Decline of maternal behavior in the virgin and lactating rat.

Sensitized virgins and postpartum lactating mothers, both exhibiting maternal behavior, were given donor litters that increased in age by 1 day, for 28 days, starting at the onset of maternal behavior. Each day females were tested for maternal behavior with pups 4-8 days old: Maternal care (i.e., nursing/crouching, retrieving, nest building and licking) and maternal withdrawal, rejection, and prevention of nursing were recorded. After the ninth day, females were also tested with the progressively older pups from 10 to 28 days of age with which they were living. Virgins and lactating mothers showed generally similar patterns of maternal care although some differences were found, and they declined in maternal behavior toward the older pups in a similar manner. Maternal behavior did not decline in tests with younger pups. The results are interpreted as supporting the hypothesis that the decline as well as the maintenance of maternal behavior postpartum is nonhormonally mediated.     

Perioral somatosensory determinants of nursing behavior in Norway rats (Rattus norvegicus)

Prior to assuming the upright crouching posture over their pups during nursing bouts, lactating rats typically engage in several oral behaviors, including nuzzling, licking and rearranging pups. By acutely depriving dams of various aspects of perioral stimulation from pups (with anesthesia of the mystacial pads or of the tongue, with mouth suturing, or with muzzling), we found the following: (1) Distal stimulation from pups maintains proximity-seeking behavior, but is insufficient to stimulate nursing behavior. (2) Lack of tongue feedback decreases pup licking and hastens the onset of crouching. (3) Snout, but not tongue, contact with pups is required for hovering over them. (4) The position of the dam while hovering over her litter enables the pups to gain access to her ventrum, thereby provoking her upright, crouching posture. (5) Older pups are capable of bypassing the dam's perioral attentions and stimulating crouching directly by burrowing under the dam's ventrum.     

Ontogeny of cholinergic mediation of behaviors in the rat.

In a series of six experiments, cholinergic mediation of behavior was studied in immature rats. It was found that although scopolamine disrupted discriminative choice behavior in both 15- and 23-day-old rat pups, it increased latency to choice in 15-day-olds and decreased latency to choice in 23-day-olds. This disruption of discriminated choice behavior was not due to differential shock thresholds or differences in locomotor activity between drug-treated and control animals, nor was it specific to a T-maze shock-escape discrimination task. These results suggest that central cholinergic mediation of different behaviors may mature at different rates.     

Maternal behavior of mice with cingulate cortical, amygdala, or septal lesions.

Nest building, pup retrieving, and pup survival and growth were evaluated in primiparous control mice and those with cingulate cortical, neocortical, amygdala, or septal lesions. Mice with neocortical or amygdala lesions showed little or no deficits in maternal behavior. Mice with septal lesions were severely impaired in all aspects of maternal care. These mice did not build nests, showed a variety of aberrant behaviors during pup retrieving, and their pups died or gained significantly less weight than those of controls. Mice with cingulate cortical lesions retrieved pups more slowly than controls, and retrieving deficits were correlated with the extent of retrograde degeneration found in the anterior thalamic nuclei.     

Sex differences in maternal behaviors of immature rats: The role of emotionality

Immature rats are able to give maternal care to pups and may increase their inclusive fitness by helping newborn siblings. Immature males are generally reported to be more maternal than females. In this research we studied sex differences and the extent to which they may be due to a different emotional response to novelty. We studied maternal response in two groups of immature rats of both sexes: in the naive group, juveniles aged from 18 to 30 days were given one test and showed clear-cut sex differences. The experience group was submitted to repeated tests from 18 to 30 days of age, thus eliminating the effects of novelty: as a result, all differences between sexes disappeared. A second experiment was designed in 24-day-old females to differentiate the effects of repeated handling and exposure to the test situation from that of repeated exposure to pups; moreover, the effects of an anxiety-reducing drug (diazepam) were studied. Exposure to pups is particularly efficient in facilitating maternal response. Diazepam injection was also effective, but its control showed that the injection per se was responsible for the effect. In conclusion, our results stress the importance of response to novelty and suggest that sex differences in maternal behavior of immature rats may be modulated by different emotional responses by males and females. In fact, emotionality competes with, and may exert an inhibitory effect on, the expression of a vast array of behaviors. © 1994 Wiley-Liss, Inc.     

