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.     

Intrauterine position,parenting, and nest-site attachment in male Mongolian gerbils

We housed male Mongolian gerbils, their mates, and foster litters of standardized size and sex ratio in enclosures that provided cover in two locations. Males had been gestated in known intrauterine positions: either between two females (2F males) or between two males (2M males). From Days 1 to 20 postpartum, we examined the frequency with which both males and females were in contact with the pups they were rearing. We found that 2F males spent more time with pups than did 2M males both during entire observation periods and when females were away from the nest. Further, when pups were moved from the nest site, 2M males spent more time than did 2F males in the vacated nest site. We concluded that 2F male gerbils spent more time with pups than 2M males not because of a greater attachment of 2F than 2M males to places of concealment, their mate, or their nest site. Rather, 2F males were more attracted to pups than were 2M males. © 1998 John Wiley & Sons, Inc. Dev Psychobiol 32: 177–181, 1998     

Activation of the immune-endocrine system with lipopolysaccharide reduces affiliative behaviors in voles

In Experiment 1, individually housed male meadow voles (Microtus pennsylvanicus) and prairie voles (Microtus ochrogaster) were injected with lipopolysaccharide (LPS) and exhibited the expected decrease in testosterone and increase in corticosterone and interleukin-1beta concentrations 3 hr later, indicating activation of the endocrine and immune systems. In Experiment 2, LPS- and saline-injected males were tethered in a 3-chamber partner preference apparatus. The time females spent in each chamber with a male, as well as the amount of time spent in social contact, was monitored. Female prairie voles, but not meadow voles, spent more time in the chamber with saline- than with LPS-injected males. LPS-injected male prairie and meadow voles engaged in less social contact with female conspecifics than did saline-injected males. These data suggest that LPS modifies physiology and behavior in male voles and that females may use these changes to discriminate healthy from potentially infected males.     

Effects of stress on parental care are sexually dimorphic in prairie voles

The effects of stress on parental care are poorly understood, especially in biparental species where males also display care. Data from previous studies in prairie voles, as well as parallels with pair-bonding behavior, suggest the hypothesis that a stressful experience might facilitate parental care in males but not in females. In the present study, male and female prairie voles were exposed to either a 3-min swim stressor or no stressor; 45 min later each animal was tested in a parental care paradigm. Following the parental care test, blood samples were collected and assayed for corticosterone (CORT). After the stressor males, but not females, showed significant changes in parental behavior including significantly more time in kyphosis (arched-back huddling), and a tendency to spend more time licking and grooming pups. In males, CORT levels measured following the parental care test were inversely related to licking and grooming but positively correlated with retrievals. These findings support earlier studies suggesting that the neuroendocrine substrates of parental behavior, as well as the effects of stressors, are sexually dimorphic in this species.     

Variability in "spontaneous" maternal behavior is associated with anxiety-like behavior and affiliation in naïve juvenile and adult female prairie voles (Microtus ochrogaster)

Juvenile female prairie voles (Microtus ochrogaster) are spontaneously maternal, while virgin adult females show significant variability in their response to first pup exposure, ranging from infanticidal to full maternal behavior. In the present study, we investigated whether differences in anxiety-like behavior and affiliation are associated with juvenile-adult and adult individual differences in the response to pups. Forty juvenile (19-20 days) and 42 adult (60-90 days) female prairie voles were exposed to pups for the first time and tested for maternal behavior, anxiety-like behavior (elevated plus maze, open field), and affiliation toward age-matched, same sex conspecifics. Juveniles displayed less anxiety-like behavior, were more affiliative to unfamiliar conspecifics, and interacted with pups more positively than adults. Adults that displayed maternal behavior spent less time immobile, made more crosses through the center of the open field arena, and were more affiliative than adults that attacked the pups. This suggests that lower locomotion or exploration in a novel environment and poor affiliative behavior are negatively associated with maternal responsiveness in female prairie voles.     

