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Maternal behavior in the rat: facilitation through gonadectomy.

Virgin rats were ovariectomized and tested for induction of maternal behavior by being housed with neonatal young. A postoperative interval of 8 weeks yielded an average latency for the onset of maternal behavior significantly lower than that for intact controls or for virgin females ovariectomized 4 weeks before testing. Replacement of estrogen in the group ovariectomized for 8 weeks or injection of the estrogen antagonist ethamoxytriphetol (MER-25) in the group ovariectomized for 4 weeks changed the average latencies accordingly. Parallel results were obtained for males that were castrated 4 or 8 weeks before testing. It is concluded (i) that maternal behavior is under gonadal control and that this control is normally inhibitory; and (ii) that only after long-term removal of the gonads, resulting presumably in the complete clearance of estrogen and testosterone, is the maternal mediating system finally released from steroid suppression.

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Patterns of maternal behavior in the spontaneously hypertensive rat.

Maternal behavior of spontaneously hypertensive (SHR) and Wistar-Kyoto (WKY) normotensive rats was assessed over the preweanling period (days 1-21). Ten litters of each strain were observed during the dark phase of the light:dark cycle using a scan sampling technique. Cages were observed periodically throughout the day and the momentary behavior of the dam was recorded on a checklist of 9 different behaviors. These behaviors included: nursing entire litter, nursing part of litter, contact with entire litter, contact with part of litter, pup carrying/retrieval, licking pups, sniffing pups, nest building, and away from litter. A second set of ten litters per strain was observed in the same manner during the light phase of the light:dark cycle thus providing around the clock data throughout the entire preweanling period. For purposes of data analysis, the 21-day preweanling period was divided into 7 3-day blocks. The mean relative frequency with which each behavior was observed from SHR and WKY mothers was determined for each block and for each phase of the light:dark cycle separately. SHR mothers were with their pups and nursing them more frequently than WKY mothers during the light phase of the circadian cycle. Complimentary to this finding, WKY mothers were observed away from their pups more frequently than SHR mothers during both light and dark phases. Finally, SHR mothers were observed to lick their pups more often than WKY mothers during both phases of the light:dark cycle. These findings were consistent across the entire preweanling period.(ABSTRACT TRUNCATED AT 250 WORDS)

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Effects of central norepinephrine depletion on the initiation and maintenance of maternal behavior in the rat.

The catecholaminergic neurotoxin, 6-hydroxydopamine (6-OHDA), was used to test the hypothesis that increased transmission across selected noradrenergic synapses is involved in the initiation of maternal behavior. Specifically, 6-OHDA was infused intraventricularly either two days before parturition or four days after parturition. Control animals were infused with the vehicle alone. Among prepartum animals, NE depletion of more than 30% of control levels interfered with the initiation of maternal behavior. Among lactating animals, similar degrees of NE depletion had no significant effect on the maintenance of maternal behavior. Thus, NE appears to be involved in the initiation of maternal behavior, but not in the maintenance of the behavior once that behavior is established.

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Postnatal undernutrition in rats: attempts to develop alternative methods to food deprive pups without maternal behavioral alteration.

Two methods were investigated as attempts to undernourish rat pups without the disturbances in maternal behavior that accompany the procedures used to date for this purpose. In the 1st method, a litter of 12 pups was raised by both a lactating mother and a "sensitized" female. The sensitized female was provided under the assumption that she could correct for the deficit in maternal care when 1 mother raises a large litter. The results showed that the pups raised by the 2 females were constantly removed by the females from each other's nests; the females engaged in constant fighting and showed altered maternal behavior. As a consequence the pups lost more weight than control underfed young. The 2nd method consisted of removing 6-8 nipples from virgin females which were mated 10 days later. After delivery these females raised litters of 6 pups. Their maternal behavior was equal to that of unoperated controls, and at weaning the pups had 20-50% less body weight. This method could be useful to study undernutrition effects on behavior, without confounding experimental variables.