"Resource" exchange in the biparental California mouse (Peromyscus californicus): water transfer from pups to parents

Mammalian mothers provide water to their young via milk. Rodent mothers reclaim much of this water by licking the anogenital areas of their pups, stimulating reflexive urination, and consuming the pups' urine. Male rodents do not provide milk (hence water) to the young, but in some species male parents may nevertheless lick their pups. We determined the amount of water transfer from pups to mothers and fathers in the biparental California mouse, Peromyscus californicus, by injecting 5-, 10-, 20-, and 30-day-old pups with tritiated water and measuring the radioactive label in maternal and paternal plasma after 24 hr of interaction with their litter. On Days 5 and 10 mothers obtained more pup urine than did fathers. Parents consumed equivalent amounts of pup urine on Days 20 and 30. Mothers engaged in more pup anogenital licking than did fathers, which accounted for the difference in pup urine consumption. Salt appetite controls in part, pup anogenital licking in lactating rats (Gubernick & Alberts, 1983). Salt appetite was not implicated in the modulation of anogenital licking in the California mouse because the mice failed to display a salt appetite. Licking of young and urine consumption are not dependent solely on the bidirectional exchange of water between the dam and her offspring.     

Effects of serotonergic and cholinergic antagonists on suckling behavior of neonatal, infant, and weanling rat pups

In Experiment 1, Sprague-Dawley rat pups at postnatal days 3-4, 7-8, 10-11, 15-16, and 23-24 were tested for suckling behavior on their anesthesized multiparous dams following administration of metergoline or scopolamine. The serotonergic antagonist, metergoline, inhibited suckling in 3- to 4- and 7- to 8-day-old rat pups, but was not found to influence suckling in older pups. Scopolamine, a cholinergic antagonist, reduced suckling primarily in 3- to 4-day-old pups. In Experiment 2, parity of the maternal female was manipulated to assess whether this variable would influence suckling behavior and the effects of metergoline on suckling of weanlings. Baseline levels of suckling were reduced in 23- to 24-day-old pups of primiparous dams when compared with multiparous-derived offspring. Administration of metergoline increased the amount of time that these primiparous-derived pups spent attached to nipples, but did not influence suckling of offspring of multiparous dams, perhaps as a result of a ceiling effect on suckling behavior in these animals.     

Effects of daily and acute restraint stress during lactation on maternal aggression and behavior in mice

A decreased reactivity to stressors during lactation might heighten the expression of maternal care (including defense of offspring) by minimizing the extent to which stress can impact maternal care. Although stressors applied during pregnancy have variable effects on maternal aggression (or defense of offspring), to date no study has examined the effects of stress applied during the postpartum period on maternal aggression. In this study, we examined the effects of both daily and acute restraint stress (30 min) applied postpartum on maternal aggression and other maternal behaviors. Daily restraint (ending 2 h before testing) did not alter any measure of maternal behavior, including nursing, licking and grooming of pups and pup retrieval, or any measure of maternal aggression. In contrast, acute stress significantly impaired total time aggressive and number of attacks, but pup retrieval was normal. c-Fos levels were significantly elevated in a number of brain regions in association with acute stress, including lateral septum (LS), caudal periaqueductal gray and medial amygdala (MeA), suggesting possible sites where stress reactivity could alter aggression. Together, the results indicate that acute restraint stress impairs maternal aggression and provide a starting point for future studies examining how stress reactivity pathways may intersect with maternal aggression pathways.     

Maternal behavior of spontaneously hypertensive and Wistar-Kyoto normotensive rats: effects of reciprocal cross-fostering of litters

Maternal behavior of spontaneously hypertensive (SHR) and Wistar-Kyoto (WKY) normotensive dams rearing either their natural pups or pups of the opposite strain was assessed when pups were 4-6 days of age. Consistent with previous reports, SHR dams caring for their natural pups were observed nursing and licking their pups more often than WKY dams and were away from their pups less often. The behavior of dams rearing cross-fostered pups demonstrated that this strain difference in patterns of maternal behavior is dependent on pup type. Mothers of both strains shifted their behavior in the direction of the opposite strain's maternal behavior pattern when caring for cross-fostered pups. This shift was most pronounced in SHR dams caring for WKY pups. These data suggest that alterations in patterns of maternal behavior produced by cross-fostering may play an important role in cross-fostering effects on the physiological development of SHRs previously reported.     