Interaction of photoperiod and testes development is associated with paternal care in Microtus pennsylvanicus (meadow voles)

During the summer breeding season, free-living meadow voles do not engage in paternal care. However, in fall when female territoriality declines, social nesting and breeding activity may overlap and adult males nest with females and young. In the laboratory, meadow voles housed under short day (SD) lengths exhibit more and better quality paternal care than those housed under long day (LD) lengths. This observation is commensurate with the hypothesis that SD paternal care may increase fitness by decreasing pup mortality during colder months. However, SD males also demonstrate variability in paternal care. We hypothesize that this variability may be due to male fertility status; SD infertile males, incapable of siring offspring, should be less likely to care for pups than fertile males, for whom paternal care may confer fitness benefits. The goal of this experiment was to determine whether paternal behavior differed between fertile LD males, fertile SD males (i.e. males that were gonadally photoperiod-unresponsive to SD lengths), and infertile SD males (i.e. males that were gonadally photoperiod-responsive to SD lengths), as indexed by paired testes weights and behavioral evaluation. Fertile SD males exhibited proportionally more paternal behavior than infertile SD males or fertile LD males, which did not differ from each other. Fertile SD males also exhibited paternal behavior faster, spent more time in contact with pups, and engaged in longer and more frequent bouts of pup-directed grooming and huddling than either infertile SD males or fertile LD males. Collectively, these data suggest that photoperiod and fertility status may interact to exert both inhibitory and permissive control over the expression of paternal behavior in adult meadow voles.     

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.     

Diurnal and nocturnal nursing behavior in the OLETF rat

The Otsuka Long Evans Tokushima Fatty (OLETF) rat model of obesity has been recently found to develop hyperphagia and obesity early in life. Our goal was to investigate the dams' nursing behavior during the day and the night in order to elucidate their contribution to the pre-obesity of the pups. We examined nursing bout number, length, posture, initiative, nursing total time and frequency of other maternal behaviors over the three postpartum (PP) weeks. In the first week, OLETF dams nursed more during the day and presented more self-directed activities during the night. In the third PP week, OLETF dams displayed increased nursing time, bout number, nursing frequency, and supine postures at the beginning of the nursing episodes and less active self-directed behaviors, both day and night, while OLETF pups displayed more initiative in starting nursing bouts. The results suggest a circadian difference in nursing behavior and self-directed activities between the strains on PP week 1 and a strong influence of the OLETF pups on the nursing behavior of the dam on PP week 3, which contributes to their obese features.     

Female prairie vole mate-choice is affected by the males’ birth litter composition

Experimental testing and retrospective examination of breeding records were used to examine the influence of sex composition and/or size of males’ birth litters on female mate-choice. Sexually naïve female prairie voles (Microtus ochrogaster) avoided males derived from all-male litters, but showed no preference for, or aversion to, males from single-male litters or from more typical mixed-sex litters. Examination of the pregnancy status of females after two weeks of pairing with a male allowed us to estimate the probabilites of a pups’ intrauterine position relative to siblings for various litter sizes. The typical prairie vole pup derived from a mixed-sex litter comprised of 4.4 pups, and had a 13% chance of being isolated from siblings in utero and a 22% chance of being between siblings in utero. Pups from single-sex litters tended to be larger at weaning than did pups from mixed-sex litters; however, male size did not influence female choice behavior. These results suggest that some aspect of the perinatal experience of prairie vole pups from single sex litters can influence social interactions later in life.     

Olfactory bulbectomy: influences on maternal behavior in primiparous and multiparous rats

Bilateral olfactory bulb ablation resulted in deficits in several components of maternal behavior in lactating, primiparous female rats. These females frequently cannibalized pups shortly after parturition. Furthermore, bilaterally bulbectomized, primiparous females spent less time nursing their pups and retrieved fewer pups than unilaterally bulbectomized or sham-operated females. In contrast to the situation in primiparous females, in multiparous females bilateral bulbectomy failed to influence any parameter of maternal behavior.     