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Induction of maternal behavior in adult female rats following chronic morphine exposure during puberty.

The peripubertal period in the female rat is the time when the stimulatory effects of opioids on prolactin (PRL) secretion develop. In the adult rat, the administration of chronic high-dose morphine has been shown to attenuate the ability of opiates to stimulate PRL secretion. One function of PRL in adult virgin rats is the induction of maternal behavior. The present study examined whether chronic high-dose morphine exposure during the peripubertal period alters PRL-mediated induction of maternal behavior in adult female rats. Two groups of juvenile female rats were administered increasing doses of morphine or vehicle (s.c.) from age 30 to 50 days. As adults, these females either remained intact, or were ovariectomized and treated with a PRL-dependent, steroid hormone regimen that stimulates a rapid onset of maternal behavior. All females were then exposed daily to rat foster pups to determine whether peripubertal morphine exposure affected their latencies to induce maternal behavior. Morphine treatment resulted in a delay in vaginal opening and a temporary reduction in the rate of weight gain; however, the rate of onset of maternal behavior was unaffected by peripubertal morphine treatment. Thus, chronic morphine exposure in the pubertal female did not impact the expression of pup-induced maternal care.

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Role of pups' ultrasonic calls in a particular maternal behavior in Wistar rat: pups' anogenital licking.

Stimuli from pups maintain maternal behavior in the postpartum period. Olfactory cues are strongly involved in a particular component of maternal behavior: anogenital licking (MAGL). In addition to the olfactive stimulus, ultrasonic calls from pups are critical in ensuring pup survival. Pups emit vocalizations in distress situations. In a first experiment, pups' calls are recorded around MAGL sequences. In 2 out of 3 cases these calls appear to induce MAGL behavior from the dam with preputialectomised pups as well as with intact pups, but preputialectomised pups alone call again at the end of MAGL sequences. In a second experiment, ultrasonic calls from pups emitted just before AGL sequences were recorded and played back to dams in a glass-dish selection test. Whatever the pups' treatment (preputialectomised or sham), dams showed the specific ingestive behavior towards filter paper impregnated with dodecyl propionate (DP) when auditory cues (pups' ultrasonic calls) and olfactory cues (DP) were combined. The coordination of pups' ultrasonic calls and anogenital odor in MAGL behavior is discussed, ultrasonic calls might be an inducing factor and DP the regulating factor.

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Maternal behavior in rats and the effects of neonatal progestins given to the pups.

This paper reports changes in maternal behavior of rats following progestin treatment of the neonates. There have been recent reports that hormonal treatment of pups can alter maternal behavior, particularly licking of pups, and that such effects might have implications for the later development of those pups. Accordingly, the major objective of the experiments described was to test the hypothesis that the effects of neonatal progestins on later behavioral development that we have previously described (Birke & Sadler, 1983; 1984) might in part be mediated by changes in maternal behavior. This was done by investigating the behavior of dams, including pup-directed behavior, following the hormone treatments that we have used previously. In the first experiment, medroxyprogesterone acetate (MPA), given via maternal milk, was found to increase rates of pup licking by dams. In the second experiment, anogenital licking was increased to litters containing pups that had received either MPA or progesterone by direct injection. No significant changes in licking following pup treatment with the antiserum to progesterone were observed, however. The results are discussed in relation to our previous work on progestin effects on later behavior, and in relation to the suggestion that hormonal effects on sexually dimorphic behaviors might, at least partly, be mediated through interactions with the mother during the neonatal period.

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Maternal behavior in the primiparous and multiparous golden hamster.

Changes in the normal behavior patterns seen during lactation in the female golden hamster have received relatively little attention in the past (Rowell 1961; Daly 1972). The purpose of this experiment was to characterize and compare maternal behavior in female hamsters during gestation and 24 days of lactation, with their first and second litters. Each was observed for 1/2 h daily, and her behavior recorded every 10 s. Maternal behavior decreased over time in the mothers during both first and second lactations, while "non-maternal" behavior increased. No differences were observed in these measures between the first and second lactation.

