Nutritive and nonnutritive determinants of milk intake of suckling rats

In order to determine the factors that enhance milk intake during deprivation, albino rats 15, 20, and 25 days of age were subjected, for 8 hr, to one of the following regimens: (1) privation, that is, separation from the dam and food; (2) privation with a maternal, thelectomized female; (3) privation with a maternal female whose nipples had been surgically ligated; (4) separation from the dam and food but receiving three 2% body weight intragastric preloads of milk; (5) with a dam whose nipples had been ligated and receiving the same intragastric preloads as Group 4; and (6) nondeprived rats. Rats were then allowed 45 min to suckle an anesthetized dam that was induced to let down milk every 4 min by intravenous oxytocin infusion. Intake at Day 15 was reduced by the opportunity to suckle, independent of receiving a milk load. This same trend was apparent, although not as strong, among Day 20 rats. By Day 25, nonnutritive suckling during the privation period no longer attenuated milk intake, although preloads did, whether or not they were paired with nonnutritive suckling. Thus, suckling in albino rats becomes increasingly freed from oral demands and more responsive to the nutritive consequences.     

The role of intraoral and gastrointestinal cues in the control of sucking and milk consumption in rat pups

Nutritive deprivation, suckling deprivation, gastronintestinal fill, and milk availability contribute to the control of sucking (as measured by jaw-muscle electromyograph) and ingestion of milk (provided via a tongue cannula) in 11–13-day-old rat pups. Depriving pups of the opportunity to suckle reliably increases subsequent sucking and milk intake. Intraoral delivery of milk also increases sucking, regardless of whether or not pups are suckling-deprived. Gastrointestinal preloads have no effect on sucking if pups are not receiving milk, but reliably block the increase in sucking which accompanies milk delivery. Finally, milk delivered to the pup's mouth prior to a suckling opportunity can either enhance or attenuate subsequent sucking depending on whether pups are allowed to consume milk while suckling. In all cases, a particular mode of sucking (“rhythmic” sucking) is most affected by experimental manipulation, and appears to be an important component of the pup's ingestive behavior.     

Changes in appetitive behavior in weanling-age rats: transitions from suckling to feeding behavior

To help identify determinants of rat appetitive behavior during the weanling period, rat pups 17-32 days of age were studied in a Y-maze. One arm of the maze provided pups with the opportunity to suckle a lactating or nonlactating anesthetized female. The other arm always contained a familiar food, either liquid diet or ground laboratory chow. In some experiments the dam was separated from the food compartment by a thin gauze screen. In other tests maternal contact could be maintained in the feeding goal but suckling in that compartment was prevented by nipple involution. Age was the major determinant of choice, with more older animals choosing the food arm. Availability of maternal contact in the feeding compartment increased the percentage of rats that chose to feed by about 20% at all ages studied. Food quality, but not quantity, affected choice at each age, as did lactational status. Prior food, water, and maternal deprivation (2 or 24 hr) did not affect choice behavior at any age but did influence behavior in the goal box. These findings are discussed within the context of the changing demands faced by the rats during the weaning period.     

Enhanced ethanol intake in preweanling rats following exposure to ethanol in a nursing context

Several studies have confirmed that diet selection patterns of adult rats are at least partially estabilished as a result of early experiences with food-related stimuli present in the milk of a lactating female (e.g., Capretta & Rawls, 1974; Galef & Clark, 1972; Galef & Henderson 1972). The present experiments were designed to investigate whether preweanling rats would similarly modify their acceptance of an ethanol solution following exposure to this cue in a nursing context. In Experiment 1, 8-, 12-, and 16-day-old rats were given ethanol, delivered intraorally in compound with milk, while given the opportunity to suckle an anesthetized dam. Subsequent testing revealed that 12- and 16-day-old subjects evidenced enhanced intake of the ethanol relative to controls, while 8-day-olds did not. Finally, the oldest (16 days of age) subjects also expressed a conditioned aversion to the milk when tested 24 hr after conditioning and ethanol-ingestion testing. Experiment 2 demonstrated that the critical factor for ethanol conditioning was the opportunity to suckle, rather than the simultaneous presence of milk. Finally, the aversion to milk observed in Experiment 1 was shown to have resulted from long-delay learning, due to the ingestion of a sufficient dose of ethanol during testing to serve as an aversive unconditioned stimulus (Exp. 3) © 1993 John Wiley & Sons, Inc.     