Lipopolysaccharide facilitates partner preference behaviors in female prairie voles

Exposure to proinflammatory cytokines (e.g., IL-1beta) or lipopolysaccharide (LPS) produces an acute activation of the immune response and results in a repertoire of behavioral patterns collectively termed sickness behaviors. Although nonspecific responses to pathogenic infection have traditionally been viewed as maladaptive effects of infection, sickness behaviors may have significant, adaptive value for the host. One set of adaptive behaviors affected by infection among mammals and birds is mate choice. In Experiment 1, female prairie voles exhibited the expected increase in blood corticosterone concentrations in response to a 0.1 cc i.p. LPS injection (50 microg), indicating activation of the endocrine system. A separate cohort of females was injected with LPS or saline and paired for 6 h with a novel, previously unpaired male. Following the cohabitation period, LPS-injected females spent significantly more time (p < 0.05) with the familiar partner when given a choice between familiar and unfamiliar males in a three-chamber apparatus designed to test partner preferences. Saline-injected females spent significantly more time with the unfamiliar male. In Experiment 2, males injected with LPS or saline spent equal amounts of time with familiar and unfamiliar females following a 6 h cohabitation with a naive female, and therefore, did not exhibit preferences. From a proximate perspective, this study provides evidence that sickness behaviors influence female, but not male, partner preference in prairie voles.     

Diurnal and nocturnal nursing behavior in the OLETF rat

The Otsuka Long Evans Tokushima Fatty (OLETF) rat model of obesity has been recently found to develop hyperphagia and obesity early in life. Our goal was to investigate the dams' nursing behavior during the day and the night in order to elucidate their contribution to the pre‐obesity of the pups. We examined nursing bout number, length, posture, initiative, nursing total time and frequency of other maternal behaviors over the three postpartum (PP) weeks. In the first week, OLETF dams nursed more during the day and presented more self‐directed activities during the night. In the third PP week, OLETF dams displayed increased nursing time, bout number, nursing frequency, and supine postures at the beginning of the nursing episodes and less active self‐directed behaviors, both day and night, while OLETF pups displayed more initiative in starting nursing bouts. The results suggest a circadian difference in nursing behavior and self‐directed activities between the strains on PP week 1 and a strong influence of the OLETF pups on the nursing behavior of the dam on PP week 3, which contributes to their obese features. © 2008 Wiley Periodicals, Inc. Dev Psychobiol 50: 203–203, 2008.     

Behavioral responses of infant rats to maternal licking: variations with age and sex

Behavioral interactions of Norway rat pups and their dams during maternal anogenital licking (AGL) were observed. Regularities in posture and orientation that may facilitate AGL were noted, and age-related changes in the pup's postural adjustments that may contribute to the decline of AGL in the 3rd postpartum week were described. It was found that cutaneous stimulation of the perineum, such as that provided by AGL, stimulates a characteristic leg extension response from pups. It was concluded that this response, which includes immobility and extension of all limbs, may permit maternal licking to continue long enough to stimulate the pup to eliminate and to allow the dam to ingest the urine. Males and females were found to exhibit similar responses and similar age-related changes. However, the latency from onset of AGL to performance of the leg extension response was shorter in males.     

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.     

Responses of male hamsters to the ear gland secretions of conspecifics

The behavioral responses of sexually experienced males toward anesthetized conspecifics were examined. Males directed more mounts and spent significantly more time investigating the ears and genital region of castrated males and diestrous females than intact males. Castrated males were treated in a similar manner to females, suggesting that the absence of an androgen-dependent factor(s) renders an animal more sexually attractive. Males were also administered paired preference tests in which they investigated the odors from the ear glands of diestrous females, castrated males, and intact males. Subjects spent significantly more time investigating the odors originating from ear glands of females and gonadectomized males than intact males. There was no significant difference in the amount of time males spent with the ears of castrated males and diestrous females. These experiments demonstrate that sexually experienced male hamsters can utilize odors associated with the ears to discriminate the gender of conspecifics.     