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Prolactin levels and maternal behavior induced by ultrasonic vocalizations of the rat pup.

The relationship among ultrasonic vocalization (USV), prolactin and maternal behavior was investigated in lactating rat mothers and their pups. The lactating mother had a cannula inserted into the external jugular vein, and was exposed to USVs emitted from a pup immediately. Changes of prolactin and maternal behavior were determined. Prolactin increased dramatically during exposure to USVs, when maternal search, retrieving and nest building behavior appeared significantly. These results suggested that the relationship among USV, prolactin and maternal behavior was included in communication between lactating mother and pup.

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Effects of pregnancy hormones on maternal responsiveness, responsiveness to estrogen stimulation of maternal behavior, and the lordosis response to estrogen stimulation.

The aim of the study was to determine whether there is an increase in responsiveness to estrogen stimulation of maternal behavior and lordosis responsiveness during pregnancy. Using separate groups of pregnancy-terminated females, we measured the initial maternal responsiveness of hysterectomized-ovariectomized (HO) females and their responsiveness to estrogen stimulation. Maternal behavior latencies were studied in females HO on the 8th, 10th, 13th, 16th, or 19th day of pregnancy (8HO-19HO) and in nonpregnant HO (NPHO) females. Groups were injected sc with estradiol benzoate (EB) in doses ranging from 0 to 200 microgram(s)/kg and tested for maternal behavior (retrieving, crouching, and licking pups). In addition, we investigated whether there is an increase during pregnancy (following HO) in lordosis responsiveness to estrogen stimulation. Lordosis behavior was studied in pregnant HO females (days 8, 16, and 22) and NPHO females given 0 to 200 microgram(s)/kg EB. There was an increase in maternal responsiveness in oil-treated HO females starting around midpregnancy. From early pregnancy on there was also an increase in maternal responsiveness to 20 microgram(s)/kg EB. In late pregnant females (16HO) there was a further increase with 50 microgram(s)/kg EB. There was no increase in lordosis responsiveness to EB stimulation during pregnancy; pregnant and nonpregnant HO females had the same EB threshold for stimulating lordosis behavior. The results of both studies were related to increases during the latter half of pregnancy in nuclear estrogen receptor concentrations in the MPOA, an area that mediates estrogen stimulation of maternal behavior, and the absence of such increases during pregnancy in the VMH, an area that mediates estrogen stimulation of lordosis behavior.

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Pup-induced maternal behavior in adult and juvenile rats exposed to alcohol prenatally.

The effects of prenatal alcohol exposure on pup-induced maternal behaviors were examined in virgin rats whose mothers consumed liquid diets containing either 35 or 0% ethanol-derived-calories (EDC) on days 6-20 of gestation. A pair-feeding procedure was utilized to control for reduced caloric intake and, in addition, an ad libitum lab chow group was included to control for possible liquid diet effects. The results from experiments 1 and 2 revealed a sexually differential effect on this behavior in adult virgins exposed to alcohol in utero. Adult 35% EDC females showed a variety of deficits in maternal behaviors relative to controls; however, males with similar prenatal treatment appeared unaffected. In experiment 3, both 35% EDC male and female juveniles displayed altered maternal behaviors relative to controls. These results demonstrate yet another behavior sensitive to prenatal alcohol exposure. Prenatal hormonal alterations occurring as a consequence of maternal alcohol consumption may be a mechanism by which this long term behavioral effect is observed. This hypothesis and the importance of future research in this relatively new area of fetal alcohol studies are discussed.

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Variability in "spontaneous" maternal behavior is associated with anxiety-like behavior and affiliation in naïve juvenile and adult female prairie voles (Microtus ochrogaster).

