Protein malnutrition in the rat: its effects on maternal behavior and pup development

Repeated time-lapse photographic observations were used to examine the maternal behavior and pup development of female Holtzman rats maintained on either a low-protein (12% casein by weight) or a high-protein (25% casein) diet throughout the period of lactation. Dams fed the low-protein diet were observed to spend more time in the nesting area with their pups than dams fed the high-protein diet. Locomotor activity of the dams did not differ between the 2 groups. The behavioral development of the pups suckling the dams receiving the low-protein diet was markedly depressed as compared with the controls. Included in this latter observation were pup behaviors such as movement from the nesting area, feeding and drinking from available supplies, and rearing and climbing activity. The results indicate that feeding a low-protein diet to a lactating dam results in behavioral changes in both the dam and pups that tend to minimize the exposure of the pups to the immediate environment.     

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.     

The effects of paraventricular hypothalamic lesions on maternal behavior in rats

The present study was undertaken to determine whether the disruptive effects of knife cuts which sever the lateral connections of the medial preoptic area (MPOA) on maternal behavior are mediated by interfering with the output of the paraventricular hypothalamic nucleus (PVN). Postpartum rats received one of the following: Knife cuts severing the lateral connections of the MPOA; knife cuts severing the lateral connections of the PVN; radiofrequency lesions of the PVN; sham lesions or knife cuts. Only females that received knife cuts severing the lateral connections of the MPOA showed severe deficits in maternal behavior. These results indicate that the influence of the MPOA on maternal behavior is not mediated by the output of the PVN. Since the PVN is the major source of oxytocin input to other brain regions, these results also suggest that oxytocinergic neural pathways are not critical for postpartum maternal behavior. Another important finding was that females with MPOA knife cuts that did not retrieve their young were capable of hoarding candy, suggesting that the retrieval deficit was not the result of a general oral motor deficit.     

The effects of early rearing environments on maternal behavior in adult female rats

The purpose of this study was to determine the effect of presence of siblings and exposure to colony cues during early life on the onset of maternal behavior at 20 and 75 days of life, and on subsequent emotional behavior in juvenile and adult female rats. Different groups of animals were reared either with a large number or a small number of siblings (sibling factor), or in the colony room or in a room apart from other mothers with pups (colony factor). Animals were tested for latency (in days) to show maternal behavior at either 20 or 75 days of age, and for emotional behavior (using the open field apparatus) at either 20-40 or 80-100 days of age. Exposure to colony sensory cues significantly reduced latencies for pup retrieval and nest-building in adults, but not in juveniles. Exposure to a large number of siblings reduced the latencies, in both adults and juveniles, to nest build; in juveniles, to lie over 75% of the litter; and in adults, to adopt a nursing posture. Consistent with prior research, juveniles had longer latencies than adults for a number of pup-directed behaviors including: latency to become maternal, latency to retrieve pups, latency to adopt a lactating posture, latency to lick/genital lick, and latency to nest-build. In the emotionality tests, the young animals scored as less emotional than the adults, an effect which was further exaggerated by early colony exposure. Overall results indicated that manipulation of early rearing environments does have a significant positive effect on later responses to young pups by both juvenile and adult female rats.     

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.     

Induction of maternal behavior in rats: effects of pseudopregnancy termination and placenta-smeared pups

The onset of maternal behavior in Long-Evans rats was examined after pseudopregnancy (PsP) termination, both with and without exogenous estrogen administration, and in response to either clean or placenta-smeared stimulus pups. Natural (spontaneous) PsP termination was as effective in hastening the onset of maternal behavior as ovariectomy plus estrogen injection. If clean foster pups were presented as soon as pseudopregnancy terminated (first proestrus or cornified smear), maternal behavior was exhibited within 2 days; placenta-smeared foster pups presented at the same time elicited maternal behavior within 2 hr. The combination of initiating maternal-behavior testing immediately after the natural termination of pseudopregnancy and proffering placenta-smeared pups apparently simulates the hormonal milieu as well as the environmental cues present at parturition, noninvasively, producing optimal conditions for the rapid induction of maternal behavior.     

Effects of adrenalectomy on maternal behavior in rats

One week prior to mating, female rats were adrenalectomized or sham-operated and, immediately following parturition, each was given a foster litter of 10 newborn pups from a mother in the same group. Retrieving measures at the time of fostering revealed no significant differences between the 2 groups. Over 16 days of maternal behavior observations the adrenalectomized mothers spent more time in the nest, more time in an active suckling position, and tended to keep the pups in the nest over a longer period of time. These results provide evidence that a functioning adrenal is not necessary for the initiation or maintenance of maternal responsiveness in rats.     

