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Nongenomic transmission across generations of maternal behavior and stress responses in the rat.

In the rat, variations in maternal care appear to influence the development of behavioral and endocrine responses to stress in the offspring. The results of cross-fostering studies reported here provide evidence for (i) a causal relationship between maternal behavior and stress reactivity in the offspring and (ii) the transmission of such individual differences in maternal behavior from one generation of females to the next. Moreover, an environmental manipulation imposed during early development that alters maternal behavior can then affect the pattern of transmission in subsequent generations. Taken together, these findings indicate that variations in maternal care can serve as the basis for a nongenomic behavioral transmission of individual differences in stress reactivity across generations.

Amygdala↗

Maternal behavior of wild and domestic Rattus norvegicus recorded continuously in dual-chambered cages.

Continuous measurements of maternal behavior--the amount of time the mother was in contact with the litter and quality of nest--indicated no differences between these 2 stocks of rats. A decrease in both measures was found for both stocks over the 22 days of postnatal observation. The data indicated that the mother was with the litter more during the light portion of the 24-hr light-dark cycle and that wild rat mothers were in contact with their litters more than domestic mothers in the period around light offset.

Animal Population Groups↗

Olfactory regulation of maternal behavior in mammals.

In mammals, olfactory cues are extensively used in many aspects of maternal care to ensure the coordination of mother-infant interactions and consequently the normal development of the offspring. Outside the period of parturition and lactation, when the young are not a behavioral priority, olfactory cues play an inhibitory role on maternal responsiveness since in most mammalian species studied so far, nonpregnant females find the odor of young aversive. On the contrary at the time of parturition, a shift in the hedonic value of infantile odors occurs so that the young now become a very potent stimulus and this sensorial processing constitutes an important part of the maternal motivational system. Moreover, infants' odors provide a basis for individual recognition by their mothers and some species (ungulates) have developed highly specialized mechanisms for processing of the infant signals. Perception of the smell of the young also regulates various aspects of maternal behavior. Dodecyl propionate, a compound released by of pup's preputial glands, has been shown to influence anogenital licking behavior, a fundamental pattern of maternal behavior in rodents. While there is no functional specificity of either the main or the accessory olfactory systems in the development of maternal behavior amongst species, it appears that only the main olfactory system is implicated when individual odor discrimination of the young is required. Neural structures, such as the main olfactory bulb, undergo profound changes when exposed to offspring odors at parturition. These changes in synaptic circuitry contribute both to maternal responsiveness to these odors, to their memorization, and to effects of long-term maternal experience.

Animals↗

Thermal constraints on maternal behavior during reproduction in dwarf hamsters (Phodopus).

The chronic hyperthermia of lactating dwarf hamster (Phodopus) dams may constrain maternal behavior if contact with the litter further increases their body temperature, forcing the termination of nest bouts to dissipate the heat load. Changes in female body temperature and nest attendance in two species of dwarf hamster (P. campbelli and P. sungorus) were recorded each minute over the reproductive cycle. As the pups develop from naked poikilotherms to well-insulated thermoregulators, they function as heat sinks and heat sources. This role of pup development in maternal thermoregulation interacts with the dam's activity, primarily nocturnal wheel running, to produce a complex pattern of heating and cooling in each species. Contact with the pups is more constrained by maternal temperature during the inactive phase (day), and more constrained in P. campbelli than in P. sungorus. The interspecific difference in pup development or maternal thermoregulation is consistent with predictions based on biparental care, and a thermoregulatory role for the male in P. campbelli, but not in P. sungorus. These data suggest that environmental temperature and water availability are ecological variables that affect maternal thermoregulation, reproductive success, and the need for biparental care.

Acclimatization↗

Maternal behavior variations and adaptations, and pup development within litters of various sizes in Wistar rat.

Variations of two maternal behavior components (time spent with litter and rapidity of pup retrieving) as well as certain physical and developmental characteristics of pups (weight, relative weight gain, and neuromotor maturation) in rats were simultaneously studied in 29 various-sized litters in which interindividual variations were not experimentally amplified. Results showed mothers' behavioral adaptations to litters' characteristics (size and weight). Time spent with young was linked to litter size, whereas rapidity of pup retrieving was related to the pups' physical characteristic. Beyond these adaptive variabilities, residual variations subsisted between mothers. These variations were determinant for differences in pup development for only one component: the time that mothers spent with their litters, while pup retrieving component variations did not have any effect.

