Prenatal stress eliminates differential maternal attention to male offspring in Norway rats

Maternal licking behavior was observed in 20 Long-Evans rat dams on two consecutive days. Stimulus pups were male and female foster pups from dams that were either housed with 5 adult males during the last trimester of pregnancy (stressed) or housed alone (unstressed). Unstressed male pups received significantly more maternal licking than their female siblings, but prenatally stressed males and females received similar levels of maternal licking, comparable to that directed to unstressed females. In a second study, urine collected from prenatally stressed male pups elicited significantly less investigation from dams in a choice test than urine from age-matched unstressed males. It is concluded that the chemosignals which stimulate dams normally to provide more maternal attention to male than female neonates are deficient in prenatally stressed males. The results raise the possibility that differential maternal care may mediate some effects of prenatal stress on behavioral development in males.     

Maternal licking by virgin and lactating rats: water transfer from pups

Rat dams provide water to their young via milk. Dams reclaim much of this water by licking the pups' anogenital areas, stimulating reflexive urination and consuming the pups' urine. Sensitized virgin rats, induced to act maternally do not provide water to pups, but they nevertheless lick them. To determine whether bidirectional transfer of water between the rat mother and her litter mediates maternal licking, water transfer from pups to sensitized virgins was compared with that to lactating dams. We used time-lapse video recordings to measure anogenital licking of pups. Sensitized virgins and lactating dams spent equivalent amounts of time licking the anogenital regions of test litters. We quantified the amount of water transferred from offspring to both virgins and dams by injecting pups with tritiated water and measuring the radioactive label in maternal plasma after interaction with a litter of 5-day-olds. Dams obtained more than twice as much urine from the litter in 4 hr than did the maternal virgins. Differences in the amount of water obtained from pups were due to differences in urine availability caused by the receipt of milk from the dams. When the dams' nipples were ligated, so that their pups received no milk, ligated dams and virgins consumed equivalent amounts of pup urine. Maternal licking and urine consumption are not dependent solely upon the bidirectional exchange of water between the dam and her offspring.     

Uterine positions and schedules of urination: correlates of differential maternal anogenital stimulation

Lactating Mongolian gerbils, like lactating Norway rats, reliably lick some pups in their litters more than they lick others. Male gerbil pups are licked more by their dams than are their sisters and some males and some females within each litter are licked more often than are their sibs of the same sex. In the present article, we explore the characteristics of same-sex littermates that are correlated with elicitation of extreme amounts of maternal anogenital licking. We found that both the male pup and the female pup in a litter of gerbils that received the most maternal anogenital licking: (1) released greater quantities of urine and (2) exhibited longer latencies to begin to urinate in response to artificial anogenital stimulation than did the male pup and the female pup in a litter that received the least amount of maternal anogenital licking. We also found that foster mothers rearing Caesarean-delivered litters spent more time licking the anogenital areas of: (1) those male pups that, as fetuses, had occupied uterine locations adjacent to relatively few females and (2) those female pups that, as fetuses, had occupied uterine locations adjacent to relatively many males. We discuss implications of these findings for understanding of how maternal behavior may mediate hormonal effects on the development of young gerbils.     

The effects of sensitization and social isolation on maternal behavior in the virgin rat

Thirty-three out of 67 virgin Sprague-Dawley rats spontaneously retrieved 5–10-day-old foster pups in a pretest. The 34 rats not responding immediately were randomly divided into three groups to study the effects of direct and exteroceptive exposure to young on the induction of maternal behavior. Retrieving, licking and crouching behavior appeared in a higher proportion of cage rats (n = 12) which received a fresh group of pups to live with throughout each day than in control rats (n = 10) that had only 5 min daily exposure. However basket rats (n = 12) also became maternal merely by exposure to exteroceptive stimuli from pups living in baskets fixed to the cage wall. In a second experiment, virgin rats that spontaneously retrieved pups were socially isolated for 2–4 weeks. As a result, a 50–60% decrease in the number of rats showing retrieval was found not only in an independent sample of rats (n = 20) but also in a related group (n = 13) that practiced the response in the week between a pretest and Week 2 in isolation. Therefore, the results demonstrate that exteroceptive cues from pups alone may be sufficient to induce maternal behavior in nonspontaneously retrieving virgin rats, and that isolation from pups and other social stimuli reduce retrieving behavior in initially responsive virgin rats.     

