradiol) and retrogradely transported fluorescent dye in the cytoplasm (indicating an efferent projection to the midbrain). Numerous [3H]estradiol-concentrating neurons in the medial preoptic region were found to send their axons to the medial midbrain. The largest numbers of estrogen target neurons that were afferent to the ventral tegmental area and to the midbrain central gray were found in the medial preoptic nucleus, in the surrounding medial preoptic area, and in the ventral bed nucleus of the stria terminalis. Double-labeled neurons were also identified in the preoptic suprachiasmatic area, in the lateral preoptic area, and in the rostral anterior hypothalamic area. Thus, a subset of the gonadal steroid target cells of the preoptic region have long projections to the medial midbrain, and a subset of the medial preoptic neurons that project to the ventral tegmental area and to the midbrain central gray concentrate estrogen. Behaviors (for example, maternal behavior, male copulatory behavior, and wheel-running) that are regulated by estrogen action in the medial preoptic region may be controlled by the direct estrogen-sensitive pathway to the medial midbrain revealed in this study.

Animals↗
PubMed1997

The integrative neurobiology of affiliation. Introduction.

The research presented at this conference, including a series of excellent posters from junior investigators, documents the pervasive importance of affiliation and other social behaviors. Affiliative behaviors interact with, but are distinct from reproductive and aggressive behaviors. Patterns of social behaviors tend to be more species-typical than the behaviors associated with reproduction or aggression. However, neural circuits necessary for approach or avoidance also are necessary for the expression of various types of affiliative behavior such as maternal behavior or pair-bond formation. Furthermore, candidate neurochemical systems have been identified that contribute to various types of affiliative behavior. For example, studies revealing new behavioral functions for steroid hormones of the adrenal axis, such as corticosterone, and neuropeptides, including the endorphins, oxytocin and vasopressin, extend our general knowledge of neurobiology; they may also lead to studies that expand our understanding of social behavior and the connections to systems that regulate emotions. The work represented in this volume also has important implications for the study of serious neuropsychiatric disorders. For example, episodes of certain of these disorders can be induced by social stressors; in other disorders, a marked decrease in affiliative behaviors is a prominent feature of the patients' difficulties. Furthermore, abnormalities in animal systems implicated in the neurobiology of affiliation (oxytocin, vasopressin, and the hypothalamic-pituitary-adrenal system) have also been documented for major depression in humans. Animal models, such as those described at this conference, offer evolutionary perspectives, from which it is possible to extract general principles. At the same time, our understanding of the mechanistic and neurobiological substrates of both constructive and destructive social behaviors is increasing. At the conference, the evolutionary and mechanistic perspectives converged on the theme that studies of affiliative behaviors cannot be fully interpreted in isolation from other social behaviors; neither can they effectively be isolated from the biological and social contexts that shape their expression. Advances in this research area seem dependent on integrating experimental research across levels of analysis. Although this task is challenging, we are confident that an awareness of integrative principles can lead to new and important research opportunities.

Aggression↗
PubMed2004

Primary parental preoccupation: circuits, genes, and the crucial role of the environment.

Parental caregiving includes a set of highly conserved behaviors and mental states that may reflect both an individual's genetic endowment and the early experience of being cared for as a child. This review first examines the mental and behavioral elements of early parental caregiving in humans. Second, we consider what is known about the neurobiological substrates of maternal behaviors in mammalian species including some limited human data. Third, we briefly review the evidence that specific genes encode proteins that are crucial for the development of the neural substrates that underlie specific features of maternal behavior. Fourth, we review the emerging literature on the "programming" role of the intrauterine environment and postnatal caregiving environment in shaping subsequent maternal behavior. We conclude that there are critical developmental windows during which the genetically determined microcircuitry of key limbic-hypothalamic-midbrain structures are susceptible to early environmental influences and that these influences powerfully shape an individual's responsivity to psychosocial stressors and their resiliency or vulnerability to various forms of human psychopathology later in life.

Environment↗
PubMed1987

Preoptic area opioids and opiate receptors increase during pregnancy and decrease during lactation.