The effects of protein malnutrition on the behavior of rats during the suckling period.

Observations of 2 groups of dams and their litters were made every 3 hr around the clock on Days 1-20 postpartum. The dams fed either an 8% or a 25% casein diet for 5 weeks before mating and during gestation and lactation. Dams on the low protein diet spent more time in the nest actively nursing their young than did high protein dams, and they exhibited no deficits in other maternal behaviors. Five of 11 kinds of behavior developed more slowly in the undernourished pups than in the well-nourished ones, but the developmental delays were no longer than a few days. Circadian fluctuations were apparent in all of the pups' activities during the 3rd postnatal week as well as in grooming and horizontal movement, 2 behaviors that were present earlier, by 6-10 days of age.     

Effects of adrenalectomy on maternal behavior in pregnancy-terminated rats

Latencies to the onset of maternal behavior were measured in 16 day pregnancy-terminated rats. Three conditions were tested and included hysterectomy-ovariectomy (HO) with testing beginning 24 hr after surgery and HO plus a concurrent subcutaneous injection of 5 μg/kg estradiol benzoate or hysterectomy only (H) with testing starting 48 hr post-operatively. Within each condition, one group was also adrenalectomized while another was sham-operated at the same time as HO or H. There were no differences in the distribution of latencies between the adrenalectomized and sham-operated controls in any of the conditions although a significantly greater percentage of the sham adrenalectomized H animals were maternal by Day 2 of testing. It was concluded that adrenal secretions are not essential for the onset of maternal behavior in pregnancy-terminated animals while they may add a facilitatory effect following H only.     

Protein malnutrition induced during gestation: its effect on pup development and maternal behavior.

Repeated time-lapse photographic observations were used to examine the ontogeny of behavioral development in prenatally malnourished rat pups following birth. Pups born to dams receiving a low protein diet (7% casein by weight) were fostered at birth to well-nourished dams and behavioral observations were made at 4-day intervals. Dams nursing gestationally malnourished pups were observed to spend more time in the nesting area with their pups towards the end of lactation. Moreover, the behavioral development (locomotion, feeding, and rearing and climbing activity) of gestationally malnourished offspring was depressed when compared to their controls. The results indicate that prenatal undernutrition alters the behavioral development of the offspring and maternal behavior of the dam in a manner which reduces the exposure of the pup to the immediate environment.     

Maternal memory in adult, nulliparous rats: effects of testing interval on the retention of maternal behavior

The retention of maternal behavior (i.e., maternal memory) was measured in adult, nulliparous rats induced to respond maternally by continuous exposure to foster pups. Specifically, the effects of the interval duration between the initial induction and the reinduction of maternal behavior were determined. Intact virgin rats were first exposed to foster young to induce maternal behavior. During the initial induction phase, females were required to be fully maternal on 2 consecutive test days. Animals were then assigned to one of three interval groups (10, 20, or 40 days). After being isolated from rat pups for these designated periods, females in each group were tested again for their latencies to induce maternal behavior. Whereas the initial median latencies to display full maternal behavior ranged from 4.5 to 5 days for each group, upon retesting, median latencies for each group declined to 1 to 4 days. The greatest reduction in latency was present in the 10-day group (80%), and the smallest reduction was detected in the 40-day group (20%). A significant negative linear correlation was found between test interval and percentage reduction in behavioral latency. Based upon this relationship and under these test conditions, "maternal memory" in the adult, nulliparous rat would be expected to be nondetectable after about an interval of 50 days between tests. The pattern of maternal memory acquisition and loss appears similar to that reported in parous animals. The present study highlights similarities and possible differences underlying the establishment of the retention of maternal behavior (i.e., maternal memory).     

Muscle morphology in infantile protein malnutrition

A study was made of the sartorius muscle in Jamaican infants dying of protein malnutrition. Total counts were made of muscle fibres and sub-sarcolemmal nuclei in transverse section and compared with controls.A striking pathology is found in severe cases. The muscle fibre is reduced to a size comparable with that of the foetus. Although there is a greatly increased concentration of cells, there is also degeneration and actual loss of fibres and of sub-sarcolemmal nuclei. The proportion of the area occupied by muscle bundles may be halved, and there is a marked relative increase in interstitial collagen.These changes profoundly affect the interpretation of the results of biochemical analysis.     