Pregnancy duration and fetal number: Effects on maternal behavior in rats

It was shown previously that in rats postpartum mothers are much more likely than pup sensitized virgin mothers to retrieve pups from a T-maze extension of their home cage. In the present experiment, the physiological basis of this difference was explored further by inducing maternal behavior (retrieving, crouching, licking) following hysterectomy-ovariectomy on Days 21, 16, and 10 of pregnancy. In general, the longer the duration of pregnancy, the shorter the latency to become maternal and the greater the propensity to retrieve pups from the T-maze. An additional group of Day 16 pregnancy terminated rats carrying six or fewer fetuses were not impaired with respect to onset of maternal behavior compared to their large-litter counterparts, but only a small percentage of these females retrieved in the T-maze. These findings suggest that both the late pregnancy estrogen surge and progesterone withdrawal after its peak and sustained secretion enhance maternal responsiveness and that T-maze pup retrieval (but not onset latency) may be additionally affected by the level of placental hormones.     

Maternal behavior in normal and androgenized female rats: effect of age and experience

The aim of the experiments presented here was to evaluate the influence of age and of previous maternal experience on care of pups in normal virgin and androgenized Wistar female rats. When sensitization occurred before they were 60 days old, androgenized females failed to develop consistent retrieving, probably because of excessive timidity (Experiments 1 and 2) whereas they were able to keep pups warm in their nests. During pup-toy choice tests (Experiment 2) young androgenized females displayed only erratic carrying of toys. On the other hand, 60-, 80- or 100-day-old androgenized females developed full maternal behavior like cyclic controls. In the third experiment, control and androgenized females exposed to pups when 60 days old, were reexposed when 95 days old. Androgenized females proved to be more sensitive to earlier exposure to pups than control females and showed significant reductions in latencies of emergence of maternal responses.     

Mother-infant interactions in two strains of rats: Implications for dissociating mechanism and function of a maternal pattern

Mother-infant interaction was observed in Long-Evans and Fischer 344 rats after fostering within or across strains. Interactions immediately following introduction of foster pups to the cage as well as undisturbed interactions with resident litters were examined. Some differences were related to alien status, some to strain of pups, and others to strain of dams. Greater responsiveness to pups of the maternal strain was exhibited in retrieval and body licking. Long-Evans pups received more crouching from dams of both strains 3-12 days postpartum, perhaps because they are significantly larger. Regardless of pup strain, Long-Evans dams engaged in more maternal licking than did F344 dams, and this was more likely directed to the anogenital region. Dams of both strains were more likely to lick male than female pups, regardless of pup strain. The strain difference in maternal licking is consistent with adult strain differences in water and salt appetite and may contribute developmentally to the superior copulatory performance of Long-Evans males. © 1997 John Wiley & Sons, Inc. Dev Psychobiol 30: 310–312, 1997     

Maternal contact inhibits pituitary-adrenal stress responses in preweanling rats

Three experiments examined psychological factors which inhibit pituitary-adrenal activity in 12-, 16-, and 20-day-old rats. Infant rats were placed in heated novel test arenas for 30 min--a treatment which increases corticosterone secretion--and were presented with different appetitive stimuli in order to determine whether these stimuli inhibit this increased hormone secretion. The first experiment was a factorial combination of two conditions: suckling an anesthetized dam and milk ingestion through an intraoral cannula. At all ages, suckling inhibited corticosterone secretion but milk ingestion did not, nor was there an interaction of these factors. In the second experiment, the importance of suckling was assessed by allowing pups' contact with an anesthetized dam either with or without the opportunity to suckle. At all ages, contact with suckling and contact alone were equally effective in inhibiting corticosterone secretion. The third experiment asked whether contact with a lactating female is necessary for pituitary-adrenal inhibition or whether more distal cues associated with lactation are sufficient. Pups were tested under one of four treatments formed by a 2(Lactating vs. Virgin Female) X 2(Contact vs. No Contact) factorial design. At all ages inhibition of corticosterone secretion occurred only in animals which were allowed contact with an anesthetized female. Lactating and virgin females were equally effective for the 12- and 16-day-old pups, but contact with a virgin female was less effective for the 20-day-old pups. These findings indicate that neuroendocrine mechanisms subserving inhibition of the pituitary-adrenal system exist during the preweanling period in the rat, and suggest the possibility of maternal regulation of this physiological system during development.     

