Exposure to pups influences the strength of maternal motivation in virgin female rats

Following repeated exposure to foster pups, virgin female rats acquire and eventually express a full spectrum of maternal caretaking behaviors directed toward pups. Though these behaviors are vigorous, these females are reportedly less motivated to seek out and interact with pups (i.e. maternally motivated) than parturient females during early postpartum. The present study systematically assesses how the length of pup-exposure and nature of interactions between the female-pup dyad affect maternal motivation in the virgin female rat. Virgin females were exposed to young pups consistently (24 h/day) across a prolonged period (21 days), briefly (1 h/day) across a relatively brief period (7 days), or distally (pups inaccessible in mesh bag). During final pup-exposure days, females were conditioned and tested for their preference for a pup-associated chamber (e.g. maternal motivation) using conditioned place preference. Early postpartum females provided a comparison group. Fully maternal behavior only emerged in females given prolonged pup-exposure; this behavior improved significantly over time and was maximally expressed for a duration equivalent to early postpartum. Females given brief pup-exposure expressed only emergent maternal behaviors initiated by pups; distal pup-exposure evoked pup-avoidance. Virgin females given prolonged or brief pup-exposure expressed substantial pup-associated chamber preference, with more females preferring the pup-associated chamber following longer pup-exposures in a subtle stepwise relationship. Maternal motivation was strikingly similar in prolonged pup-exposure virgin and early postpartum females. Females given distal pup-exposure completely lacked maternal motivation. Maternal behavior did not predict chamber preference. Results suggest that pup-exposure, regardless of length, is sufficient to support strong maternal motivation, whereas parity is not required.     

Coexpression of sexual behavior and maternal aggression: the ambivalence of sexually active mother rats toward male intruders

The sexually active female rat solicits the male to approach for copulation, while the maternal dam displays aggression to expel him from the nest, suggesting that both behaviors are mutually exclusive. However, the rat has a postpartum estrus during which she is sexual and maternally motivated. Can she perceive the male as attractive and aversive, soliciting and attacking him at the same time? This study shows that postpartum estrous females exhibit a merge of sexual and maternal aggressive responses toward male intruders in the home cage. The concurrent expression of these behaviors did not affect their intensities, although the stimulation of maternal behavior increased maternal aggression without modifying sexual solicitation. These results indicate that the postpartum estrous rat can optimally express two opposite and independently regulated motivations, and that the male can be perceived as an ambivalent stimulus.     

Experience-hormone interactions and maternal behavior in rats

Three studies were conducted to determine the effects of reproductive condition and hormonal background on the acquisition and retention of a prior maternal experience. In the first study five experience conditions were compared. All animals gave birth and received either no postpartum contact with pups or 1/2 hr, 1 hr, 2 hr or 24 hr of pup contact and were tested for maternal behavior 10 days later. Animals receiving pregnancy and parturitional experience, but minimal social experience with young, exhibited significantly longer maternal onset latencies than did groups receiving 2 or 24 hr of prior experience; also, comparisons of 10- and 30-day retention intervals indicated that animals tested 10 days after a 24-hr experience exhibited shorter latencies than those tested 30 days later. Thus, the duration of the postpartum experience and the interval since prior experience both affect the level of maternal responsiveness shown. In the second study six groups of females were tested. Four groups were permitted one day of interaction with pups either after parturition (primiparous animals) or following pup induction procedures (nulliparous animals) and were tested for their maternal responsiveness to foster pups 25-35 days later, either on day 19 of a subsequent pregnancy or following resumption of estrous cycling. For most measures of maternal behavior there were significant main experience and test effects; experienced and pregnant animals exhibited shorter latencies to retrieve, lick and crouch over pups than did inexperienced and cycling animals, respectively. Significant interactions were also found for genital licking latency as well as for retrieval and crouch frequencies.(ABSTRACT TRUNCATED AT 250 WORDS)     

Effects of hormonal, sexual, and social history on mating and pair bonding in prairie voles

