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.     

Incidence of pup killing and parental behavior in virgin female and male rats (Rattus norvegicus): differences between Wistar and Sprague-Dawley stocks

The responses toward young shown by males and nulliparous females differed substantially between two outbred stocks of laboratory rats. Sprague-Dawley females showed maternal behavior either spontaneously (35% of the naive rats) or through concaveation (92% of the initially neutral virgins). Of the Wistar females, however, only 10% showed maternal behavior spontaneously, and only 29% of the neutral virgins came to behave maternally during 15 days of concaveation. Prepubertal cohabitation with lactating rats did not facilitate maternal responsiveness in adulthood in the Wistar virgin females. Of the Sprague-Dawley males, 50% showed paternal behavior spontaneously, and only 4% killed the young. Among the Wistar males, however, only 4% showed paternal behavior spontaneously, and 76% killed pups. Such profound differences between outbred stocks of rats may be a source of discrepancies between the results of studies dealing with the induction of parental behavior in nonlactating rats.     

Responses of virgin mice, and of maternal females, to normal and caesarian-section delivered pups.

Pups were presented to adult mice of the Porton strain. Significantly more mothers and virgin females retrieved pups to the nest than did virgin males. More virgin females than males licked pups, built nests and assumed lactation posture. Differences were significant even if males that attacked pups were excluded from consideration. Latencies to first appearance of maternal activities were higher than reported by most other workers. Possible genetic strain differences in the response of virgin mice to pups are discussed. In Experiment 2 pups delivered by caesarian section with placentas attached were used. More mothers than either virgin males or females cleaned and accepted pups, indicating that pup cleaning may be controlled by factors different from those influencing other maternal activities.     

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.     

The effects of cross-fostering on the development of social preferences in meadow voles (Microtus pennsylvanicus)

To determine the role of the parental environment in the formation of species attachments in the meadow vole (Microtus pennsylvanicus), young of this species were fostered to either meadow vole parents (in-fostered young) or to prairie vole parents (M. ochrogaster; cross-fostered young). At 50 to 60 days of age, subjects were tested for social preference in an environment that simulated the conditions of a runway system. The testing design assessed the reaction of fostered animals to a novel species (M. pinetorum) as well as to the parental and biological species. The proportion of total test time spent near stimulus animals did not vary as a function of rearing condition. However, when compared to in-fostered controls, cross-fostered meadow voles displayed increased preference for prairie voles. Novelty did not appear to be a significant factor in test animal choice. These results suggest that in meadow voles, preference for the species of social partner is dependent on postnatal experience with parents.     

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.     

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.     

Differences in affiliative behavior, pair bonding, and vaginal cytology in two species of vole (Microtus ochrogaster and M. montanus)

Prairie voles (Microtus ochrogaster) and montane voles (M. montanus) display marked differences in social organization in the field. Trios of 1 male and 2 females were studied in a large enclosure for a 10-day period. Prairie voles spent 59% of the observation time in side-by-side contact, whereas montane voles spent only 7% of the time in contact. Vaginal smears indicated female-female suppression of estrus in prairie voles; female montane voles appeared to cycle in the presence of males. Male prairie voles preferentially paired and nested with 1 of the females, and vaginal estrus generally followed pair formation by 2 days. Male montane voles did not spend time preferentially with either female, even after mating. These results suggest that the contrasting mating systems of these species result from differences in the propensity for affiliative behavior and social bonding rather than from mate availability or female receptivity.     

Estrus induction in four species of voles (Microtus).

Male-induced estrus was examined in montane (Microtus montanus), meadow (M. pennsylvanicus), prairie (M. ochrogaster), and pine (M. pinetorum) voles. Duration of male contact needed for receptivity, effects of parity, and vaginal cytology were assessed. Among nulliparous females, montane voles attained receptivity with less male contact than prairie voles. Meadow and pine voles showed very low receptivity rates. Among parous females, montane and meadow voles did not differ in duration of male contact needed for receptivity and required less than prairie voles. Overall, parous females had higher receptivity rates than nulliparous females. When isolated from males, prairie and pine voles had more leukocytes and fewer cornified cells in vaginal smears than montane or meadow voles. Species differences in estrus induction are discussed in relation to species differences in social organization.     