Maternal behavior of rats is affected by hormonal condition of pups

Previous research has found that maternal rats discriminate male from female offspring and provide more anogenital licking to males. Two experiments were performed to determine whether this discrimination is based on hormonal condition of young. It was found that 500 micrograms of testosterone, estradiol, or dihydrotestosterone injected on the day of birth into female pups led to their receiving an equivalent amount of maternal anogenital licking as males and significantly more than either oil or untreated females. The different steroids had similar effects. Maternal nonanogenital licking was not affected by sex or hormonal condition of pups, but it was significantly increased by injection per se. Effects on maternal behavior of hormonal condition or neonatal injection of young were apparent 1 and 9 days after injection.     

Adrenocortical activity during conditions of brief social separation in preweaning rats

Rat pups (18 days of age) placed into a novel test cage for 30 min exhibited greater concentrations of plasma corticosterone if alone than if with the biological mother regardless of whether she was conscious or anesthetized. Pups tested with a conscious nonlactating female had higher corticosterone levels than did pups tested with their own conscious mother. Anesthetizing the adult stimulus females eliminated this differential effect. Further, pups isolated in the home cage for 30 min exhibited corticosterone elevations as great as those of pups placed into a novel environment. However, pups left in the home cage with the mother for 30 min displayed corticosterone elevations similar to those of pups isolated in the home cage. In contrast, if pups were left in the home cage with both the mother and the littermates corticosteroid levels were reduced. These results indicate that, under certain conditions, brief separation from the mother can elevate plasma corticosterone levels in the 18-day-old rat. The differential effect of the biological mother and the nonlactating female appears attributable to differences in the behavior of the adult females. Finally, brief isolation from all littermates was also found to evoke a plasma corticosterone response.     

Maternal aggression in mice: The non-specific nature of the exteroceptive maintenance by young

Five hours of pup removal during early lactation (Postpartum Day 6) reduced maternal aggression in mice, while placement of the dam's entire litter (six pups) or a single pup behind a double wire mesh partition in the homecage maintained aggression at a level identical to that of mothers in direct contact with their young. When placed behind the partition, unfamiliar 6, 13, and 20-day-old pups, but not 30-day-old mice, maintained the behavior as effectively as the dam's own young. The relationship of the findings to communal rearing conditions in the mouse is discussed.     

Litter gender composition affects maternal behavior of the primiparous mouse dam (Mus musculus)

Thirty-nine litters of the outbred Swiss CD-1 mouse strain were reduced at birth to 6 pups, according to three conditions: MM (all males), MF (3 males and 3 females), or FF (all females). The maternal behavior of their respective dams (frequency and duration of nursing, licking, nest-building, and other activities such as eating, drinking, sniffing, grooming, and undirected locomotor activity) were scored during a single 10-min session on Days 2, 3, 5, 7, 10, 14, and 18. Dams rearing MM litters showed higher scores of maternal care on Days 2 and 18 in the case of nursing, on Days 2, 7, and 10 in the case of nest-building, and on Day 18 in the case of licking. These results confirm previous rat data, which indicated that male and female pups are exposed early in infancy to a different pattern of maternal behavior. Concomitant measurements of pup development (body-weight gain and achievement of a number of physiological and neurobehavioral landmarks) indicated that these effects of litter gender composition are not mediated by gross changes in the maturational trends of the pups.     

Oxytocin links mothering received,mothering bestowed and adult stress responses

We review recent discoveries that implicate oxytocin in the intergenerational transmission of similar levels of maternal behavior and acute stress responses in female rats. First, ICV-infused oxytocin antagonist decreased the display by nursing dams of pup-licking (PL) and arched-back nursing (ABN), but not other components of maternal behavior, and increased maternal self-grooming suggesting that oxytocin may shift the balance of oral grooming by dams away from themselves and toward pups. Second, oxytocin receptor concentrations in areas of the adult brain where oxytocin stimulates maternal behavior or diminishes anxiety and adrenal axis responses to acute stress were positively related to PL-ABN received during infancy. Third, oxytocin and oxytocin antagonist treatments of pups on postnatal days 2-10, respectively increased and decreased PL by the treated rats when adult and themselves nursing dams. This indicates that oxytocin activity in female pups, which may be regulated by PL-ABN received from their mothers, influences their adult levels of PL. These three lines of evidence suggest that oxytocin selectively enhances PL-ABN by rat dams, which then increases oxytocin activity in female pups and, thereby, facilitates their expression of central oxytocin receptors (and perhaps other aspects of central oxytocin systems) and, consequently, their adult PL-ABN frequencies and acute stress responses.     