Maternal contact inhibits pituitary-adrenal stress responses in preweanling rats

Three experiments examined psychological factors which inhibit pituitary-adrenal activity in 12-, 16-, and 20-day-old rats. Infant rats were placed in heated novel test arenas for 30 min--a treatment which increases corticosterone secretion--and were presented with different appetitive stimuli in order to determine whether these stimuli inhibit this increased hormone secretion. The first experiment was a factorial combination of two conditions: suckling an anesthetized dam and milk ingestion through an intraoral cannula. At all ages, suckling inhibited corticosterone secretion but milk ingestion did not, nor was there an interaction of these factors. In the second experiment, the importance of suckling was assessed by allowing pups' contact with an anesthetized dam either with or without the opportunity to suckle. At all ages, contact with suckling and contact alone were equally effective in inhibiting corticosterone secretion. The third experiment asked whether contact with a lactating female is necessary for pituitary-adrenal inhibition or whether more distal cues associated with lactation are sufficient. Pups were tested under one of four treatments formed by a 2(Lactating vs. Virgin Female) X 2(Contact vs. No Contact) factorial design. At all ages inhibition of corticosterone secretion occurred only in animals which were allowed contact with an anesthetized female. Lactating and virgin females were equally effective for the 12- and 16-day-old pups, but contact with a virgin female was less effective for the 20-day-old pups. These findings indicate that neuroendocrine mechanisms subserving inhibition of the pituitary-adrenal system exist during the preweanling period in the rat, and suggest the possibility of maternal regulation of this physiological system during development.     

Long-term alterations in the maternal behavior of neonatally undernourished rats

The effect of early food and sensory deprivation on the maternal responsiveness of female rats was investigated. Animals that were neonatally undernourished by daily mother-litter separation (involving both food and sensory deprivation) showed significant deficits in maternal care, consisting of a reduction in nest rating, nursing time, and retrieving responses. Moreover, they exhibited exaggerated grooming and circling movements in comparison with the controls. Dams neonatally undernourished by the nipple-ligation of their mothers (a method that minimizes sensory deprivation) displayed less alterations in maternal behavior, and no significant differences in grooming and circling from the controls. The data suggest that nest rating, nursing time, and retrieving latency are closely related to food restriction, while the frequency of grooming and circling behavior are primarily associated with sensory deprivation. These results support the view that environmental influences related to food intake and sensory stimulation, interacting at critical stages of brain development, are essential for the maturation of adult behavioral patterns.     

The ontogeny of nipple-shifting behavior in albino rats: Mechanisms of control and possible significance

Nipple-shifting behavior was studied in rats 3–-30 days old in 4 experimental paradigms. The incidence of nipple-shifting of rats tested in groups of 3 on their nonlactating, anesthetized mother was age-related. Rats 12 days of age and younger did not leave the nipple first suckled during the 2-hr test period. Starting by Day 15, however, nipple-shifting increased and reached its maximum in 24-day-old rats. This behavior's incidence was directly related to maternal (and, therefore, nutrient and water) deprivation (Experiment I). Milk letdown reduced the incidence of nipple-shifting behavior at all ages studied and synchronized its occurrence, as almost all shifts occurred immediately after letdown and almost none during the 15-min interval between successive milk letdowns (Experiment II). Testing rats individually on the nonlactating, anesthetized mother produced age-related effects. Shifting was virtually eliminated in 15-day-old rats, markedly reduced in 21-day-old rats, and not affected in 27-day-old rats tested individually (Experiment III). Rats 27 and 30 days of age, upon leaving a nipple, ate and did not return to suckle. Rats 15 days old never ate and always returned to suckle (Experiment IV). Twenty-one-day-old rats suckled, and many ate in the mother's presence. The significance of these findings relates to maximizing milk intake and facilitating the process of weaning.     

The capacity to develop maternal behavior is enhanced during aging in rats

The induction of maternal behavior (MB) in response to stimulation by pups was studied in aged rats (19-20 months old). We used virgin female rats, neonatally androgenized female rats and male rats. Both groups of female rats showed a constant estrous vaginal smear. Maternal responsiveness was compared with that of young rats (3-4 months old). Normal and androgenized female aged rats showed a very high percentage of immediate maternal responsiveness and 100% of the rats were fully maternal within 24 hr of testing. The percentage of cyclic and androgenized young rats showing MB were significantly lower. Chronic ovariectomy performed 17 months before testing but not acute ovariectomy abolished MB. Estrogen treatment (5 micrograms 15 hours before pup presentation) to chronically ovariectomized aged rats was not sufficient to reestablish significantly the capacity of the normal female aged rats to become short-latency maternal. Young and aged male rats showed no difference in maternal responsiveness to the presence of foster pups. The percentage of maternal aged male rats was significantly lower than that of the normal and androgenized aged female rats, whereas young male and female rats showed a similar level of MB, indicating a sex difference in the development of MB with age. In conclusion the high percentage of rats becoming maternal and the short-latency maternal responsiveness in aged female rats appears to be the result of a prolonged estrogen and/or prolactin stimulation.     

Absence of behavioral deficits following neonatal undernutrition in the rat

Previous studies of the effects of early undernutrition on behavior in adult rats have confounded underfeeding with maternal deprivation or membership in a large litter. In the present experiment food-deprived rats received full-time maternal care and lived in the same-sized litters as well-fed controls. In contrast to previous findings food-deprived animals in the present study did not differ from controls in the open-field test, in a test of motor coordination, and in 2 learning tasks. However, food-deprived animals were more active than controls in a residential plus maze. Females showed less effect of food deprivation on body growth, but a much greater effect on activity, than males. These findings suggest that early undernutrition when not confounded with social and maternal deprivation may have more restricted effects on adult behavior than has been previously believed.     