Role of female aggression in prevention of infanticidal behavior in male common voles,Microtus arvalis (Pallas, 1779)

Infanticidal behavior of male common voles (Microtus arvalis) was investigated in relation to the age of unfamiliar pups. Sires from 18 pairs were removed after parturition of their offspring and replaced by unfamiliar males at different ages of the neonates. In group 1, containing six females with their offspring, the new male was introduced into the females' cages on day 1 after the parturition. In group 2 the new male was introduced on day 5 after parturition and in group 3 on day 9 after parturition. The male was removed after 3 days and the neonates recounted. Male common voles killed up to 100% of the neonates in litters containing neonates younger than 9 days by rapid bites to the head of the neonates (groups 1 and 2, mortality rates of 0.86 and 0.38). However, with older pups, a mortality rate of 0.06 was observed while 33% of the intruder males showed signs of injuries (group 3). These findings show that infanticidal behavior of male common voles represents one factor of pup mortality. The results are discussed in relation to changes in the degree of maternal aggression and in the context of the social system of the common vole for solving the conflict between postpartum estrous mating and infanticidal behavior of male common voles. Aggr. Behav. 23:293–298, 1997. © 1997 Wiley-Liss, Inc.     

Stimulus control of maternal responsiveness to Norway rat (Rattus norvegicus) pup ultrasonic vocalizations

Mother rats (Rattus norvegicus; 6 to 8 days postpartum) approach and maintain proximal orientation to a pup that is emitting ultrasonic vocalizations (USVs) far more than do virgin females (W. J. Farrell & J. R. Alberts, 2002). We used a playback regimen to examine the roles of acoustic and nonacoustic cues in regulating maternal proximal orientation toward vocalizing pups. When presented with recorded USVs, mothers of 6- to 8-day-old pups and nulliparous virgin females exhibited equivalent levels of proximal orientation toward the playback speaker. Mothers did show enhanced proximal orientation toward recorded USVs, however, if a silent pup was positioned below the speaker. Pup odors appear to be crucial for the maternal response to vocalizing pups, as peripherally induced anosmia attenuated maternal proximal orientation toward a vocalizing pup. Furthermore, spatial contiguity between olfactory and auditory stimuli was required for a maximal maternal response.     

Short-term early exposure to pups alters infanticide in adulthood in male but not in female wild house mice (Mus domesticus)

Male and female wild house mice (Mus domesticus) were allowed to remain in the cage of their parents until 30-35 days of age. When a second litter was delivered, the first litter was exposed to the younger pups for 2-10 days. In adulthood the male and female mice that had been exposed to pups as juveniles and an additional group that had cohabitated with their parents for the same length of time but were not exposed to pups were tested for infanticidal behavior. The frequency of infanticide by the adult female mice was not significantly different (55% vs. 70%, respectively). In contrast, the adult males that were exposed to pups as juveniles were significantly less likely to kill young in adulthood when compared with males that were not similarly exposed (35% vs. 80%, respectively). These data further demonstrate the strong influence of experience on the expression of infanticide by male mice and its relative unimportance to the expression of female infanticide.     

The biparental care system of the California mouse, Peromyscus californicus

Most knowledge of parent-offspring relations in mammals is derived from studies of mother-infant interactions. Male parental care has been less well studied. We explored maternal and paternal behavior of the California mouse, Peromyscus californicus. Six pairs of parents and their young were videotaped continuously for 12 hours/day, on alternate days from Days 1 to 31 postpartum. Males exhibit all parental activities and to the same extent as displayed by mothers, except lactation. Male parental behavior begins on the day of birth. Mothers and fathers spend substantial and equivalent amounts of time in the nest and in physical contact with pups throughout lactation. Males devote more time than females to licking pups, although females engage in more pup anogenital licking. Mothers nurse for at least 4 weeks, and fathers and mothers both build nests and carry young. The biparental care system of Peromyscus californicus affords an opportunity to develop a broader, more complete view of parent-offspring relations.     

Maternal behavior, paternal behavior, and pup survival in CD-1 albino mice (Mus musculus) in three different housing conditions

Parental behavior, food consumption, and pup development in litters of CD-1 albino mice (Mus musculus) with single mothers or paired mothers in 3 different housing conditions were compared. Fewer pups survived when parents were required to run in a wheel to obtain food, and these pups had lower weights than pups in the wheel-noncontingent and no-wheel groups. The presence of the male facilitated pup survival in the wheel-contingent group but had no effect on pup growth. Mice in the wheel-contingent group ran more revolutions than those in the wheel-noncontingent group and spent less time in parental care. In the wheel-contingent group, males spent more time running and ate less food than females, suggesting that males may indirectly facilitate pup development by providing food for the mother. The results suggest that the presence of the male increases pup care and may facilitate maternal behavior under appropriate environmental conditions.     