The interactive effects of hormones, sexual history and cohabitation on sexual and social behaviors were examined in pairs of ovariectomized female and sexually experienced male prairie voles (Microtus ochrogaster). Monitoring with time lapse video tape revealed that females in estradiol benzoate (EB)-induced estrus, and their male partners engaged in high levels of sexual activity which continued intermittently for at least 3 days (until observations were arbitrarily terminated). In conjunction with other studies, these results indicate that the hormonal condition of the female at the time of testing is a major determinant of sexual activity. Prior hormonal, copulatory, or cohabitation experience did not significantly influence sexual responses between females and unfamiliar male partners. However, affiliative behaviors, such as side by side contact, were higher in pairs that were familiar due to prior sexual and cohabitational experience. These results indicate that social and sexual behaviors are independently regulated. Other behaviors, including nasogenital investigation and autogrooming were influenced by the hormonal and sexual history of the female. The implications of these behavioral patterns for reproductive activation, pair bonding, and incest avoidance are discussed.     

Reproductive success and mate choice in Long-Evans rats

In the present study, mating behavior was observed in female rats that were given the opportunity to mate with two male rats simultaneously. Eleven sexually na?ve, naturally cycling rats were assigned to one pair of sexually experienced cohabitating male rats. Each female rat was mated during proestrous with her assigned pair of males. Eight females successfully became pregnant and gave birth to healthy pups (approximately 9 pups/litter). After the offspring were weaned, paternity of each pup was determined using microsatellite DNA markers. Based on this analysis, it was determined that one male in each pair sired the majority of the pups in the litter. No male sexual behaviors or characteristics distinguished male rats that sired the majority of pups from those that sired few or none of the pups. Furthermore, neither female mate preference nor measures of paced mating behavior differed between male rats that had a reproductive advantage from those that did not. Finally, ejaculation order also failed to predict reproductive success of the male rats. Together, these results suggest that reproductive success of some male rats may not depend on specific mating behaviors, but rather their success may depend on physiological or genetic traits that make them unique.     

Stability and potential inheritance of infanticidal behavior in prairie voles

Naïve female prairie voles show significant variability in their behavioral response to newborns. We investigated whether that behavioral response (a) was related to the quality of postpartum maternal behavior; (b) was affected by postpartum maternal experience; and (c) could be selectively bred. The behavior of females was recorded in three conditions: as naïve in a nonreproductive context, as single lactating (no male present), and as experienced mother in a nonreproductive context. Finally, females and males with similar behavioral response to newborns were selectively bred for three generation. Males were removed before the offspring was born. Our results revealed that (a) naïve females that attacked pups, spent more time distant from them after parturition than those that were maternal or ignored the pups (p < .05); (b) postpartum maternal experience did not reverse infanticidal behavior; and (c) at the third generation of selective breeding, 90% of the offspring of females that were nonmaternal as virgins, behaved as their mothers. These findings suggest that the infanticidal behavioral response is a stable behavioral trait and might be passed to the offspring. © 2010 Wiley Periodicals, Inc. Dev Psychobiol 52: 825–832, 2010.     

Role of urine in coordinating reproduction in a desert rodent (Dipodomys merriami)

Detection of reproductive status from chemical signals in the urine of a desert rodent was examined. Intact and castrated male and estrous (induced) and nonestrous (ovariectomized) female Dipodomys merriami were tested for their preferences for various combinations of water and urine from intact males, estrous females, castrated males, and nonestrous females. Intact and castrated males were also tested for their responses to urine from females at different stages of the reproductive cycle: proestrus, estrus, and diestrus. Neither intact nor castrated males exhibited a preference for urine from females in any stage of the estrous cycle. Urine from intact males, however, was preferred by both intact males and estrous females. Urine from reproductively active males, rather than from estrous females, seems to contain information for coordinating reproduction in D. merriami.     

