Paternal behavior in the spiny mouse (Acomys cahirinus)

The responsiveness of adult male spiny mice (Acomys cahirinus) to both their own and alien precocial young was investigated. Paternal behavior was manifested primarily by the males huddling with their offspring and the coordination of pup attendance between adult males and females. With less than 2 days exposure to their own neonates, males were found to discriminate between their own and alien young. Experience plays an important role in the development of paternal behavior in spiny mice. Males who have never had pups of their own sniff and attack unfamiliar neonates more than males who have fathered pups. The adaptive significance of paternal investment in this uniquely precocial murid rodent was discussed.     

Rank order in pairs of communally nursing female mice (Mus musculus domesticus) and Maternal Aggression Towards Conspecific Intruders of Differing Sex

This study examined social behavior between pairs of unfamiliar lactating females, with litters of the same age, at different periods after parturition (3, 7, and 17 days). Tests were generally followed by the formation of communal rearing nests, and subsequent maternal attack on intruders of differing sex was assessed. In all three intervals lactating females showed ritualized attack with formation of clear dominance-subordination relationships before combining litters into communal nests. The dominant females in 90% of cases started to retrieve alien pups into their nests. Agonistic behavior and communal nest formation were most rapid when pups were around 3 days old. Maternal attack on conspecific intruders was mainly displayed by the dominant lactating females. Male and female intruders were equally attacked (in terms of frequency and intensity of attack), but there was less such aggression when pups were around 17 days of age. Nevertheless the topography of biting attack employed against female and male conspecific intruders was different. Females were attacked using a strategy avoiding bites to the head and ventral surface (indicative of “offensive” behavior) whereas males were severely bitten on vulnerable body regions (indicative of “defensive” behavior).     

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.     

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.     

Social influences on parental and nonparental responses toward pups in virgin female prairie voles (Microtus ochrogaster)

Pair-bonded prairie voles (Microtus ochrogaster) are biparental after the birth of pups. However, whereas most adult virgin males are parental, most virgin females are not. In 6 experiments, influences on the parental behavior of virgin female prairie voles were examined. It was found that (a) young virgin females were more maternal than older females, (b) the postweaning sex ratio of cage-mates did not affect females' responses to pups, (c) females raised to adulthood with their parents and younger siblings present were highly parental, (d) 48-hr exposure to pups beginning at weaning increased some aspects of later maternal responding, (e) rearing to adulthood with the parents even in the absence of younger siblings also increased females' maternal responding, and (f) the increase was seen only if both parents were present. Continued parental presence promotes alloparental behavior, possibly important if daughters do not disperse from the natal nest.     

Hysterectomy-induced maternal behavior during pregnancy in the rat.

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

Vasopressin, maternal behavior, and pup well-being

The brain peptide, vasopressin (VP), was studied with respect to its effects on maternal care in rearing natural and cross-fostered pups. Long-Evans (LE) rats synthesize hypothalamic VP; whereas, Brattleboro (DI) rats do not produce this peptide. Long-Evans dams exhibited superior maternal care when compared with DI dams when rearing their own as well as foster pups. This enhanced behavior was evidenced by the higher survival rate of pups reared by LE mothers compared to those reared by DI mothers. Later, when the offspring were subjected to the stress of 23 hours of food restriction each day, LE animals reared by their natural mothers survived for a significantly longer period of time and developed significantly less stomach pathology than DI animals reared by their natural mothers or LE foster mothers. The results demonstrated that the secondary factor of maternal care in the absence of VP was of little consequence in the characteristic difficulties observed in DI offspring.     

Vasopressin,maternal behavior,and pup well-being

The brain peptide, vasopressin (VP), was studied with respect to its effects on maternal care in rearing natural and cross-fostered pups. Long-Evans (LE) rats synthesize hypothalamic VP; whereas, Brattleboro (DI) rats do not produce this peptide. Long-Evans dams exhibited superior maternal care when compared with DI dams when rearing their own as well as foster pups. This enhanced behavior was evidenced by the higher survival rate of pups reared by LE mothers compared to those reared by DI mothers. Later, when the offspring were subjected to the stress of 23 hours of food restriction each day, LE animals reared by their natural mothers survived for a significantly longer period of time and developed significantly less stomach pathology than DI animals reared by their natural mothers or LE foster mothers. The results demonstrated that the secondary factor of maternal care in the absence of VP was of little consequence in the characteristic difficulties observed in DI offspring.     