Opiate receptor and endogenous opioid content were determined in pregnant, lactating, ovariectomized, and ovariectomized and subsequently estradiol- and progesterone-treated adult female rats. Levels of estradiol and progesterone produced by Silastic capsules implanted in animals of the ovariectomized, hormone-treated group were similar to natural levels of those hormones induced during pregnancy. Quantitative receptor autoradiography and radioimmunoassay were used to determine [3H]naloxone binding density and immunoreactive beta-endorphin content, respectively, in the preoptic area of the hypothalamus. Both opiate receptor binding density and beta-endorphin content in the preoptic area varied in the same direction in all experimental groups. The highest levels of both were observed during pregnancy and the lowest levels during lactation. Ovariectomy without subsequent hormone treatment produced intermediate levels of both opiate receptor and beta-endorphin. Ovariectomy with experimentally-induced estradiol and progesterone levels similar to those of pregnancy produced opiate receptor density and beta-endorphin content similar to those observed in pregnant animals. These data suggest that gonadal steroids are capable of altering function of the endogenous opiate system in the preoptic area. Moreover, preoptic area levels of opioids and opiate receptors are normally elevated during pregnancy and reduced during lactation. Since opiates are known to disrupt ongoing maternal behavior, a reduction of preoptic opiate function during lactation may be required to promote normal maternal behavior. The specific preoptic region involved in opiate regulation of maternal behavior may be illustrated by the zone of opiate receptor alteration observed herein.

Animals↗
PubMed1999

Feasibility of using fMRI to study mothers responding to infant cries.

While parenting is a universal human behavior, its neuroanatomic basis is currently unknown. Animal data suggest that the cingulate may play an important function in mammalian parenting behavior. For example, in rodents cingulate lesions impair maternal behavior. Here, in an attempt to understand the brain basis of human maternal behavior, we had mothers listen to recorded infant cries and white noise control sounds while they underwent functional MRI (fMRI) of the brain. We hypothesized that mothers would show significantly greater cingulate activity during the cries compared to the control sounds. Of 7 subjects scanned, 4 had fMRI data suitable for analysis. When fMRI data were averaged for these 4 subjects, the anterior cingulate and right medial prefrontal cortex were the only brain regions showing statistically increased activity with the cries compared to white noise control sounds (cluster analysis with one-tailed z-map threshold of P < 0.001 and spatial extent threshold of P < 0.05). These results demonstrate the feasibility of using fMRI to study brain activity in mothers listening to infant cries and that the anterior cingulate may be involved in mothers listening to crying babies. We are currently replicating this study in a larger group of mothers. Future work in this area may help (1) unravel the functional neuroanatomy of the parent-infant bond and (2) examine whether markers of this bond, such as maternal brain response to infant crying, can predict maternal style (i.e., child neglect), offspring temperament, or offspring depression or anxiety.

Adult↗
PubMed2005

Motherhood and the hormones of pregnancy modify concentrations of hippocampal neuronal dendritic spines.

Short-term fluctuations in steroid hormones such as estradiol (E2) and progesterone (P) can affect the concentration of hippocampal dendritic spines in adult, cycling nulliparous female rats. Pregnancy is characterized by a significantly longer duration of substantially elevated E2 and P compared to the estrous cycle. Thus, even greater changes than those reported during estrus may be evident. In two experiments, we examined the extent to which reproductive and hormonal state altered the concentration of apical neuronal dendritic spines of the CA1 region of the hippocampus in the following age-matched groups (N's = 7-10/group) of rats: in Exp. 1., CA1 dendritic spine density was examined in nulliparous diestrus (DES), proestrus (PRO), and estrus (ES) females, and late-pregnant (LP) (day 21) and lactating (day 5-6; LACT) females. In Exp. 2, the effects on spine density of a regimen mimicking pregnancy (and that stimulates maternal behavior) were examined, using ovariectomized, no hormone-exposed (OVX-minus) vs. sequential P&E(2)-treated (OVX + P&E2) groups. For both experiments, brains were removed, Golgi-Cox-stained and the most lateral tertiary branches of the apical dendrite of completely-stained hippocampal CA1 pyramidal neurons were traced with oil-immersion at x 1600 and dendritic spine density (# spines/10 micro dendritic segment) recorded. In Exp. 1, spine density was increased in LP and LACT females (which were not different) compared to the other virgin groups, including PRO females, who had more spines than DES and ES. In Exp. 2, OVX + P&E2 displayed significantly more dendritic spines per 10 micro than OVX-minus females (and had numbers that were similar to those of LP and LACT from Exp. 1). Pregnancy and its attendant hormonal fluctuations, therefore, may alter hippocampal neurons that regulate some non-pup-directed components of maternal behavior (e.g., nest building) or behaviors that support maternal behavior (e.g., foraging, associative memory).