Parental Control, Adolescent Delinquency, and Young Adult Criminal Behavior

Adolescence and young adulthood are periods of increased autonomy. Higher levels of autonomy could increase the opportunities for risky behavior such as delinquency. During these periods of transition, the role of parental control becomes less clear. Previous studies have demonstrated the association between parental control and adolescent delinquency, but few have extended examination of such association into young adulthood. The purpose of the study is to examine the association between parental control and delinquency and parental control in adolescence and young adult criminal behavior. We propose that, even though adolescents seek autonomy during this stage, lack of parental control is positively associated with delinquency and has continued influence in young adulthood. Using a national longitudinal dataset, we analyzed the relationship between parental control and delinquency. Findings from regression analyses indicated that lack of parental control had a positive association with delinquency both concurrently and longitudinally into young adulthood. When analyzing delinquency in young adulthood, females reported a lower level of delinquency and younger age was associated with more delinquent behavior. Unexpectedly, parents’ college education was positively associated with delinquency in young adulthood. The findings suggest that parental control is still influential through the period of adolescence and early parental control is still influential in young adulthood. Ways to practice parental control and implications of results are further discussed.     

Interfemale aggression in adult bank voles (Clethrionomys glareolus)

Agonistic interaction may play a large role in shaping the social structure and spatial distribution of rodents such as Clethrionomys glareolus. Aggressive and non-aggressive behaviors of adult bank vole females were investigated with a home cage test during 10 min sessions. The number of attacks was significantly higher in virgin females kept with intact adult males than in singly reared females or those exposed to male urine. Bulbectomy of the tested females completely inhibited the male stimulating effect. This indicates that males influence the behavior of females by activating their olfactory systems. Aggressive behavior in pregnant or lactating females, which is linked to maternal behavior, was also tested. Female bank voles between 11 and 17 days of pregnancy or lactating at 3–4 days or 9–10 days attacked their partners significantly more frequently than virgins did. Females that had direct contact with males, even if they were not fertilized, appeared to be more successful in same-sex competition. Aggr. Behav. 24:53–61, 1998. © 1998 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.     

Medial preoptic area and onset of maternal behavior in the rat.

The present series of experiments examined whether the medial preoptic area (MPOA) is involved in the onset of maternal behavior in the rat. Previously, the MPOA had been shown to be important in the maintenance of maternal behavior in the lactating rat. The first experiment investigated whether estradiol benzoate (EB) acts on the MPOA to facilitate the onset of maternal behavior in the 16-day pregnant, hysterectomized, and ovariectomized female rat. Such rats when given EB implants in the MPOA had significantly shorter latencies for the onset of maternal behavior than had females implanted with cholesterol in the MPOA or with EB in the ventromedial hypothalamus, in mammillary bodies, or under the skin. A second experiment showed that estrogen-induced prolactin release was not involved in this facilitation. A third experiment indicated that MPOA lesions disrupt the onset of maternal behavior that is induced by pup stimulation in virgin females. It was concluded that the MPOA is involved not only in the maintenance of maternal behavior but in the hormonally mediated onset of maternal behavior and the onset of maternal behavior induced in virgin females by pup stimulation.     

Targets and tactics of agonistic and precopulatory behavior in montane and prairie voles: Their relationship to juvenile play-fighting

Play-fighting by juvenile montane and prairie voles involves attack and defense of the head, neck and shoulders. Since during play animals typically borrow behavior patterns from other functional contexts, two adult behavioral contexts were compared to juvenile play-fighting. These were serious fighting and sexual encounters. During serious fighting in a resident-intruder paradigm, most bites are directed at the rump and lower flanks. During sexual encounters, especially in precopulatory behavior, the head, neck and shoulders are gently contacted. Therefore, play-fighting by juveniles would appear to involve attack and defense of areas of the body contacted in adult precopulatory behavior, not adult fighting. Furthermore, the species-specific differences in juvenile play-fighting were also found to be matched by species-specific differences in precopulatory behavior. In both playful and precopulatory encounters, montane voles contacted the head and used upright defensive behaviors more often than prairie voles. In contrast, prairie voles made mutual contact more often and were more likely to rotate to supine in defense of contact to the nape and head. These findings support our hypothesis that juvenile play-fighting in muroid rodents involves the precocial expression of precopulatory, not agonistic behavior.     

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.