Response of male and female Siberian hamsters towards pups

The influence of sex, reproductive maturity, and parental experience on the behavior of Siberian hamsters (Phodopus sungorus sungorus) toward strange pups was examined in this study. Immature, mature, or parentally experienced male and female Siberian hamsters were presented with 3- to 8-day-old pups. We recorded pup carrying during the initial 10 min, nesting with pups after 8 or 14 h, and attacking pups during the test period. Among inexperienced animals, more mature males attacked pups than did immature males or mature females. Parental experience significantly decreased pup attacks by males and increased nesting with pups by both males and females. Repeated testing did not modify the responses to pups. We conclude that in Siberian hamsters both caretaking and aggressive responses to pups may be shown by immature and mature animals of both sexes. Parental experience resulted in increased caretaking by males and females and decreased aggressive responses by males.     

Perioral anesthesia disrupts maternal behavior during early lactation in Long-Evans rats

The role of perioral somatosensory stimulation from pups in maternal behavior was investigated in lactating Long-Evans rats (Rattus norvegicus) during early lactation by local anesthesia of the mystacial pads with lidocaine, which blocks conduction in the infraorbital nerve. It was concluded that (1) acute perioral anesthesia markedly inhibited pup retrieval when the subjects had no formal pretreatment retrieval experience. Further, these dams displayed little tolerance to the lidocaine treatment when they were tested repeatedly. (2) The severity of the effects of perioral anesthesia on retrieval was dependent upon prior experience and the testing situation. Following pretreatment retrieval experience, and in a test cage with dark and light compartments which provided a strong incentive to retrieve, 80% of lidocaine-injected dams did retrieve. However, retrieval efficiency was impaired by perioral anesthesia, largely due to increased time in contact with pups prior to each retrieval and to increased carrying time. (3) Perioral anesthesia also inhibited pup licking, but not self-grooming, suggesting that the former, but not the latter, is largely under peripheral stimulus control and that deficits in maternal oral activities cannot be due to impairment of mouth opening and use. (4) The onset of nursing behavior was delayed until after the recovery of snout sensations and retrieval. This suggests that a maternal behavior not directly involving the mouth is nonetheless dependent upon the dam's receipt of perioral tactile input from pups.     

Effect of postweaning social experience on response of Siberian hamsters (Phodopus sungorus sungorus) toward young

Between 18 and 50 days of age, Siberian hamsters were housed either with same-sex littermates, opposite-sex littermates, opposite-sex littermates and parents, or opposite-sex littermates, parents, and a younger litter. When adults, these animals were presented with two 3-8-day-old pups for 8 hr, and their responses were recorded. Rearing conditions did not affect behavior of females. Males housed with female littermates in the absence of a younger litter showed fewer pup attacks and more nesting with pups than did males housed only with other males. Thus, housing with females in the early postweaning period may influence males' later (adult) responses toward pups. Only among hamsters housed with same-sex littermates did males and females differ in their response to pups, a result emphasizing that sex differences in behavior may depend on early social rearing.     

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

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

Mother rats interact differently with male and female offspring.

Lactating Long-Evans rats were observed to interact differently with male and female pups during the first 18 days postpartum. Differences in the mother's behavior were related to the gender composition of her litter (GHL), to the sex of a single introduced pup, and to the sex of individual pups within her litter. Major differences were the greater time spent in licking the anogenital region of own male pups and the greater stimulation of anogenital licking by male foster pups, an effect that did not interact with GHL or age of pup. The GHL interacted with day of testing to affect nest building and time spent near pups.     

啮齿动物主动母性行为动态改变的神经机制

主动母性行为是雌性哺乳动物在哺乳期内有效照料幼崽的一种动机行为, 对幼崽的生存和行为发展有重要影响。证据显示, 啮齿动物的主动母性行为会经历从产后早期的发动和维持到晚期衰退的动态改变, 反映了雌鼠对幼崽奖赏价值阶段性变化的适应; 这一过程不仅涉及分娩激素事件开启下丘脑内侧视前区(MPOA)-中脑腹侧被盖(VTA)-伏隔核(NA)-腹侧苍白球(VP)通路, 还需要杏仁核基底外侧核(BLA)和内侧前额皮层(MPFC)等脑区对上述通路进行实时调节。哺乳期主动母性行为动态改变及其神经机制的研究, 可以加深对行为进化和早期发展的认识, 也对人类母亲产后抑郁等临床问题的干预有借鉴意义。本文首先利用条件化位置偏好(CPP)任务的行为学证据分析幼崽奖赏价值与主动母性行为动态改变的关系; 然后系统阐述调控这一动态改变的神经机制; 最后对未来需要研究的一些重要问题或方向进行探讨。