Animals↗
PubMed1990

Activation of excitatory amino acid inputs to supraoptic neurons. II. Increased dye-coupling in maternally behaving virgin rats.

Electrical stimulation of the lateral olfactory tract (LOT) has been shown to excite, monosynaptically, supraoptic nucleus (SON) neurons in slices of hypothalamus taken from male, virgin female or lactating rats. Only in the last of these, however, did 10 min of 10 Hz stimulation produce an increase in the incidence of Lucifer yellow dye-coupling, an indicator of electrotonic interactions. This coupling is virtually exclusively dendrodendritic. Since virgin females that have been induced to show full maternal behavior have altered dendritic morphology reminiscent of lactating animals (but different from males and untreated virgins) we investigated the effects of LOT stimulation in slices from maternally behaving virgins. Similar to the data for lactating rats, electrical stimulation of this tract, the terminals of which release excitatory amino acid transmitter, increased the incidence of dye-coupling by 112% (P less than 0.01). Also similar to lactating rats, the coupling was dendrodendritic and the increase was due entirely to increasing the number of neurons coupled to the injected neuron. No increase in coupling was seen in stimulated slices from pup-exposed control rats. We conclude that the maternal behaviors engaged in by both real mothers and induced virgins 'primes' the supraoptic neurons to increase coupling in response to olfactory system stimulation. This priming may occur via olfactory and vomeronasal stimulation during such behaviors as sniffing and anogenital licking of the pups. That coupling increased in tissue from maternally behaving virgins comparably to that from nursing mothers further suggests that SON neurons may play a role in maternal behavior independent of its well-documented role in the milk ejection reflex.

Action Potentials↗
PubMed1995

Maternal aggression in rats: effects of olfactory bulbectomy, ZnSO4-induced anosmia, and vomeronasal organ removal.

Previous studies from our laboratory indicate that somatosensory inputs to the snout and ventral trunk, but not visual or auditory stimuli, play critical roles in the elicitation and maintenance of maternal aggression by lactating Norway rats toward a strange male intruder. There are conflicting reports on the influence of olfaction on maternal aggression. We explored the possible roles of central or peripheral anosmia on maternal aggression in Long-Evans rats during early lactation. In Experiment 1, responsiveness to both volatile and non-volatile odors was eliminated by bilateral olfactory bulbectomy (BOB), carried out during mid-gestation. BOB resulted in a reduced likelihood and intensity of maternal aggression on days 1 and 5 of lactation (L1 and L5), but also severe deficiencies in maternal behavior and litter growth and survival. In Experiment 2, anosmia to volatile odors was induced by spraying zinc sulfate intranasally on gestation day 21 and L1. This treatment had little or no effect on maternal aggression on L1 or L2 or on maternal behavior, especially if there was a 1-day recovery between the second treatment and testing. In Experiment 3, responsiveness to non-volatile odors was eliminated by vomeronasal-organ removal (VNX) carried out prior to mating. VNX did not disturb maternal behavior on L2-L8 or maternal aggression on L1 or L5. These results and others suggest that the expression of maternal aggression is affected by volatile odors, mediated possibly by accessory chemosensory systems such as the septal organ, or by neural changes that follow olfactory deafferentation, or both.

Aggression↗
PubMed1977

The effect of stimuli emitted by sucklings on tactile contact of the bitches with sucklings and on number of licking acts.

Bitches changed abruptly their maternal behavior on 15th and 16th day of the maternal cycle, following an exchange - on the beginning of 15th day - of some puppies from their own litter for other 2-3 days old puppies. The total time of tactile contact with puppies on days 15 and 16 greatly increased as compared with the 13th and 14th day, i.e., the days immediately preceding the exchange of puppies. The number of licking acts also increased. In control bitches, whose puppies were not exchanged, the indices of maternal behavior showed no increase on days 15 and 16, compared with days 13 and 14 of the maternal cycle. The foster 2-3 days old puppies were also a source of much stronger stimuli releasing care-giving reactions than the own, correspondingly older puppies.