Effects of litter‐overlapping on emotionality,stress response,and reproductive functions in male and female rats

In rats, mating at postpartum estrus and delayed dispersal of the young would result in the overlapping of two different‐age litters. As a consequence, newborn pups' early experience will include not only that acquired during the interaction with the mother and age‐matched littermates, but also with older siblings. As early‐life experience modulates rodents' brain function, behavior and reproduction, we aimed to assess how changes in the early environment provoked by the overlapping of litters would affect emotionality, stress response and reproductive functions of male and female pups during adulthood. Results showed that both male and female overlapped reared pups exhibited a reduced behavioral inhibition in the open field test during adulthood. In addition, overlapped reared adult females, but not males, showed a blunted corticosterone response to an acute stressor during diestrus and a reduction in sexual behavior. In summary, natural changes in early experience provoked by the overlapping of litters, long‐term modulate affective and reproductive behaviors, and the endocrine stress response in a sex dimorphic manner. © 2008 Wiley Periodicals, Inc. Dev Psychobiol 51: 259–267, 2009     

Reproductive cycle-dependent plasticity of perception of acoustic meaning in mice

How may perception, maternal motivation and behavior of female mammals change during different phases of their estrous cycle? Here, we show effects of estrous cycle phase on the perception of acoustic meaning and maternal behavior in virgin house mice (Mus musculus) during contact with young for which they were co-caring together with the mother. Cycling females in diestrus, proestrus, estrus or metestrus responded to mouse pup wriggling calls and two synthesized call models when they were in a “nursing” position on the pups. Independent of the phase of their estrous cycle, the virgin females' response rates to naturally vocalized calls and the rates of their spontaneous maternal behavior were about half of those of mothers in the same behavioral setting. This suggests that the maternal motivation of virgin females is generally half of that of mothers but rather constant during the estrous cycle. The response rates to the call models changed during the females' estrous cycles. During diestrus and proestrus (not in estrus and metestrus) they perceived acoustic differences between the call models and responded with different rates of maternal behavior. In estrus, they showed maternal behavior at a high rate and preferred the call models similar to the natural calls. In metestrus, response rates to the synthesized call models were low, so that only natural calls (not call models) released maternal behavior at a high rate. These behavioral data from house mice show remarkable similarities with perceptual plasticity and emotional and mood-dependent reactivity during the menstrual cycle in women.     

Maternal behavior induced in male rats by bilateral lesions of the bed nucleus of the accessory olfactory tract.

In the present study, we investigate the effect of bilateral electrolytic lesions of the bed nucleus of the accessory olfactory tract (BAOT) in male Wistar rats that did not have care-pups experience, using a test of induced maternal behavior. Consistent with our previous findings in virgin female rats (10), there was a significantly shorter sensitization (3 days) and retrieval (2 days) latencies in the BAOT-lesioned group than in the sham-lesioned and intact-control male groups (12 days for both). Based on these findings, we propose that BAOT, a sexually dimorphic nucleus of the vomeronasal system, exerts an inhibitory modulation in the expression of parental behavior in male and female virgin rats. It may do so by maintaining an olfactory-based tonic inhibition of maternal behavior, thereby resulting in the adults' tonic avoidance of the pups until this inhibition is abolished by lesion, or reduced or overridden by appropriate hormonal and/or sensory influences.     

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.     

Overlapping litters in rats: effects on maternal behavior and offspring emotionality

Female rats have a fertile postpartum estrus, which can result in a simultaneous gestation and lactation and later in the overlapping of two different-age litters. These different physiological and contextual situations may affect the maternal behavior of lactating rats and provoke long-lasting changes in the affective behavior of the litter. Therefore, we aimed to assess the effect of pregnancy and of litter overlapping on the maternal behavior of lactating rats and to describe the maternal- and anxiety-like behaviors of the juveniles that remained in contact with their younger siblings. Results showed that pregnant lactating rats spent more time outside the nest and less time nursing than non-pregnant mothers. On the other side, mothers with overlapping litters licked less the newborn pups than mothers with single litters. These deficits in maternal licking received by neonates were overridden by the juveniles' licking behavior to their younger siblings. Adult male and diestrous female rats reared with younger siblings showed a reduced anxiety-like behavior as compared to age-weaning matched animals without this experience. Thus, natural changes in the reproductive conditions and in the early experience, affect the maternal behavior and long-term modulate affective behavior of the individuals.     

