Parental environment: effects on survival, growth and aggressive behaviors of 2 rodent species

The influence of the parental environment on the development of aggressive behaviors was studied in 2 muroid rodent species. Litters of southern grasshopper mice and northern white-footed mice were reared by the natural parents or were reciprocally cross-fostered soon after birth to parents of the opposite species. After weaning at 24–26 days, mice of both species were isolated and observed at 10-day intervals from 30 to 100 days of age in one of the following tests: (1) predation on house crickets; (2) interspecific aggression toward Swiss-Webster laboratory mice; and (3) intraspecific aggression toward opponents of the same gender and approximate age. Naturally reared grasshopper mice males and females displayed extremely high levels of aggressive and predatory behaviors whereas white-footed mice controls were passive and defensive in all tests. Rearing by white-footed mice foster parents resulted in a significant decrease in the aggression of grasshopper mice males and females toward laboratory mice. During intraspecific encounters, fostered grasshopper mice initiated fewer social interactions than naturally reared controls. The predatory behavior of grasshopper mice was not altered by the fostering procedure. The behavioral measures of fostered white-footed mice showed no systematic changes when compared to controls. These results indicate that the postnatal parental environment contributes to the naturally high levels of aggressive behaviors of grasshopper mice. In contrast, the limited aggressive behaviors of a naturally passive species, white-footed mice, were not increased by fostering at birth to parents of a highly aggressive species, grasshopper mice.     

Intergenerational effects of complete maternal deprivation and replacement stimulation on maternal behavior and emotionality in female rats

The present study investigated the effects of early rearing experiences on the development of maternal behavior in Sprague-Dawley female rats. Pups from individual litters were assigned to four different groups on Day 3 of life. From days 4 to 20 of life, these were reared artificially, without mother and receiving minimal "licking-like" tactile stimulation (AR-MIN), or maximal stimulation (AR-MAX) or were reared with their mothers (MR-CONTROL and MR-SHAM). At 70-100 days all AR and MR animals were mated and then observed with their own offspring, culled to eight pups. After maternal testing open-field tests were conducted. The female offspring in these litters (all raised by their MR and AR mothers) were reared to adulthood and then observed interacting with their offspring. Results show that in adulthood AR mothers engaged in significantly fewer pup-retrievals and less pup-licking (genital and body), and crouching, but significantly more non-maternal tail-chasing, digging, and hanging/climbing. As well, they were more active in the open field. Comparisons between the two AR groups and the MR groups, showed that most of the differences were between the AR-MIN and MR groups, with the AR-MAX animals showing levels of behavior between the two, and differing from neither. Analyses of covariance indicated that early experience and adult emotional behavior both influence adult maternal behavior, but their effects are independent of one another. A cross-generational effect of artificial rearing was also found. Daughters of AR and MR mothers that were observed after the birth of their own litters in adulthood showed a pattern of behavior that mimicked the pattern shown by their mothers. These results are discussed in terms of the variety of possible behavioral, endocrine, and neurochemical mechanisms that mediate the effects of early experiences on adult maternal behavior.     

The effects of preparturient avoidance conditioning on postnatal caretaker behavior and offspring catecholamine levels and behavior in C57BL/6J mice.

Avoidance conditioning during pregnancy, changes in caretaker behavior during lactation, and changes in offspring catecholamine levels and behavior were investigated in C57BL/6J mice. Three equal groups of mice were employed. One group was avoidance conditioned prior to pregnancy and continued to avoid shock during pregnancy; a 2nd group was avoidance conditioned during pregnancy; and the 3rd group served as untreated controls. Offspring were crossfostered after birth. During lactation the proportion of time the caretaker spent on the nest was observed. At weaning pups were individually housed. Offspring dopamine concentrations were measured in the corpus striatum at birth and at days 22 and 42 of age. Their performance was evaluated in the open field at Day 42 of age. The results showed that mice receiving avoidance conditioning prior to parturition were more likely to cannibalize their offspring at parturition than were control animals. Furthermore, preparturiently avoidance conditioned mice spent less time on the nest if they reared offspring from biological mothers who had been avoidance conditioned when compared to similarly treated caretakers who reared offspring from untreated control biological mothers. Regardless of postnatal experiences, adult offspring from avoidance conditioned biological mothers had significantly reduced levels of dopamine in tissue from the corpus striatum and were significantly less active in the open field when compared with offspring from control biological mothers. Behavioral results support the findings of others that the prenatal environment plays an important role in shaping the later behavior of offspring. The decrease in dopamine levels suggests that avoidance training as one form of psychosocial stimulation during pregnancy can be disruptive to the development of the dopamine regulatory mechanisms.     