Long-term effects of postnatal undernutrition and maternal malnutrition on mouse cerebral cortex

Quantitative analysis of cellular densities as well as an estimate of the cortical volume and of its total cell population were performed on the cortex of postnatally undernourished mice (2--21 days) and on that of pups from malnourished mothers (gestation and lactation). Animals were followed until 180 days of age after more than 5 months of nutritional rehabilitation, and data were obtained at 10, 30, 60, and 180 days of age. The neuronal density was much higher in all cortical layers of the two experimental series, suggesting a delay in cortical maturation. Moreover, layers II, III, and IV were more delayed than layers I, V, and VI. Postnatal undernutrition had more severe effects than maternal malnutrition and the degree of recovery after a long rehabilitation was much less. The increase of the cortical volume was greatly reduced in postnatal undernutrition and to a lesser degree in maternal malnutrition. The total number of glial cells was also reduced more in postnatal undernutrition than in maternal malnutrition, but the total number of neurons was never smaller than in the controls.     

Effect of protein-calorie malnutrition on the development of social behavior in rats

The effect of early protein-calorie malnutrition on the development of social behavior was studied during the first weeks of postnatal life. Activity and social interaction were recorded in groups of young rats either in the rearing cage or in a novel enviornment. The malnourished group had a delayed development of social behavior and smaller number of social contacts in all tests. During the suckling period, the nutritionally deprived pups were also more dependent on the mother, showed no social grooming, but were also more aggressive. On the 49th day, the normal rats showed increased exploration of the social stimulus whereas the malnourished rats were markedly inhibited. Apparently, early nutritional deficiency altered the social structure of the litter and of all individuals from the beginning by disturbing behavior and interactions of all members of the “family”.     

Long-term effects of postnatal undernutrition and maternal malnutrition on mouse cerebral cortex

Summary Quantitative analysis of the dendritic branchings of pyramidal cells from layers V and III, as well as of the number of spines on their apical dendrites, were performed on the visual cortex of postnatally undernourished mice (2nd–21st day) and on that of pups from malnourished mothers (gestation and lactation). Animals were followed till 180 days of age after more than 5 months of nutritional rehabilitation, and data were obtained at 10, 15, 21, 30, 60, and 180 days of age. The increase and maturation of dendritic branchings and spines were much more reduced in postnatal undernutrition than in maternal malnutrition. Furthermore, permanent damage still remained at 180 days in postnatal undernutrition while almost no damage was statistically detectable after maternal malnutrition.     

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.     

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)     

A cross-fostering analysis of the effects of PCB 77 on the maternal behavior of rats

Polychlorinated biphenyls (PCBs) are environmental contaminants known to cause multiple behavioral and developmental problems in humans and animals. In rats, gestational exposure to the PCB congener 3, 4, 3', 4'-tetrachlorobiphenyl (PCB 77) affects the brain and behavior of the offspring as well as the maternal behavior of the dams. Whether the behavior of dams is affected by direct effects of the contaminant or indirectly by actions of the PCB on the developing offspring is not known. We investigated this question using a cross-fostering paradigm in which pregnant rats were exposed to either oil vehicle or 2 mg/kg of PCB 77 on gestational days 6 through 18, and then raised pups that had been exposed to either oil or PCB 77 during gestation. Maternal behavior was observed on postnatal days 1, 2, 4 and 6. Some of the effects on maternal behavior, including an increase in the frequency of nursing bouts and in the amount of maternal autogrooming, can be ascribed to prenatal exposure of the litters to the PCB. Other behavioral effects, including an increase in time on the nest and in the amount of pup grooming as well as a reduction in high-crouch nursing, appear to be due to both direct effects of the PCB on the dams and effects mediated by changes in the offspring. Our results show that exposure to PCB 77 can have complex effects on the behavioral interactions between the dams and their litters with a potential impact on the development of the offspring.     

Pregnancy duration and fetal number: Effects on maternal behavior in rats

It was shown previously that in rats postpartum mothers are much more likely than pup sensitized virgin mothers to retrieve pups from a T-maze extension of their home cage. In the present experiment, the physiological basis of this difference was explored further by inducing maternal behavior (retrieving, crouching, licking) following hysterectomy-ovariectomy on Days 21, 16, and 10 of pregnancy. In general, the longer the duration of pregnancy, the shorter the latency to become maternal and the greater the propensity to retrieve pups from the T-maze. An additional group of Day 16 pregnancy terminated rats carrying six or fewer fetuses were not impaired with respect to onset of maternal behavior compared to their large-litter counterparts, but only a small percentage of these females retrieved in the T-maze. These findings suggest that both the late pregnancy estrogen surge and progesterone withdrawal after its peak and sustained secretion enhance maternal responsiveness and that T-maze pup retrieval (but not onset latency) may be additionally affected by the level of placental hormones.     

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.