Early experience affects the traits of monogamy in a sexually dimorphic manner

The goal of this study was to examine the effects of early life experiences on the subsequent expression of traits characteristic of social monogamy in prairie voles (Microtus ochrogaster). During cage changes parents and their offspring were either transferred between cages in a cup (zero manipulation, MAN0) or with a gloved hand (one manipulation, MAN1). Following weaning the offspring were tested for alloparental behavior. In adulthood they were tested for the capacity to form partner preferences, behavior in an elevated plus-maze (EPM), and corticosterone levels. MAN0 males (but not females) showed lower levels of alloparental behavior than MAN1 males. MAN0 females (but not males) were less likely to form pair bonds than MAN1 females. MAN0 animals of both sexes were less exploratory in the EPM than MAN1 counterparts. These experiments support the hypothesis that behaviors used to characterize monogamy are vulnerable in a sex-specific manner to early experience.     

Sex differences and developmental effects of manipulations of oxytocin on alloparenting and anxiety in prairie voles

In adult animals, peptide hormones, including oxytocin and arginine vasopressin, have been implicated in both parental behavior and the modulation of anxiety. The purpose of this study was to examine the consequences of developmental manipulations of oxytocin for the later expression of alloparental behavior as well as behavioral responses to a novel environment, the elevated plus maze (EPM). Prairie voles (Microtus ochrogaster), a cooperatively breeding species, were selected for this study. On neonatal Day 1, pups received an ip injection of oxytocin or oxytocin antagonist, or were controls, receiving either saline or handling only. At 21 and approximately 60 days of age, each animal was tested for parental care toward novel stimulus pups. At approximately 67 days, an EPM test was administered. Control females at 60 days of age were more likely to attack pups and spent less time in the open arm of the EPM, both of which might reflect higher levels of anxiety in females than males. In males, neonatal treatment with oxytocin antagonist was associated with reductions in parental care, especially during the initial exposure to pups on Day 21. Female behavior was not significantly changed as a function of neonatal treatments. Findings to date implicate vasopressin in the behavioral changes in males, that in later life followed a single exposure to an oxytocin antagonist, and suggest caution in the clinical use of agents such as Atosiban, which may have the potential to influence infant development.     

Costs of pair-bonding and paternal care in male prairie voles (Microtus ochrogaster)

The direct costs of paternal care are relatively well documented in primates, however little research has explored these effects in monogamous rodents. The present study examines the long-term effects that pairing and parenting have on male prairie voles. We hypothesized that there would be a significant weight loss over the course of pairing and parenting, presumably from the energetic demands that accompany these changes in social condition. In a longitudinal study, we followed ten male prairie voles through being housed with their brother; paired with a female; and caring for three consecutive litters. We found a significant drop in bodyweight across time, with maximum weight loss near the weaning of the first litter. At that same time, feeding increased, leading to possible recovery in weight; however, leptin levels dropped precipitously across time and did not recover. Corticosterone did not change significantly across time points, and overall activity levels also did not vary significantly over the course of the study. In addition, newly paired males showed a significant increase in preference for a 2% sucrose solution during a three-hour test, indicating a metabolic need for more calories. A cross-sectional study confirmed leptin and corticosterone findings, and showed significant loss of subcutaneous (inguinal) fat in males that had cared for a litter of pups, when compared to males housed with their brothers or newly paired males. These results suggest that cohabitation with a female, and caring for pups, all have costs for male prairie voles.     

Weaning in rats: I. Maternal behavior

Maternal behavior during the weaning period (postpartum Days 14-35) was described from continuous timelapse videorecordings of Norway rat dams and their litters. Time spent nursing declined steadily after Day 20 but persisted until Day 34, about a week longer than suggested by reports of milk transfer. Most of the decline in nursing was due to progressively fewer nursing bouts per day; milk letdowns per day were consequently diminished. Although a private feeding chamber was available to the dams, they did not use this chamber to spend more time away from the pups as weaning progressed. Instead, the dams remained with the pups in the nesting chamber but devoted increasingly less time to nursing. Subtle, progressive changes in maternal behavior are closely orchestrated and coordinated with pup development.