Opioid receptor antagonism during early lactation results in the increased duration of nursing bouts

High levels of mu opioid receptor activation during the postpartum period result in the disruption of ongoing maternal behavior. The role of physiological levels of endogenous opioids on the mediation of maternal behavior in postpartum females, however, has not been closely examined. The purpose of the present experiments was to examine the function of endogenous opioids during early and mid-lactation by treating postpartum females with the opioid antagonist naloxone and monitoring their behavioral interactions with pups. Although this treatment did not lead to any qualitative differences in the maternal behaviors measured (pup retrieval and grooming, nest building, grouping of pups, or crouching over pups), there was a quantitative difference in the amount of time the females spent with pups on the nest and actively nursing pups. Naloxone, given either systemically or centrally (intracerebroventricularly), resulted in prolonged nursing and nesting bouts. This effect, however, was only observed during the early lactation time point (postpartum days 5-7). Females tested later in lactation (postpartum days 10-12 or 12-14) did not display the increased nursing or nesting bouts in response to the antagonist. These data indicate that central opioids play a role in the duration of nursing bouts during early lactation.     

The medial preoptic area is necessary for motivated choice of pup- over cocaine-associated environments by early postpartum rats

Converging evidence suggests that the motivation to seek cocaine during the postpartum period is significantly impacted by the competing incentives of offspring, a stimulus unique to this life stage. In the present study, the functional role of the medial preoptic area (mPOA), a critical site involved in maternal responsiveness, on processing incentive value of pup-associated cues and influencing response allocation for pup- over cocaine-associated environments was investigated using a concurrent pup/cocaine choice conditioned place preference (CPP) paradigm. Early postpartum females with bilateral guide cannulae aimed into the mPOA or into anatomical control sites were conditioned, from postpartum days (PPD) 4 to 7, to associate different uniquely featured environments with pups or cocaine. CPP was tested on PPD8 following intra-mPOA infusions of either 2% bupivacaine or saline vehicle. In two additional experiments, the effects of intra-mPOA infusions of bupivacaine on expression of conditioned responding induced by environments associated with either pups or cocaine were examined separately. Transient inactivation of the mPOA selectively blocked the conditioned preferences for pup-associated environments, significantly contrasting the robust pup-CPP found in non-surgical and intra-mPOA vehicle-treated females. In contrast, mPOA inactivation failed to alter cocaine-CPP in postpartum females. When given a choice between environments associated with pups or cocaine, transient functional inactivation of the mPOA altered choice behavior, biasing the preference of females toward cocaine-associated environments, such that almost all preferred cocaine- and none the pup-associated option. The anatomical specificity was revealed when inactivation of adjacent regions to the mPOA did not affect CPP responses for pups. The findings support a critical role for the mPOA in mediating pup-seeking behavior, and further suggest that the competing properties of pups over alternative incentives, including drugs of abuse, rely on mPOA integrity to provide relevant pup-related information to the circuitry underlying the choice behavior between pups and alternative stimuli.     

Experience with pups sustains maternal responding in postpartum rats

In these studies, we investigated the sustaining of postpartum maternal responsiveness through pup experience. In the first study, females were tested for maternal behavior at various times after pregnancy termination by Caesarean section (CS) at term. The females remained rapidly responsive to young for 7 days after pregnancy termination, but were no more responsive than virgins after 10 days. In the second study, females were allowed varying times of complete access to pups, beginning 24 hours after CS, and were tested for maternal behavior 10 days later. Females who retrieved and cared for pups for 30 minutes during exposure, remained rapidly maternal 10 days after CS; those who were allowed only 15 minutes of caring for pups did not. In the third study, females received 24 hours of exposure to distal sensory stimuli from pups, beginning 24 hours after CS. The proportion of females who became maternal within 24 hours of the beginning of maternal testing, 10 days after CS, was greater than that among females who received no exposure to pups.     