Age Factors↗

Absence of maternal behavior in rats with lithium/pilocarpine seizure-induced brain damage: support of MacLean's triune brain theory.

Female rats, with and without maternal experience, received limbic seizure-inducing (SC) injections of lithium and pilocarpine. Following the subsequent parturitions, these rats displayed a complete absence of maternal behavior. Rats that did not display seizures after receiving the lithium/pilocarpine injections displayed behaviors that were comparable to normal controls. Although the multifocal limbic, thalamic, and cingulate damage abolished maternal care, there was no evidence of aberrant effects upon fecundity, litter size, or mammary function; infanticide was negligible. The pattern of brain damage involves the evolutionarily more recent thalamocingulate system of mammals and supports MacLean's theory that these pathways are required for normal mother-offspring interaction.

Animals↗

Bicuculline infusion into the accessory olfactory bulb facilitates the induction of maternal behavior in rats.

The GABAA antagonist bicuculline, intracranially infused into the accessory olfactory bulb (AOB), facilitated the expression of maternal behavior (MB) in virgin Wistar female rats. Behavioral effects were observed 24 hours after infusion and were injection dependent. Pheromonal stimuli, generated by the pups, are thought to exert an inhibitory effect on vomeronasal nuclei involved in MB in virgin rats. The present study investigated the possibility that a decrement in AOB output, resulting from long-term compensatory synaptic changes to chronic bicuculline infusion, would facilitate the expression of MB. The implications of our findings for the mechanisms involved in the induction of MB and the maternal experience effect are discussed.

Animals↗

Effects of acute hypergravity exposure and parity on maternal behavior in CD-1 mice.

We assessed the behavioral response to acute hypergravity exposure in lactating mother mice, Mus musculus of the outbred CD-1 strain. Primiparous or terziparous dams were exposed with their litters to a centrifugal force equivalent to 2G hypergravity for 1 h daily from postnatal day 2 (P2) to P9. We made detailed behavioral observations before, during and after the rotation on selected days to identify elements of the maternal behavioral repertoire vulnerable to 2G challenge. Licking and nest building were reduced during rotation while mothers sniffed and snouted their pups more. Nursing and total time in physical contact with pups were relatively stable. The effects of rotation were most pronounced on P2, dams appearing to habituate to the treatment with repeated exposure. Dam parity had a limited effect on the behavioral response to rotation, primiparous mothers tending to spend longer nursing their pups during the rotation and showing a greater tendency to lick and nest-build in post-rotation. Differences between parity groups diminished over days. Body weight was decreased in rotated primiparous dams and their pups gained less weight than stationary controls. Ultrasonic vocalization (USV) rates recorded on P2, P5 and P9 seemed to indicate delayed behavioral development in rotated pups.

Animals↗

Phencyclidine: effects of chronic administration in the female mouse on gestation, maternal behavior, and the neonates.

Phencyclidine (PCP) (5 mg/kg) was administered daily throughout gestation and pups were crossfostered or fostered after birth. Prenatal weight gain, lenght of gestation, length of parturition, and the size and birth weight of the litters were not affected by PCP administration. No congenital malformations were evident and the mother's health during chronic exposure remained normal. Physical development of the pups (indicated by neonatal weight gain, pinna opening, and eye opening), and neurological development (indicated by the maturity of four reflex actions) were normal for the PCP pups. Behaviorally, PCP pups were slightly more active in the open field at 60 days. Maternal behavior was not influenced by drug treatment, but was affected by the fostering procedures.

Animals↗

Early experience and maternal behavior in rats.

This study examined the effects of early experience (early weaning with group housing in sibling groups (EG), or early weaning plus social isolation (EI) from 14 to 24 days of age) on maternal, play, and social behaviors expressed during 5 days of sensitization at 24 days, and then later at 100 days of age. Our results showed that maternal behaviors at 24 days could be altered by these early experiences. At 24 days of age fewer EI animals retrieved compared with normally weaned controls (NW), but more showed play behavior in the presence of pups. EG animals showed intermediate levels of retrieving relative to NW controls, and no concomitant changes in play behaviors. When retested as adults, females in all groups showed similar levels of all maternal behaviors. But EI adults of both sexes showed persistent intrusion of play behaviors, and higher levels of rearing and undirected activity in the presence of neonates. Factor analyses revealed that previously sensitized adult males showed patterns of organization of maternal behaviors that resembled adult females rather than those shown by control males reared without sensitization experience. Previously sensitized females also showed a retention of the play behavior patterns characteristic of juveniles, not present in females without sensitization experience. These results show that social experience during the weaning period can affect the development of maternal and play behavior elicited by neonates during the juvenile period that persist into adulthood, and the juvenile sensitization experience exerts longterm effects on adult patterns of maternal behavior in both sexes.