Genetic and littermate influences on yawning in two selectively bred strains of rats

This study was made to separate genetic from postnatal maternal influences on yawning in two strains of Sprague‐Dawley rats selected for high‐ (HY) and low‐yawning frequency (LY). Foster mothers of the two strains reared litters of pups in the four possible combinations and yawning was recorded in a novel environment when the adult offspring were 75‐day‐old. Yawning frequency of males and females was affected by pup strain but not by the strain of the foster mothers, when litter size was made constant; HY adult offspring yawned more than LY adult offspring. Yawning frequency was higher in HY male offspring than in HY female offspring. An interaction term between pup sex and the strain of the foster mothers revealed that while males reared by LY mothers yawned more than males reared by HY mothers, females reared by HY mothers yawned more than females reared by LY mothers. Mean frequency of yawning increased with the sex ratio of HY litters. These findings indicate that genetic and genotype‐correlated littermate effects influence yawning frequency of adult offspring in response to a novel environment. © 2008 Wiley Periodicals, Inc. Dev Psychobiol 51: 243–248, 2009     

Maintenance and decline of the suppression of infanticide in mother rats.

Virgin female rats kill foster neonates, whereas newly parturient mothers do not. We demonstrated previously that this tendency to kill is suppressed shortly prepartum, presumably by physiological factors. In this study, we show that a) suppression of infanticide is maintained through the first two weeks of lactation; b) the mothers that do not kill foster neonates are not necessarily the same mothers that respond maternally toward older foster pups, and those that kill neonates are not necessarily the same ones that are nonmaternal to older pups, the two behaviors being somewhat independent; and c) some virgins can be induced to be noninfanticides by prolonged exposure to young, but only under special testing conditions not required by actual mothers, which are nonkillers of foster young. This suggests that the maintenance of the suppression of infanticide in mothers owes something to the special circumstances of lactation other than continued exposure to young.     

Some effects of a split litter cross foster design applied to 15 day old rat pups

Rat litters were divided and cross fostered on a postnatal Day 15 so that each mother had 4 of her own pups and 4 pups of a second litter, until weaning at 21 days. Daily weight and body temperature measurements made between Day 15 and 21 showed no differences between foster pups and pups who stayed with their biological mothers. However, by the age of 30 days, foster pups weighed less than pups reared by their own (biological) mothers; and foster pups at that age did not survive food deprivation as well as the pups reared by their biological mothers. In their Day 30 weights and the capacity to survive food deprivation, foster pups resembled pups that had been permanently separated from their mothers on postnatal Day 15. We conclude that the split cross foster design may introduce variability rather than reduce it. Nonetheless, this design may be useful in the experimental investigation of maternal behavior and mother-pup interactions in the rat.     

Effects of differential early experience upon parental behavior in Mus musculus

Infant mice reared with both parents were subjected to 1 of 4 different early experience contingencies at 3, 6, 9, and 12 days of age. Observation of parental behaviors following return of the pups to the nest revealed that mothers attended more to pups subjected to intermediate levels of stress, with the differences in maternal behavior persisting across the age span without change. Fathers exhibited marked changes in responsiveness to young across the ages observed, with their attention to young correlating directly with rate of ultrasonic calling by the young.     

Experiments on maternal and paternal transmission of Creutzfeldt-Jakob disease in mice

Summary No transmission of Creutzfeldt-Jakob disease in mice was observed in 75 offspring born to CJD agent-inoculated females or to normal females mated with inoculated males and in 19 normal offspring maintained by foster nursing with the inoculated mothers. The fertility of young adult female mice was lost by the 57th day after the inoculation, whereas the reproductivity of male mice was maintained over 106 days after the inoculation.     

Variation in infanticide and parental behavior in male mice due to prior intrauterine proximity to female fetuses: Elimination by prenatal stress

When sexually-naive male mice are placed together with newborn young, some males will commit infanticide (kill the young) while others will behave parentally (retrieve the young to a nest and keep them warm). The intrauterine position of male mouse fetuses, which is recorded at Cesarean delivery, has previously been found to influence the titers of estradiol that male fetuses are exposed to in utero. In adulthood, most male mice that developed in utero between male fetuses (2 M males) behaved parentally toward young, while most males that developed in utero between female fetuses (0 M males) committed infanticide. When 0 M and 2 M males were castrated at birth and tested with young in adulthood, few males committed infanticide. But, when these same males were tested with young after 25 days of treatment with testosterone, more 0 M than 2 M males committed infanticide and more 2 M than 0 M males behaved parentally. In contrast to the above findings, more 2 M than 0 M males that were castrated when 28 days old behaved parentally without treatment with testosterone; few of the non-parental males committed infanticide, but, instead, ignored the young. Finally, stressing pregnant mice by placing them under bright lights during the last third of pregnancy eliminated the effect of developing next to female fetuses in the male offspring, and all prenatally-stressed males resembled 2 M males in their behavior toward young: most prenatally-stressed males were parental rather than infanticidal when tested with young. The significance of these findings to models of hormonal effects on sexual differentiation is discussed.     