Differences in maternal behavior of rats and the sociosexual development of the offspring

This paper describes experiments designed to investigate long-term behavioral consequences for offspring of changes in maternal behavior directed toward them as pups. Specifically, the hypothesis was considered that experimentally induced alterations in maternal behavior would result in general and wide-ranging effects on offspring development, including effects on later social and sexual behavior. The first experiment looked at the effects of changing pup odors on maternal responsiveness toward the pups, and showed that the application of perfume, particularly to the anogenital region, resulted in significant lowering of maternal anogenital licking of pups. Non-pup-directed behavior did not differ between groups. The behavior of those pups that had thus differed in infant experience was then followed in three subsequent experiments. In Experiment 2, social behavior during the juvenile period was investigated, focusing particularly on the expression of social play. The most noticeable difference to emerge in this experiment was that male pups that had been anogenitally perfumed as infants showed much higher levels of social play than male or female pups from other treatment groups. The last two experiments considered adult behavior. Experiment 3 showed that there are no lasting effects of the neonatal treatment on the attractiveness an animal has for its conspecifics. In the final experiment, "masculine" sexual behavior of males (mounts with intromission), and "feminine" sexual behavior of females (i.e., lordosis and proceptive behavior) were investigated. This confirmed previous reports by Moore (1984) (Moore, C. L. (1984). Maternal contributions to the development of masculine sexual behavior in laboratory rats. Dev. Psychobiol., 17:347-363) that those male pups that had received lower rates of anogenital licking as pups showed longer intermount intervals, when tested as adults. The results are discussed in relation to the development of sexually differentiated behavior.     

Effects of consanguinity, exposure to pregnant females, and stimulation from young on male gerbils' responses to pups.

In three experiments investigating variables affecting responses of male Mongolian gerbils to conspecific young, we compared the behavior directed towards pups of natural fathers, virgin foster fathers, and sexually experienced foster fathers (Experiment 1); males either previously exposed or not exposed to pregnant females (Experiment 2); and males provided or not provided with extra opportunities to huddle over pups (Experiment 3). We found no difference in responses to pups among natural fathers, virgin foster fathers, and foster fathers that had fathered litters. On the other hand, both a week of exposure to a pregnant female and opportunity to huddle over pups for an extra 15 min/day had significant effects on males' subsequent responses to conspecific young. We speculate on the reasons why a male's response to pups might be affected by his exposure to a pregnant female and stimuli from pups, but not by the probability that the pups were his own offspring.     

Sensory regulation of maternal behavior in rats: Effects of pup age

Maternal behavior (retrieving, crouching, and licking) was induced in Sprague-Dawley virgin female rats by constant exposure to pups aged 1-2, 3-4, 5-6, 7-8, 9-10, 11-12, 13-14, or 15-16 days. The incidence of spontaneous components of maternal behavior, notably retrieving, was geater towards pups 1-8 days of age than towards older pups, whereas the occurrence of cannibalism did not differ as a function of pup age. With pups 1-2 through 13-14 days, the latency to onset of full maternal behavior was shortest with 1-2-day-old pups (2-day median) and longest with 13-14-day-old pups (7-day median). Females exposed to pups aged 3-4 through 11-12 days did not differ significantly in their latencies, the medians of which ranged from 4.0 to 5.5 days. Only 1 female out of 8 exposed to pups aged 15-16 days became fully maternal, but 5 more displayed components of maternal responsiveness. The optimal nature of neonates and the general attractiveness of a wider range of pup ages as stimuli for the elicitation of maternal behavior in rats, as well as comparisons to mice and hamsters, were discussed.     