Animals↗

Intrauterine repair of a lesion resembling cleft lip and its effect on maternal behavior in rats.

Two studies were done to determine the ideal day to perform an intrauterine procedure and to explore maternal behavior toward repaired cleft lip offspring rats. The first study showed that the best time to create a surgical cleft lesion was on the 19th day of pregnancy. Thus, for the second study rat fetuses were operated in utero on the 19th day of gestation, and the pups were delivered by cesarean section. One group was obtained with a lesion resembling cleft lip and a second group with repair of such lesion. Nonoperated litter mates were used as a control group. Two animals of each type were placed inside a cage, and the order in which the mother retrieved them and carried them to the nest was noted. Statistical analysis showed that retrieving them was not at random. All controls and 14 out of 18 treated animals were retrieved, but only 4 out of 18 of the clefted group were retrieved.

Animals↗

Mouse vomeronasal organ: effects on chemosignal production and maternal behavior.

Adult male mice excrete a urinary chemosignal that accelerates puberty in females, whereas group-housed female mice excrete a urinary chemosignal that delays puberty in young females. We found that: (1) the excretion of the puberty-acceleration chemosignal by males persisted in the absence of the vomeronasal organs and (2) the puberty-delay chemosignal was not present in the urine of group-housed females whose vomeronasal organs had been surgically removed (VNX), but was present in the urine of group-housed females subjected to sham surgery (SHAM). These results suggest that in males, vomeronasal chemoreception does not affect the excretion of the puberty-acceleration chemosignal, but that in females, the vomeronasal organ receives chemosignals that influence the excretion of the puberty-delay chemosignal. Additionally, we found no difference between SHAM and VNX females in rates of conception, litter size, pup growth, pup recognition, or maternal behavior, indicating that normal maternal processes are expressed in the absence of an intact accessory olfactory system.

Animal Communication↗

Maternal behavior in cyclic and androgenized female rats: role of ovarian hormones.

A comparative study on the induction of maternal behavior (MB) in response to pups was carried out in cyclic and androgenized rats. Moreover, the effects of exposure to ovarian hormones on the induction of MB in response to pups were studied in cyclic and androgenized rats. A high percentage of androgenized and proestrus rats displayed MB after 48 hr of exposure to pups (87.9% and 87.5% respectively). Diestrus day-1 rats were significantly less maternal (37.5%). Ovariectomy did not impair MB in androgenized rats. High serum progesterone levels induced in androgenized rats by treatment with 10 I.U. of HCG (40 hours before pup presentation) or with progesterone silastic implants prevented the onset of MB. Ovariectomy performed 8 hours before HCG administration restored MB. When behavioral testing began 72 hours after HCG treatment, 75% of the rats were maternal 12 hr after exposure to pups. This rapid onset of MB in proestrus and androgenized rats appeared to be estrogen dependent. The presence of progesterone inhibited the maternal response of androgenized rats.

Animals↗

Oral bis(tri-n-butyltin) oxide in pregnant mice. I. Potential influence of maternal behavior on postnatal mortality.

Pregnant Swiss mice were treated with 0, 5, 10, 20, and 30 mg/kg body weight of bis(tri-n-butyltin) oxide (TBTO) on d 6-15 of gestation. At birth litters were normalized to eight pups, and postnatal evaluation of pup growth rate and behavioral observations of dams were carried out. Litters were sacrificed on postnatal days (pnd) 7, 14, and 21, to perform hematological analysis, in connection with another study. Dam weight gain was impaired in all the treated groups (except at the lowest dose level) in the late phase of gestation. A high incidence of anticipated or delayed parturitions, without any correlation with fetal mass, was observed in the treated groups. All the treated dams showed a significant increase in resorptions, and a decrease in body weight gain between gestational day (gd) 6 and pnd 1. At birth, only the 20 and 30 mg/kg dose groups showed reduced litter size and reduced pup weight. Body weight gain reduction of pups persisted in wk 1 of life only in the 10 and 20 mg/kg dose groups. In addition, the maternal weight trend was affected during the lactation period in the higher dose groups. Postnatal death rate and growth rate of treated pups were affected by an altered maternal behavior; pups, apparently viable and with normal weight, were found often scattered throughout the cage with signs of wounds, and the percentage of dams that had not built a nest increased in the 10, 20, and 30 mg/kg dose groups. Total absence of parental care was noted in many litters, and many infanticidal events were reported. Our results seem to confirm low TBTO embryofetotoxicity, and strongly support the assumption that TBTO's toxicity to the mother is much stronger than its embryo-fetotoxic potential. Most of the reproductive parameters examined in this study were unaffected in the low-dose group, while some indices, such as gestation length and maternal weight gain between gd 6 and pnd 1, were markedly altered also at the 5 mg/kg dose level and appear to be sensitive parameters in assessing maternal toxicity.