Prepartum changes in maternal responsiveness and nest defense in Rattus norvegicus

Changes in maternal responsiveness during late pregnancy were traced by exposing females to foster pups (15-30-min tests) under conditions favoring the rapid initiation of maternal behavior. Groups were tested when nonpregnant or on Days 17, 20, 21, or 22 of pregnancy (Day 22 = parturition). Nulliparous females were compared with primiparous and with "experienced breeders." Nest defense was observed by introducing unfamiliar males (2-min tests) on Day 22. Results focused attention on three periods: (a) Days 17-20, when maternal responsiveness was lower than in the nonpregnant condition, (b) Day 21, when maternal responsiveness returned to or rose above nonpregnant levels, and (c) on Day 22, the 3.5 hr prior to delivery, during which 90% of females almost immediately retrieved, gathered, and tended foster pups and during which 92% attacked the unfamiliar intruders. (Attacks were rare earlier.) Maternally experienced females were more responsive to pups than nulliparous females when nonpregnant and throughout late pregnancy, but both groups were equally likely to show prepartum aggression.     

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。     

Can but don’t: olfactory discrimination between own and alien offspring in the domestic cat

Mammalian maternal care usually comes at a large energetic cost. To maximize their fitness, mothers should preferentially care for their own offspring. However, the majority of studies of mother–offspring recognition have focused on herd- or colony-living species and there is little information on maternal discrimination in more solitary-living species. Olfaction has been found to play a major role in mother–offspring recognition across various taxa. Therefore, our aim was to study this in a species evolved from a solitary-living ancestor, the domestic cat. We asked whether cat mothers distinguish between their own and alien offspring when providing maternal care, and whether cat mothers use olfactory cues in the offspring discrimination process. Results of Experiment 1 showed that cat mothers do not discriminate between own and alien young when retrieving them to the nest. They treated own and alien young similarly with respect to latency and order of retrieval. However, the results of Experiments 2 and 3, where we used an olfactory habituation-discrimination technique, showed that mothers were able to distinguish between the odours of their own and alien kittens. We discuss what ecological and/or behavioural factors might influence a mother’s decision when faced with discriminating between own and alien young, and why mothers might not discriminate between them when they are able to do so. Our findings support the view that maternal care alone should not be used as a measure of offspring recognition, and equal maternal care of own and alien young should not be immediately interpreted as an inability to discriminate between them.     

Recognition of maternal environment in piglets: effects of age and some discrete complex stimuli

Ethological evidence suggests that 1-week-old piglets can distinguish between their own mother or home environment and alien ones. The bases for this discrimination were investigated in two series of experiments employing a T-maze. In the first series, the apparatus was placed between two pens each housing a sow and its piglets, with each of the two goal-arms having a wire mesh end protruding into one of the pens. When piglets from each of these pens (as well as controls from other litters) were run individually in the apparatus, piglets of all ages from 1 to 14 days showed preferential responses towards their home environment. In the second series of experiments, various discrete but complex natural stimuli were placed at the end of the goal-arms: in each case, the stimuli in the two goal-arms were indentical in nature except in their derivation from the maternal pen or an alien one. One-week-old piglets showed a significant preference for their own mother (vs. another sow visible and audible through wire mesh), for wood shavings mixed with sow faeces from their own pen (on the floor of the goal-arm), and for air blown over maternal faeces and shavings. But they showed no evidence of distinguishing between a littermate and another piglet (penned at the other side of the wire mesh terminating a goal-arm).     

A possible function of the preference for hind nipples in prairie voles (Microtus ochrogaster)

Prairie vole pups (Microtus ochrogaster) in laboratory cages prefer hind nipples. In this research, the author observed 8 litters of prairie voles in a seminatural environment to confirm the preference for hind nipples and to determine if young on hind nipples were groomed more frequently or dislodged less frequently than were young on other nipples. Prairie vole pups in seminatural environments preferred hind nipples; this preference was illustrated by the progressive use of more anterior nipples only as litter size increased and by the reluctance of pups to voluntarily release their hold on hind nipples. Maternal grooming of young did not vary with suckling location. Prairie vole young on hind nipples, however, were dislodged less frequently than were young on other nipples. Less frequent dislodgment from hind nipples during maternal movements may play a role in the preference for hind nipples in prairie voles.     

Effects of transections to the vomeronasal nerves or to the main olfactory bulbs on the initiation and long-term retention of maternal behavior in primiparous rats.

While the onset of maternal behavior at parturition is mediated by hormones, the maintenance of maternal behavior during the first few postpartum weeks depends on experiences acquired while the dam interacts with pups (Rosenblatt, 1990). In fact, if female rats are permitted as little as 2 h or maternal experience within 36 h after Cesarean delivery, they exhibit heightened maternal behavior during maternal induction tests 10 days later; in contrast, dams separated from young at the time of Cesarean delivery and not permitted a maternal experience fail to respond maternally in tests 10 days later (Orpen & Fleming, 1987). In this study we investigated the role of chemosensory input through the vomeronasal and main olfactory systems in this maternal experience effect. Six groups of primiparous females were tested for maternal behavior to foster pups presented 9-10 days after Cesarean delivery: three groups were permitted to interact with pups for a 2-h period 36 h after Cesarean delivery; and three groups were separated from pups until testing and were given no maternal experience. Within each experience condition, one group sustained bilateral section of the vomeronasal nerves, one sustained bilateral coronal cuts through the midsection of the main olfactory bulbs, and one group sustained small medial olfactory bulb cuts. The results showed that animals sustaining vomeronasal or olfactory transections, regardless of experience condition, exhibited significantly reduced latencies to maternal behavior in maternal induction tests. However, these chemosensory disruptions did not prevent an additional facilitation of maternal behavior produced by a prior maternal experience.     