Morphine treatment and reproductive condition alter olfactory preferences for pup and adult male odors in female rats

Administration of morphine sulfate (MS) to pregnancy-terminated and postpartum lactating female rats disrupts both maternal behavior and postpartum aggression. Since the display of these behaviors may be heavily dependent on olfactory cues provided by the stimulus animals (rat pups and adult male rats, respectively), we examined whether MS was affecting the perception of the olfactory stimuli, and whether olfactory perception was modified by reproductive condition. In Experiment 1, lactating rats had their pups removed and were injected with MS (5.0 mg/kg, sc.) or saline. 60 min later they were placed into a two-choice apparatus, one side of which contained bedding soiled by neonates and the other clean bedding. Time spent on each side was recorded for a total of 5 min (300 s; chance = 150 s). Saline-treated mothers spent significantly more time on the pup-odor side, whereas MS-treated females spent significantly less. In Experiment 2, lactating females were treated with MS or saline and exposed to male odors (soiled bedding). MS significantly increased time spent on the side with male odors; when treated with saline, time spent was significantly reduced. Thus, in lactating rats. MS creates an aversion for pup odors while reducing the female's normal aversion toward male odors. In Experiment 3, ovariectomized (ovx) virgin females expressed neither an aversion nor a preference for the odor of pups following saline administration. After MS treatment, however, the virgins showed a distinct preference for pup odors. When exposed to male odors in Experiment 4 ovx virgins showed a marked preference for male odors after MS treatment, and neither a preference nor an aversion after saline. Experiment 5 examined pup odor preferences in intact virgins, early (Day 7), middle (Day 14), late-pregnant (Day 21), and prepartum (Day 22) rats. The pup odor preferences of virgin, Day 7, Day 14, and Day 21 pregnant rats were not different and generally were at chance levels. Day 22 pregnant females exhibited a marked preference for pup odors compared to chance levels, as well as compared to the other four groups. These findings suggest that opiates and endogenous opioids may regulate olfactory preferences and that alterations in this system may underlie normal behavioral changes toward conspecifics prepartum as well as during lactation.     

Trigeminal lesions and maternal behavior in Norway rats: III. Experience with pups facilitates recovery

In lactating rats, upper snout desensitization by trigeminal denervation severely impairs maternal behavior, with substantial recovery 12–24 hr later. The potential effects of interaction with pups on this recovery was investigated. Dams were subjected to bilateral infraorbital denervation or sham surgery on Day 5 postpartum and observed for 30 min with 6 foster pups 24 hr later, after separation from pups for 4 or 24 hr. Long separation reduced likelihood of retrieval and nursing behavior, infraorbital denervation reduced duration of pup licking, and these deprivations combined greatly increased latencies of pup sniffing and durations of facial self-grooming. Both conditions, and especially their combination, prolonged retrieval duration, the retrieval sequence being interrupted by other pup contact, such as licking. Thus, interaction with pups and adequate trigeminal stimulation maintain normal maternal behavior. These findings are possibly relevant to the normal decline of maternal responsiveness during late lactation and to other lesion-induced deficits. © 1997 John Wiley & Sons, Inc. Dev Psychobiol 30: 115–126, 1997     

2-Mercaptoacetate does not stimulate chow intake in periweanling rats

In adult rats, administration of drugs that suppress oxidation of fatty acids, like mercaptoacetate (MA), produces increases in food intake. During development, the consequences of administration of MA are more varied. For example, in very young pups, intake of milk diets is unaffected by MA, while pups aged 12 to 15 days demonstrate increases in intake. However, in 18- and 21-day-old rats, milk intake is suppressed by administration of MA. Typically, the paradigms used to test rat pups differ significantly from those used to assess intake in adult rats. The present experiments were designed to examine whether 18-day-old pups tested with adultlike paradigms showed adultlike responses to administration of MA. In the first experiment, rat pups aged 18 days were injected with 0 or 68.4 mg/kg MA, then given 60-min tests while consuming either milk or chow diets that were novel, or to which they had previously been exposed. The results demonstrated that chow intake was not affected by administration of MA, but milk intake in experienced animals was suppressed by MA. Experiment 2 demonstrated that in contrast to administration of MA, 18-day-old pups deprived of food overnight showed increases in intake of chow and milk diets. In Experiment 3, when the effects of a range of doses of MA (22.8, 45.6, 68.4 and 91.2) on chow intake over a 4-h period were assessed, all doses of MA produced a significant suppression of chow intake in 18-day-old pups. Taken together, the data suggest that alterations in fatty acid oxidation produced by administration of MA do not stimulate chow intake in periweanling pups tested in an adultlike fashion.     