Effects of parental environment on the prevalence of convulsive seizures in Onychomys torridus

Male and female southern grasshopper mice (Onychomys torridus) were reared in 1 of 3 different parental environments: (a) with the natural male and female parents; (b) with the female parent only; or (c) with foster parents of a closely related species, Peromyscus leucopus. All mice were weaned at 25 days of age, then observed individually in an open field arena at 10-day intervals from 30 to 100 days of age. Twenty-seven of 59 subjects (45.8%) that were reared by the natural parents exhibited convulsive seizures during at least 1 of the 8 tests in the open field arena. The prevalence of convulsive seizures increased significantly in subjects that received altered parental care: 27 of 41 subjects (65.9%) reared by the female parent only or by Peromyscus foster parents seized during at least 1 of the 8 tests in the open field. Subjects from the 3 treatment groups did not differ in the mean number of seizures observed during the 8 open field tests. These results demonstrate a significant influence of the preweaning parental environment on the prevalence of convulsive seizures in Onychomys torridus.     

Septal damage and muricide: effects of stain and handling

Rats from two strains (Long-Evans and Sprague-Dawley) were subjected to either septal ablations or sham operations and were either handled or not handled for the first four postoperative days. On the fifth day all animals were tested for muricidal behavior using albino mice. L-E rats showed a greater tendency to kill than S-D rats. Additionally, septal lesions increased the probability of muricide in the L-E strain while no difference was observed in S-D rats. Finally, handling had no effect upon the expression of muricide.     

Effect of maternal feed restriction on blood pressure in the adult guinea pig

Small size at birth has been associated with increased blood pressure in adult men and women. In rats, isocaloric protein restriction reduces fetal growth and increases systolic blood pressure in adult offspring. Balanced maternal undernutrition in the rat also increases adult blood pressure, but not consistently. The aim of this study was to determine the effect of moderate balanced maternal undernutrition (85% of ad libitum intake from 4 weeks before, and throughout pregnancy) on blood pressure of adult offspring in the guinea pig, a species that is relatively mature at birth. Blood pressure was measured in chronically catheterised offspring of ad libitum fed or feed-restricted mothers, at 3 months of age (young adult). Maternal feed restriction reduced birth weight (-17%) and increased systolic blood pressure (+9%, P < 0.03) in young adult male offspring. In offspring of ad libitum fed and feed-restricted mothers, combined data showed that systolic blood pressure and mean arterial pressure correlated negatively with head width at birth (P = 0.02 and P = 0.04, respectively, n = 28). Systolic blood pressure also correlated negatively with birth weight and the ratio birth weight/birth length, but only in offspring of ad libitum fed mothers (P = 0.04 and P = 0.03, respectively, n = 22). The effect of maternal feed restriction on systolic blood pressure in male offspring was not significant when adjusted for these measures of size at birth. Thus, moderate balanced undernutrition in the guinea pig increases systolic blood pressure in young adult male offspring; however, these effects may be mediated, at least in part, through effects on fetal growth.     

Similarities in affiliation and aggression between cross-fostered rhesus macaque females and their biological mothers

In female-bonded primate species, there is cross-generational consistency in female affiliative and aggressive behavior. This consistency could be the result of maternal effects, offspring learning, shared environment, and/or direct genetic inheritance of behavioral or psychological traits. In this study, I investigated possible similarities in affiliation and aggression between cross-fostered rhesus macaque females and their biological mothers. Ten female infants were cross-fostered at birth, and selected aspects of their affiliative and agonistic behavior over the course of their first 3 years of life were compared to the behavior of their foster and biological mothers. Average offspring rates of social contact and aggression across the 3 years, and in particular in Years 2 and 3, resembled those of their biological mothers whereas no clear behavioral similarities between offspring and foster mothers were observed at any age. Heritable variation in female social behavior may be maintained by natural selection and leads to adaptation to different socioecological niches within macque populations.     

Avoidance conditioning in mice as a function of their mothers' training

Prior to mating, inbred female mice were exposed to 1 of 4 conditions for 15 days: 50 trials of avoidance conditioning per day; equivalent (yoked) exposure to conditioned stimulus (CS) and shock, but without the response contingency; yoked exposure to the CS alone; or no experimental treatment. Within 48 hr after birth the offspring of these females were transferred to unrelated foster mothers. The treated females served as foster mothers for the offspring of untreated females. When the adult avoidance conditioning performance of the offspring was analyzed, an interaction was found between the sex of the offspring, the treatment of the mothers, and the developmental period during which the maternal treatment influenced the offspring. In general, the prenatal effect of maternal treatment was the reverse of the postnatal effect, and its effect, while somewhat greater on female offspring, also was the reverse of its effect on male offspring.     