Age Factors↗
PubMed1994

Maternal teaching behaviors and temperament in preschool children.

This research investigated the relationship between young children's temperament and maternal teaching techniques in 20 mother-child dyads. Children's temperament was assessed by mothers' reports on the Behavioral Style Questionnaire. Teaching behaviors, as assessed with the Maternal Teaching Observation Technique, were inquiry, directive, negative verbal feedback, modeling, visual cue, physical affection, positive physical control, and negative physical control. Correlations were -.55 to -.60 for activity with mothers' use of verbal cues, children's adaptability and mothers' positive and negative verbal feedback, and children's distractability and mothers' modeling. The need for further research on parent-child interactions is noted.

Attention↗
PubMed2000

Mouthbrooding in the black-chinned tilapia, Sarotherodon melanotheron (Pisces: Cichlidae): the presence of eggs reduces androgen and estradiol levels during paternal and maternal parental behavior.

The black-chinned tilapia (Sarotherodon melanotheron) is considered a paternal mouthbrooder in which the male churns the eggs in his mouth for 14-18 days after they are fertilized. We previously showed that plasma androgen and estradiol concentrations increased significantly between the beginning and end of mouthbrooding. Here we provide evidence that androgen and estradiol are relatively high in prespawning male tilapia, decrease significantly with the initiation of mouthbrooding, and return to and slightly surpass prespawning levels by the end of mouthbrooding. We then test the hypothesis that the initiation of mouthbrooding causes a decrease in androgen and estradiol. We raised single pairs of tilapia in seawater aquaria and conducted two experiments. In the first, we removed eggs from males on the morning of Day 1 of mouthbrooding, followed changes in plasma androgen and estradiol in the afternoon of Day 1 and on Days 6, 11, and 16, and compared them to levels in control males who kept their eggs. Removing eggs from mouthbrooding males on the morning of Day 1 eliminated the decrease in plasma androgen and estradiol observed in the afternoon of Day 1 of mouthbrooding. This demonstrates that the eggs are necessary for the decrease. We observed that, infrequently, the female of the pair would pick up the eggs to brood them in her mouth. In a second experiment, in the afternoon of Day 1, we sampled both the male and female of pairs in which the female brooded eggs. In female-brooding pairs, the females had significantly lower androgen and estradiol levels than prespawning females. The black-chinned tilapia in captivity exhibits both paternal and maternal parental behavior. In both sexes the initiation of mouthbrooding triggers a decrease in androgen and estradiol concentrations. We conclude that the presence of eggs inhibits the pituitary-gonadal axis in both males and females and hypothesize that a chemical signal from the eggs is delaying the initiation of the next brood.

Androgens↗
PubMed2000

The effect of pregnancy intention on child development.

In this paper, we use data from the National Longitudinal Survey of Youth to investigate the empirical link between unintended pregnancy and child health and development. An important contribution of our study is the use of information on siblings to control for unmeasured factors that may confound estimates of the effect of pregnancy intentions on infant and child outcomes. Results from our study indicate that unwanted pregnancy is associated with prenatal and postpartum maternal behaviors that adversely affect infant and child health, but that unwanted pregnancy has little association with birth weight and child cognitive outcomes. Estimates of the association between unwanted pregnancy and maternal behaviors were greatly reduced after controls for unmeasured family background were included in the model. Our results also indicate that there are no significant differences in maternal behaviors or child outcomes between mistimed and wanted pregnancies.

Adolescent↗
PubMedDate not supplied

Prenatal exposure of rats to diphenhydramine: effects on physical development, open field, and gonadal hormone levels in adults.