Long-term effects of prenatal morphine exposure on maternal behaviors differ from the effects of direct chronic morphine treatment

Previous studies have demonstrated that chronic morphine treatment of pregnant rats alters maternal behavior. Other studies have shown long-term effects of prenatal exposure to morphine, including changes in reproductive behavior in adult females. The present study investigated the effects of prenatal morphine exposure on a variety of maternal behaviors such as nursing, maternal activities, nonmaternal activities, and pup retrieval. Prenatal morphine exposure increased active and decreased passive nursing. There were no differences in maternal activities such as presence in the nest, contact with pups, grooming of pups, and/or manipulation of nest shavings. In the retrieval test, prenatally morphine-exposed mothers were faster in carrying the first pup, retrieving the first pup back to the nest, and returning all pups to the nest than prenatally saline-exposed mothers. Maternal and nonmaternal activities also were affected by the light: dark cycle. All saline- and morphine-exposed mothers nursed more, were more often in the nest, and more often in contact with greater than half of their litter during the light than the dark sessions. On the other hand, nonmaternal activities increased during the dark sessions: Mothers cared for themselves (groomed, ate) more and displayed more rearing and sniffing. Mothers spent more time resting with their eyes closed during the light sessions regardless of prenatal drug exposure. The present study demonstrated that the effect of morphine on maternal behavior is different in adult exposed and prenatally exposed mothers. While direct morphine treatment impaired maternal behaviors, prenatal morphine exposure has the opposite effect.     

Olfactory cues and accessory olfactory bulb lesion: effects on sexual behavior in the cyclic female rat

The influence of olfactory cues and accessory olfactory bulb (AOB) lesion on female sexual behavior was studied in virgin female Wistar rats. In Experiment 1, it appeared that distance or contact exposure to male urine soiled bedding for 8 hours before testing increased sexual receptivity, i.e., the number of receptive females at 18:00-19:00 on proestrus. In Experiment 2, we observed that sexual receptivity at 18:00-19:00 on proestrus was not affected by AOB lesion as compared to sham-operated females. In Experiment 3 the effects of both AOB lesion and olfactory cues were analyzed. Sexual receptivity at 18:00-19:00 on proestrus did not significantly differ in sham-operated and accessory olfactory bulbectomized females both exposed to the odor of male urine. Regarding lordosis quotient in the three experiments, no significant difference was observed. Mechanisms whereby olfactory cues and/or AOB lesion modified female sexual behavior on proestrus in virgin female rats were discussed in the light of previous and present observations.     

Inhibition of infant glucocorticoid stress response: specific role of maternal cues

Previous work from this laboratory has shown that passive contact with an anesthetized lactating dam eliminates the corticosteroid stress response to novelty in 12-, 16-, and 20-day-old rat pups. In the present study, we further examined some of the sensory and developmental aspects of this phenomenon. In two experiments, we asked whether inhibition of the corticosteroid stress response is related exclusively to contact with a maternal stimulus as opposed to other social stimuli. Experiment I compared the effectiveness of contact with an anesthetized dam vs, an anesthetized adult male rat. At 12 and 16 days of age, contact with an adult male was somewhat effective in reducing stress responsiveness, whereas at 20 days, contact with an adult male was entirely ineffective. At all ages, contact with an anesthetized dam was an effective inhibitor of the stress response. Experiment II compared the relative effectiveness of contact with an anesthetized dam vs. an anesthetized sibling pup. At all ages, contact with a dam was very effective, whereas contact with an anesthetized pup was entirely ineffective in inhibiting the glucocorticoid stress response. In Experiment III, the effect of maternal contact was assessed during a period of development when the biological, and presumably social, significance of the lactating-dam stimulus is changing. In this study, 20-, 24-, and 28-day-old rat pups revealed a progressive decrement in the ability of maternal contact to inhibit stress responsiveness. These findings replicate and extend our previous ones by showing that maternal stimuli play a special role in the modulation of pituitary-adrenal activity during development.     