Changes of brain serotonin and muricide behavior following chronic administration of theophylline in rats.

Temporal modification of amygdaloid serotonin (5HT) content and the resultant muricide behavior, compared to isolated and olfactory bulbectomized rats, were studied after chronic theophylline administration. Theophylline raised amygdaloid 5HT after Day 28 and amygdaloid 5-hydroxyindoleacetic acid (5HIAA), its deaminated metabolite, after Day 7. Theophylline applied for 29 days elevated 5HT and 5HIAA in the amygdala, the diencephalon and the brain stem, but not in the cortex. Effects of theophylline were reduced latency and maintained tendency to kill, even after overnight muricide test. The 5HT content of the amygdala decreased in bulbectomized rats. Discrepancy between brain 5HT changes and aggressive behavior were discussed.     

Immune responsiveness in offspring of adoptively immunized mothers

The rate of appearance of cells forming 19S hemolytic antibody (PFC) in the spleens of F1 newborn mice after adoptive anti-paternal immunization of fetuses, newborns and/or their mothers during pregnancy has been studied. An increase in the number of PFC was found at the age of 6 to 11 days in offspring of adoptively immunized mothers. These newborns, even when foster nursed by untreated mothers, still had a significantly higher number of PFC in comparison to the controls. In contrast, adoptive immunization of the newborns themselves resulted in a decrease of PFC during the second week after birth. Several possible explanations for the obtained results are discussed including the putative transplacental passage of immunocompetent cells.     

Seizure susceptibility and avoidance conditioning in adult rats treated prenatally with chlorpromazine

Offspring of female rats treated early in gestation with chlorpromazine (CPZ) were tested at 30 days of age for seizure susceptibility and at 90 days of age for shock avoidance learning. Fostering procedures permitted separation of prenatal influences from postnatal rearing influences of drug treatment. Offspring of drug-treated mothers had higher avoidance scores, higher intertrial activity levels, and greater seizure susceptibility than offspring of controls. Animals reared by previously treated mothers also had higher avoidance and greater seizure susceptibility. This postnatal effect depended on sex and was not accompanied by an overall increase in intertrial activity. Rearing by a previously drug-treated mother was also found to modify the influence of neonatal stress on adult avoidance learning.     

Prenatal psychological stress effects on taste neophobia

Pregnant mothers were subjects to a novel environment, a treatment which is known to induce an 11-hydroxycorticosterone (stress) response, for 30 min daily for five successive days while control mothers were control handled. The novelty and control treatments were given to the pregnant mothers either during terms 1, 2 or 3 of pregnancy. After parturition, all offspring were fostered to neutral foster mothers. Testing for the neophobic taste response was carried out after the offspring were 90 days old. It was found that prenatally stressed animals responded with increased neophobia to a novel saccharin solution. Female offspring drank significantly more of the test solution than male offspring. The neophobic response appears to be an index of exploration. The neophobic response of prenatally treated rats was found to be in the opposite direction of postnatally treated rats. However, both findings follow similar response patterns of pre- and postnatal stressed rats tested in an open field.     

Antecedents of toddler aggression: dysfunctional parenting in mother-toddler dyads.

Aggression is stable as early as 2 years of age and predicts many negative adult outcomes. Although longitudinal predictors of child aggression have been identified, information is lacking regarding the proximal precursors of toddlers' aggression. During a 30-min interaction, 54 mother-toddler dyads were observed. Toddlers were categorized as aggressive or nonaggressive based on whether they exhibited aggression toward their mothers within the interaction. Most toddlers in both groups escalated from mild to more severe forms of misbehavior. Mothers of aggressive toddlers displayed more lax and over-reactive discipline when addressing misbehaviors that preceded aggression than did mothers of nonaggressive toddlers. Mothers of aggressive toddlers either ignored or attended neutrally or positively to the aggression. Implications for parenting interventions are discussed.     

Mother - infant interactions: Effects of early handling of offspring on rat mothers' open-field behavior

Two experiments studied the open-field behaviors of rat mothers as a function of offspring manipulation. In the first experiment mothers whose offspring were “handled” were compared with mothers whose offspring were not handled. Mothers of handled offspring were found to be less emotional in the open field than control mothers. In the second experiment control litters and litters handled during their first week were fostered to mothers of nonhandled litters. The foster mothers and their new litters were not disturbed again until weaning 2 weeks later. Again, mothers which reared handled litters were less emotional than those which reared nonhandled litters. It was concluded that mothers are affected by early handling of their offspring, that the direction of influence can be from infant to mother, and that the effects of mother-infant interactions are likely to be extremely complex.