Diphenhydramine (DPH), a classical H1 receptor antagonist, has been used in pregnancy for the treatment of allergies, nausea, and vomiting. It has been reported that 10-20% of pregnant women take antihistamine-containing preparations at some point during pregnancy. The present study analyzed the influence of prenatal exposure to DPH of rats on: 1) maternal behavior and milk production of dams; 2) physical and reflexologic development of offspring; and 3) long-term effects on open field behaviors and gonadal hormone levels in offspring. Female pregnant rats were injected s.c., daily, with 20 mg/kg DPH or saline from embryonic day (E) 0 to 21. After delivery, maternal behavior was assessed and offspring physical and reflexologic development was examined. Open field activity of male and female rats was measured at 21 and 75 days of age and plasma hormone levels were evaluated in both sexes at 120 days of age. Neither maternal behavior nor milk production was affected by DPH treatment. Treated offspring showed an accelerated pinna unfolding, eye opening, and a delay of testes descent and vaginal opening. Both righting reflex and negative geotaxis development were accelerated, but prenatal exposure to DPH did not modify offspring locomotor activity. When tested as adults, a lack of sexual dimorphism in the open field activity of males and females was observed. No differences were observed between gonadal hormone levels of control and experimental groups of either sex. The findings suggest that prenatal DPH exposure influences physical and reflex development of rat pups.

Animals↗
PubMed1990

Effects of dysphoria on maternal exchange dispositions.

Defining dysphoria as subclinical depression, we explored the extent to which maternal dysphoria influences the quality of relationships within the family and evaluated whether the effect of dysphoria on family relationships is selective or general and whether dysphoric effects on maternal behavior are similar or different when ratings of maternal behaviors are made by mothers versus observers. We expected that dysphoria would have general rather than selective effects on family relations rated by mothers and observers. In a sample of 40 American families at risk of child abuse or neglect, we found that maternal dysphoria did have significantly negative effects on mother-to-child and mother-to-parenting-partner relations, suggesting that maternal dysphoria has general rather than selective effects.

Child Abuse↗
PubMed1992

Nature/nurture and the nature of nurture in the etiology of hypertension.

Four reviews on the the role of developmental factors in hypertension are introduced and set in historical context. Recent research in the laboratory rat has shown that the preweaning environment makes an important contribution to the level of blood-pressure reached in adult life in genetic models of hypertension. Both of the most commonly used models of hypertension, the SHR and SS/Jr rat strains, exhibit lower BP in adult life, if they are fostered shortly after birth to mothers from their normotensive control strains. It has been suggested that it is the idiosyncratic maternal behavior of the hypertensive mothers which contributes to the elevated BP of their offspring, and it has been amply demonstrated that there is an association between a constellation of behaviors emitted by rat mothers and the adult BP of their offspring in a wide variety of genetic groups (inbred hypertensive animals, F1's and F2's). In addition to the above, maternal environment has been demonstrated to have a significant impact on the pathophysiological response of hypertensive animals to a high salt diet. Being raised by an SHR mother, versus an SS/Jr mother, increases the magnitude of BP increases to a high salt diet, susceptibility to hemorrhagic stroke, body weight loss and the risk of mortality. A variety of physiological systems are undergoing rapid change during the preweaning period and may mediate the effects of differences in the maternal environment. These include the renin-angiotensin system and the peripheral sympathetic nervous system. Nutritional factors may be involved in all of the phenomena referred to above. Thus, any physiological mechanisms that are proposed to link maternal behavior to its effects on the physiology of adult animals should recognize the involvement of nutritional factors. Research on the role of developmental factors such as maternal behavior in genetic models of hypertension is at the interface of two growing disciplines: behavior genetics and developmental psychobiology. The methodological and conceptual contributions of these fields to advancing our understanding of these phenomena is emphasized.

Animals↗
PubMed1977

[Relationship between (perceived) maternal rearing behavior and personality characteristics of behaviorally disturbed children and juveniles].

A survey of the literature on methodological problems associated with, and results of, the diagnosis of parental educational attitudes and practices as viewed and experienced especially by those receiving education is followed by a report on an investigation of the maternal educational behavior perceived by behaviorally disturbed children and juveniles of male sex. Correlative results obtained from the evaluation of questionnaires confirm the interrelation of disturbed (maternal) emotional relations to children and abnormal behavior shown by children. The inclusion in the diagnostic practice of reports given by those receiving education on the educational behavior shown by parents or other persons in whom the right of education is vested is considered to be a necessary and useful supplementary method.

Adolescent↗