Administration, Oral↗

Oxytocin induction of short-latency maternal behavior in nulliparous, estrogen-primed female rats.

This study was designed to test whether intracerebroventricular (icv) administration of oxytocin can shorten the latency of estrogen-treated virgin rats to respond to foster pups with maternal care. A secondary goal was a description of the behavioral effects of icv oxytocin in rats. Forty-eight hours before pup presentation female rats (Sprague-Dawley strain, obtained from Zivic-Miller Laboratories, Inc.) with chronic lateral ventricle cannulae were ovariectomized and treated with 100 micrograms/kg body wt estradiol benzoate (EB). Immediately before pup presentation either 400 ng oxytocin or the normal saline vehicle was infused. A second control group of noncannulated animals received the same surgery, EB treatment, and behavior tests without any icv infusion. Maternal behavior was scored on a scale from 0 to 5, one point each being given for licking pups, carrying pups, grouping pups, crouching over pups, and nest building. At the end of 1 hr of pup exposure 65% of the oxytocin-infused animals received scores of 4 or 5, while only 25% of the control animals attained these scores. Maternal behavior appeared as a unit in both spontaneously maternal and oxytocin-treated animals, with fewer than 10% in either group receiving scores of 1, 2, or 3. The oxytocin group also spent significantly more time grooming. In a second experiment in which oxytocin or normal saline was administered icv to oil-treated animals, this grooming effect was shown to be estrogen independent while the induction of maternal behavior required prior treatment with estrogen. Finally, a slight, transient hyperthermic effect of oxytocin on body temperature was observed in this test paradigm. These data suggest a role for oxytocin, acting with estrogen, in the onset of maternal behavior in rats.

Animals↗

Maternal behavior in New Zealand white rabbits: quantification of somatic events, motor patterns, and steroid plasma levels.

Several parameters associated with maternal behavior were quantified under laboratory conditions in New Zealand white rabbits. Digging behavior appeared earliest (8-6 days prepartum), its decline preceding the onset of straw carrying (3-1 days prepartum). Hair pulling consummated the construction of the maternal nest. Food intake significantly decreased on days 2 and 1 prepartum. On parturition day, all females spent 300-500 s with the litter while, for the rest of lactation, nursing bouts lasted 199 +/- 7 s. Milk yield increased linearly up to lactation day 19, declining thereafter. Pup weight increased linearly throughout lactation despite the decline in milk yield. Plasma estradiol (E) levels did not significantly vary across pregnancy: 60 +/- 2 pg/ml (days 10-25) and 75 +/- 6 pg/ml (day 30). The testosterone (T) levels at these times were: 200 +/- 10 and 308 +/- 0.03 pg/ml, respectively. Testosterone significantly declined from pregnancy day 30 to lactation day 1 (202 +/- 0.02 pg/ml). Progesterone (P) levels significantly declined from pregnancy day 20 (9 +/- 1 ng/ml) onwards. Progesterone levels were negligible across lactation. Thus, mother rabbits display a sequence of motor patterns and somatic events correlated with changes in plasma levels of T and P against a background of E.

Animals↗

Effect of handling on maternal behavior following return of pups to the nest.

Handling rat pups during the 1st week after birth altered adult behavior in the open-field, whereas simply spearating the pups from their mothers during the same period produced differences in body weight at weaning. Observations of mother-infant interaction following pup treatment yielded different patterns of maternal behavior. Moreover, pups receiving early treatment were more active as adults in a novel environment and had a greater body weight at weaning. The quality of maternal care and the immediate effects of infantile stimulation on the mother-infant relation should be considered in specifying a mediating mechanism for the effects of early experience.

Age Factors↗