Juvenile female prairie voles (Microtus ochrogaster) are spontaneously maternal, while virgin adult females show significant variability in their response to first pup exposure, ranging from infanticidal to full maternal behavior. In the present study, we investigated whether differences in anxiety-like behavior and affiliation are associated with juvenile-adult and adult individual differences in the response to pups. Forty juvenile (19-20 days) and 42 adult (60-90 days) female prairie voles were exposed to pups for the first time and tested for maternal behavior, anxiety-like behavior (elevated plus maze, open field), and affiliation toward age-matched, same sex conspecifics. Juveniles displayed less anxiety-like behavior, were more affiliative to unfamiliar conspecifics, and interacted with pups more positively than adults. Adults that displayed maternal behavior spent less time immobile, made more crosses through the center of the open field arena, and were more affiliative than adults that attacked the pups. This suggests that lower locomotion or exploration in a novel environment and poor affiliative behavior are negatively associated with maternal responsiveness in female prairie voles.

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Demanding pups improve maternal behavioral impairments in sensitized and haloperidol-treated lactating female rats.

The impairments in the maternal behavior of ovariectomized sensitized females, relative to lactating dams, resemble those deficits found in lactating females after treatment with the D1/D2 DA receptor antagonist haloperidol, which interferes with maternal motivation. Therefore, it could be speculated that these behavioral deficits found in sensitized females and haloperidol-treated dams are due to a reduced motivation to interact with pups. In support of this hypothesis, we have found that both sensitized and haloperidol-treated lactating females exhibited remarkably similar impairments in the expression of all active maternal behaviors relative to lactating dams. Furthermore, these deficits were overridden when they were allowed to interact with 12h-isolated pups (demanding pups). Interestingly, lactating dams also improved their maternal behavior in the presence of demanding pups, and clearly chose demanding more than non-demanding pups in a preference paradigm. These data support the idea that the behavioral deficits of sensitized and haloperidol-treated lactating females are due to a reduced behavioral activation in response to the incentive cues from pups compared to lactating dams, and not because of a motor inability to express maternal behavior. These findings ultimately suggest that pups modulate the activity of DA system involved in the regulation of maternal behavior.

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Alterations in the maternal behavior of rats rearing hypothyroid and hyperthyroid offspring.

To determine whether maternal behavior could serve as a mediator for thyroid hormone effects on behavior, I assessed nesting, nursing, grooming, contact, and retrieval in mothers of hypothyroid, hyperthyroid, and control litters, as well as in mothers of litters receiving thyroxine replacement therapy. Females assigned to the hypothyroid and replacement therapy treatments were placed on a goitrogenic diet of .2% propylthiouracil from Day 15 of gestation to Day 22 postpartum. Hyperthyroid and replacement therapy pups were injected daily with thyroxine starting on the day of birth. The decline in nesting and nursing was delayed in hypothyroid litters whereas the decline in nesting was accelerated in hyperthyroid litters. Retrieval was not affected, but grooming of pups occurred less frequently in hypothyroid and replacement therapy litters. Maternal care received by hypothyroid pups was considered adequate. Maternal behavior may alleviate some of the effects of perinatal hypothyroidism,, but does not seem to be responsible for the more severe effects of hypothyroidism.

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Maternal behavior following rehabilitation of rats with intergenerational malnutrition. 1. Persistent changes in lactation-related behaviors.

Female rats rehabilitated for one or two generations on an adequate level of dietary protein following a history of intergenerational malnutrition were studied during the postnatal suckling period. No recovery occurred after two generations of dietary rehabilitation for most measures of maternal behavior including active nursing, passive nursing, pup-oriented behavior, time spent in the nest or time spent in contact with the young. In contrast, nest quality improved to normal levels after rehabilitation. In addition, growth of pups born to females rehabilitated for one generation was similar to growth of control pups, and in the case of mothers rehabilitated for two generations, growth of offspring exceeded that of the control pups. These results demonstrate variable sensitivity of different maternal behaviors to rehabilitation following a history of intergenerational malnutrition, with lack of normalization of a considerable number of maternal behaviors. Consequently, some of these abnormalities in maternal behavior may result in persistent abnormalities in the behavior of offspring over several generations.