Comparison of the parental behavior of pair-bonded female and male prairie voles (Microtus ochrogaster)

The behavior of primiparous lactating prairie voles (Microtus ochrogaster) and their mates individually interacting with pups was continuously assessed for 45 min after a 2-h parent-litter separation on days 3-4 and 10-11 postpartum. Both sexes were highly parental after reunion with the young, and their general pattern of behavior consisted of bouts of quiescence interspersed with bursts of heightened activity. Lactating females spent more time than males in contact with pups, and more time being quiescent, most often in the kyphotic (upright crouched) nursing posture. Even in the absence of nipples upon which the pups could suckle, males also displayed kyphosis, although for shorter durations than females. Males spent more time, however, huddled over the litter in a hunched position than their mates. In accordance with their decreased quiescence, male voles licked and carried pups more and were more exploratory than females. Compared with the first week postpartum, bouts of kyphosis were shorter during the second week postpartum for both sexes, while laying prone on the pups increased. Males spent less time licking and more time carrying older pups than younger ones, and were more exploratory during the second week postpartum. Sex differences in the parental behavior of prairie voles may reflect differences in the somatosensory stimulation that females and males receive from pups. Furthermore, the display of kyphosis by male voles indicates that the sensorimotor organization of this posture in voles differs from that of lactating rats, which require suckling stimulation for its regulation.     

Nursing behavior in rats is impaired in a small nestbox and with hyperthermic pups

The supine nursing posture, which occurs increasingly as growing pups initiate nursing from their recumbent dam, was demonstrated to require more space than that provided in earlier studies of mother-young contact (e.g., Leon, Croskerry, & Smith, 1978). Further, hyperthermic rat pups were shown to be deficient in eliciting normal nursing behavior. During a 4-hr separation from their dam, 7-day-old rat pups were incubated at 34°C (nest temperature) or at 39°C (WARM). Compared to controls, WARM-litter dams showed increased licking of and hovering over pups and decreased upright crouching, while WARM litters showed decreased nipple attachment and weight gain. On Day 13, similar effects occurred after incubation at 39°C (vs. 34°C), but not at 36 or 38°C. The results stress the need for ethologically meaningful conditions and direct behavioral observations to reveal the importance of pup activity in the mother-young dyad. © 1996 John Wiley & Sons, Inc.     

Behavior of mother rats in conflict tests sensitive to antianxiety agents

Previous studies of freezing and open-field activity have demonstrated that lactating rats are less fearful or less anxious than nonpregnant ones. The purpose of this investigation was to observe the behavior of mother rats in conflict tests, which are frequently used in studies on the neurobiology of anxiety. In the punished drinking test, in which licking from a water spout is punished by electric shocks, mothers (observed on Day 1 postpartum following 24 hr of water deprivation) were found to drink more than virgins. Mothers (Day 1 postpartum) also consumed more food than controls in an unfamiliar open field. In contrast, no difference between mothers (Day 5 postpartum) and virgins was present in the exploration of an electrified shock probe. The largest maternal anticonflict effects in the drinking and feeding tests were recorded when the females were tested with their pups. Increased punished drinking was also observed in virgin rats treated with the anxiolytic benzodiazepine midazolam. Water-deprived virgins and mothers did not differ in the shock titration test, a result suggesting that diminished pain reactivity was unlikely to account for the increased punished drinking in mothers. Moreover, females in late pregnancy, which are hypoalgesic (Gintzler, 1980), did not lick more than virgins in the punished drinking test. Following 24 hr of water deprivation, unpunished drinking was higher in lactating females than in virgins, so the increased acceptance of punishment by mothers might have been due to their being more thirsty than virgins.(ABSTRACT TRUNCATED AT 250 WORDS)