Homosexual and heterosexual partner preference in ovariectomized female rats: effects of testosterone, estradiol and mating experience

Ovariectomized female rats, longterm treated with estradiol benzoate (EB, 20 micrograms, 3 x/week) or testosterone propionate (TP, 0.4 mg, 3 X/week), were tested for homo- or heterosexual partner preference behavior with either tethered animals (sexually active male vs. estrous female) or animals behind a wire mesh. A preference score was calculated by subtracting the time spent in the vicinity of the stimulus female from the time spent in the vicinity of the stimulus male. Thus, a positive score indicates preference for the male (heterosexual preference), a negative score preference for the female (homosexual preference). Two weeks of EB treatment caused a clearcut preference for the male incentive. This heterosexual preference was significantly different from the indistinct preference of the TP-treated females. Sexual interaction with a freely moving active male (with or without a vaginal mask which prevented intromissions) did not alter the preference for the male of the EB-treated females. It did affect, however, the preference behavior of the TP-treated females significantly: it changed in the direction of the sexually active estrous incentive female, i.e., a homosexual preference. This change in preference could not be attributed to the experience of penile intromissions, it occurred despite the presence of a vaginal mask. Apparently, being mounted by a sexually active male had a negative reinforcing value in the TP-treated female rats and provoked a homosexual partner preference.     

Photoperiod and gonadal hormones influence odor preferences of the male meadow vole, Microtus pennsylvanicus.

Male meadow voles housed in a long photoperiod (14 h light/day, LP) preferred female to male odors, whereas males maintained in a short photoperiod (10 h light/day, SP) did not display preferences for odors of either sex. These odor-preference patterns matched those of free-living males during spring and autumn, respectively. The preference of LP male voles for female over male odors was eliminated by gonadectomy and reinstated by treatment with testosterone. In SP males, although gonadectomy did not affect odor choices, a preference for female odors was induced by testosterone treatment. Treatment with estradiol did not alter odor preferences of LP or SP males. In conjunction with previous result, the present findings suggest that hormonal responsiveness of neural substrates that control odor preferences are sexually dimorphic and may reflect sex differences in reproductive strategies.     

Male-induced estrus synchronization in the female Siberian hamster (Phodopus sungorus sungorus)

Olfactory cues play an integral role in the organization of events that mediate reproductive success. In a variety of species, priming pheromones, in particular, are important for ensuring reproductive fitness. To date, very little research has focused on how male-emitted priming pheromones, such as those that regulate the onset of puberty and estrus synchronization in females, affect the reproductive physiology of the female Siberian hamster (Phodopus sungorus sungorus). This lack of research may be due to the physiology of the Phodopus genus; vaginal cytology cannot be used as a reliable indicator of estrus or ovulation. Using a jugular cannulation technique to determine estrous stage by blood analysis of prolactin and luteinizing hormone, we sought to determine if male priming pheromones affect estrous cyclicity in the female Siberian hamster and, if so, whether the production of these priming pheromones is androgen dependent. Our results showed that females exposed to bedding from mature, intact males showed a significantly higher incidence of proestrus 3 days later than did females exposed to the bedding of mature, gonadectomized males. Therefore, we found that not only do male Siberian hamsters emit chemical signals that induce estrus synchronization, but also that this ability is likely to be androgen dependent.     

Aging and sex influence the anatomy of the rat anterior cingulate cortex

Cognitive processes supported by the prefrontal cortex undergo an age-related decline. Until very recently, nonhuman animal models of aging have relied on the exclusive use of male subjects. This study was designed to investigate the influence of age, sex, and ovarian hormonal state on anatomy of the rat medial prefrontal cortex (anterior cingulate cortex). Dendritic tree extent and spine density were examined in young adult (3-5 mos.) and aged (20-24 mos.) male and female rats. Young adult females were examined either at proestrus or estrus, and aged females were examined in one of two reproductively senescent (estropausal) phases, persistent estrus or persistent diestrus. Neither the estrous cycle nor state of estropause influenced spine density or dendritic tree extent. However, the anatomy of the anterior cingulate cortex of young adult rats was sexually dimorphic, with males having greater dendritic spine density as well as arborization. While there was a reduction in density and tree extent with age for both sexes, this reduction was more pronounced for males, resulting in a disappearance of most sex differences with age. Thus the results of this study suggest that aging of the rodent cerebral cortex may follow a sexually dimorphic pattern.