Age Factors↗

Postpartum luteinizing hormone release and maternal behavior in the rat after late-gestational depletion of hypothalamic norepinephrine.

The effects of depletion of hypothalamic norepinephrine (NE) during late pregnancy on the postpartum ovulatory LH surge, the onset and maintenance of maternal behavior and lactation were examined in adult female rats. Bilateral transections of the ascending noradrenergic pathways (ANP) between days 14 and 17 of gestation resulted in a 70% depletion in hypothalamic NE content when assayed on day 6 postpartum. In spite of this depletion in hypothalamic NE content, a postpartum ovulatory surge of LH was observed in transected rats at 18:00 h on either the day of parturition or 1 day later. The magnitude of the LH surge in experimental animals at this time appeared equal to that of controls. A second group of transected and sham-transected rats was tested for maternal responsiveness postpartum and through day 6 postpartum. Primiparous transected females displayed normal maternal behavior during this period with only minor disruptions in nest-building behavior. The lactational performance of transected rats, however, was inferior to that of sham-transected animals. The hypothalamic content of NE in females that showed impairment of lactation was consistently below the NE content found in the controls. The importance of the noradrenergic system in the control of maternal behavior is discussed, and it is proposed that noradrenergic involvement in maternal behavior is modulatory rather than directly regulatory.

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Maternal behavior in rats: evidence for the involvement of preoptic projections to the ventral tegmental area.

This study provides evidence that a neural system extending from the preoptic region to the ventral tegmental area (VTA) of the midbrain is important for the normal expression of maternal behavior in lactating rats. In the first experiment, bilateral electrolytic lesions of the VTA severely disrupted the maternal behavior of postpartum rats. In the second experiment, lactating rats that received a unilateral knife cut severing the lateral connections of the medial preoptic area (MPOA) paired with a contralateral lesion of the VTA showed more severe maternal behavior deficits than females that received one of the following treatments: (a) a unilateral knife cut severing the lateral connections of the MPOA paired with an ipsilateral VTA lesion; (b) a unilateral knife cut severing the lateral connections of the MPOA paired with a contralateral lesion of the medial hypothalamus posterior to the MPOA; (c) a unilateral knife cut severing the lateral connections of the lateral preoptic area paired with a contralateral VTA lesion. The oral components of maternal behavior (retrieving and nest building) were particularly affected as a result of bilateral damage to the system extending from the preoptic area to the VTA.

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Hormonal interaction with stimulus and situational factors in the initiation of maternal behavior in nonpregnant rats.

Previous hormonal studies have identified the hormonal and stimulus factors mediating the initiation of maternal behavior but have failed to reduce hormone-induced latencies of nonpregnant females to less than 1-2 days of continuous pup exposure. For the purpose of testing whether this delay is due to an olfactory-vomeronasal-mediated aversive reaction to pups like that found in untreated virgins, estrogen-injected hysterectomized-ovariectomized (HO-EB) nonpregnant females were subjected to olfactory-vomeronasal deafferentation. Median latencies were reduced to 0 and 1.5 hr compared with 72 hr for HO-EB nondeafferented females, which indicates that normally after HO-EB treatment, tendencies to initially avoid pup contact remain strong. Next, the hypothesis was explored that experiences during late pregnancy and/or parturition interact with hormonal priming to modify pup avoidance. Nonpregnant HO-EB females that had been exposed to pregnant-parturient females for 2 wk were tested under conditions simulating parturition. A high percentage rapidly initiated maternal behavior, but conditions during testing proved more important than prior exposure to pregnancy/parturition. The contributions of three stimulus/situation factors were analyzed: pup age--newborn versus 3-8 day; method of pup presentation--four at once versus staggered introduction; and time of day--lights versus dark phase. Hormonally treated but not sham-treated females initiated maternal behavior most rapidly when first exposed to one newborn in the nest during the light phase (76% within 1.5 hr). Prepartum caesarean-delivered females, however, responded maternally to four 3-8-day-old pups outside the nest, which indicates that additional factors operate at parturition.

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