Enhanced feminine sexual behavior and infertility in female rats prenatally treated with an antiestrogen

An attempt to elucidate the possible role of prenatal estrogen on the development of feminine sexual behavior and reproductive function was made by treating females with the antiestrogen CI628 prenatally on days 13-19. Control females were prenatally treated with saline or remained untreated. The animals were delivered by caesarian section on day 22 of pregnancy and placed with foster mothers whose newborn pups had been previously removed. Intact peripubertal females in each treatment group were observed for several reproductive measures, including the capacity to become pregnant. Other females were ovariectomized in adulthood and treated with estradiol benzoate (EB) (1, 1.5, 2 or 4 micro g/rat) and 0.5 mg progesterone and tested for receptivity, proceptivity and sexual partner preference. Two weeks after the completion of these tests, the females were injected daily for 7 days with 0.25 mg testosterone and tested for sexual partner preference and mounting behavior. The results obtained showed accelerated vaginal opening, and infertility in the antiestrogen-treated intact females and enhanced receptivity and proceptivity in response to 1 micro g EB in the antiestrogen ovariectomized females. Sexual partner preference and mounting behavior did not differ between groups. These results suggest an involvement of prenatal estrogen on the development of female reproductive function, but not on behavioral differentiation.     

Maternal responsiveness to infant Norway rat (Rattus norvegicus) ultrasonic vocalizations during the maternal behavior cycle and after steroid and experiential induction regimens

When removed from the nest and placed in a cool environment, Norway rat (Rattus norvegicus) pups emit ultrasonic vocalizations that can elicit maternal search behavior. The authors examined the behavior of pregnant dams, mothers, and virgin females during exposure to a pup that was either warm and silent or cool and vocalizing. Results indicate potentiated maternal reactions to a vocalizing pup: Mothers approached and maintained proximal orientation to a vocalizing pup far more than did virgin females. Elevated levels of proximal orientation appeared within hours of birth, increased during the 1st week postpartum, and declined by the time of weaning. Estrogen plus progesterone administration facilitated virgin females' proximal orientation toward vocalizing pups, whereas prolonged exposure to pups in the absence of hormones was without effect, suggesting that the ontogeny of the maternal response is regulated, at least in part, by maternal hormones.     

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.     

Maternal aggression toward infanticidal males of different social status in wild house mice (Mus musculus domesticus)

Maternal aggression was examined in wild female mice (Mus musculus domesticus) derived from animals trapped in Alberta, Canada. Lactating females were tested for their behavior toward intruder males during the time of postpartum estrus while housed in a two-cage apparatus containing a defensible nest area. Prior to being used as intruders, sexually naive males were screened for their behavior toward a newborn pup (83% exhibited infanticide). Only infanticidal males were then housed in pairs and allowed to establish a dominance hierarchy. Dominance status was further verified by a urine marking test. The dominant and subordinate infanticidal males were then placed into a lactating female's cage and observed for 1 hr. The test was terminated immediately when a male began to attack the pups. Lactating females attacked the males in both groups, but subordinate males received more intense attacks than dominant males. Dominant males elicited significantly more fear/defense behavior than subordinate intruders. All of the dominant males and only one submissive male attacked the pups. Females were thus successful in blocking infanticide only by infanticidal subordinate males. Since females do not persist in attacking males with high fighting ability, one function of maternal aggression could be to assess the fighting, and resource holding, potential of a future mate. © 1994 Wiley-Liss, Inc.     

Differential Effects of Short- and Long-Term Early Maternal Separation on Subsequent Maternal Behavior in Rats

Female Sprague-Dawley pups were separated from mothers every other day for 8 hr (long-term separation/LTS), 4 hr (short-term separation/STS), or 0 hr (no separation/NS) from postnatal day 2–20. In adulthood, they were mated and tested for maternal behaviors during two lactations. It was expected that females separated from mothers as pups would show deficits in maternal behavior as adults. Contrary to expectations, LTS showed better nest building and grouped young faster during both lactations. LTS were first to display aggression and displayed more aggression during the second lactation. Notably, while some measures decreased from first to second lactation in NS and STS, LTS maintained levels of maternal care. These results suggest that extended periods of maternal separation may exaggerate some aspects of maternal behavior.     

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.