Tail-pinch facilitates onset of maternal behavior in rats

Previous reports indicated that non-maternal female rats display a component of maternal behavior, namely, ano-genital licking of pups during, but not after a mild tail-pinch. The present study extends these findings and demonstrates that intermittent applications of brief tail-pinches accelerate in a dose-dependent pattern, the onset of all components of pup-stimulated maternal behavior in virgins. This suggests that the behavioral effects of tail-pinch stimulation outlast the pinch period and are cumulative.     

Olfactory influences on the ingestive behavior of infant rats

Twenty-four-hour deprived infant rats from 1 to 12 days of age were exposed to the odor of milk, either by itself or accompanied by oral infusions of water, sucrose, quinine, or milk (Experiment 1). Pups from 3 to 9 days of age became behaviorally active, and mouthed and probed in response to the odor of milk, even in the absence of oral infusions. Six- and 9-day-old pups also increased their intake of various test solutions in the presence of milk odor. This responsiveness to milk odor was not seen in 1-day-old pups, and waned by 12 days of age. Other stimulus odors that were presented in the same context (Experiment 2) failed to elicit such intense behavioral activation, indicating that there was some degree of specificity in the responsiveness to milk odor. Finally, 2 manipulations that influence pups' ingestion of milk, deprivation and ambient temperature, were found to influence pups' responses to milk odor (Experiment 3).     

Effect of maternal deprivation on milk intake in normal and bilaterally facial nerve-injured developing rats

We examined effect of maternal deprivation (2, 4 and 6h) on milk intake in developing rats. Milk intake was obtained by body weight gain after 1h lactation. The amounts of milk intake significantly differed depending on the duration of the deprived periods at P7 and P14 with proportional increase by longer deprivation. Further, milk intake was measured in the bilaterally facial nerve-injured neonatal rats. The results show that milk intake is increased during development affected by maternal deprivation, and that milk intake of the facial nerve-injured group is decreased by 35% (2h), 7% (4h) and 7% (6h) at P7, and 25% (2h), 20% (4h) and 27% (6h) at P14 compared to that of the control group.     

Determinants of suckling versus drinking in weanling albino rats: Influence of hydrational state and maternal contact

Preferences of weanling albino rats (15, 20, and 25 days of age) for nonnutritive suckling or drinking were determined using a Y-maze. Age, hydrational state, and the opportunity to contact the mother all influenced choice behavior. When tested in a maze that allowed continuous maternal contact in the “drinking-goal box,” dehydrated rats chose to drink, while nondehydrated rats chose to suckle. Testing dehydrated rats in a maze that precluded maternal contact in the “drinking-goal box” eliminated drinking preference at all ages. These observations identify maternal presence as an important condition for the expression of drinking behavior during the weaning period and confirm our previous demonstration of dehydration's inhibition of suckling behavior.     

Maternal deprivation potentiates pituitary-adrenal stress responses in infant rats

In three experiments we examined the effect of maternal deprivation on the pituitary-adrenal response of 12-, 16- and 20-day-old rat pups to novelty stress. Infant rats were either deprived individually in heated incubators or left in the home nest with their mother and then tested for their corticosteroid response to 30-min exposure to a novel test arena (novelty-stress). In Experiment 1 we showed that the magnitude of the stress response was a positively accelerated function of the deprivation interval. Stress responses were not increased after 1 hour of deprivation, were modestly increased after 8 hours of deprivation, and were dramatically increased after 24 hours of deprivation. In Experiment 2 we asked whether potentiation of the stress response resulted from the maternal or the nutritive components of the deprivation procedure. Pups were tested under one of four treatment conditions formed by a 2 (Maternally Deprived vs. Nondeprived) x 2 (Nutritively Deprived vs. Nondeprived) factorial design. At 12 and 16 days of age, potentiation of the stress response was traced to the absence of maternal care and not nutrients. At 20 days of age, both maternal and nutritive deprivation contributed to the potentiated stress response. The results of Experiment 3 showed that this effect was mediated, at least in part, by increased adrenocortical sensitivity to ACTH, because the corticosteroid response to exogenous ACTH administration was also increased by maternal deprivation. These findings add to a growing body of literature that supports the concept of maternal regulation of infant physiology. They also support previous reports from this laboratory indicating that suppression of the pituitary-adrenal system is modulated by maternal variables during the preweaning period in the rat.     

Effects of neonatal maternal deprivation and postweaning environmental complexity on dendritic morphology of prefrontal pyramidal neurons in the rat

It has been reported that periodic maternal separation in rats leads to a variety of endure behavioral, neurochemical and microstructural sequelae associated with the pathophysiology of anxiety disorders. Since it has been proposed that these changes might be permanent, we examined whether environmental complexity aid to recover the structural dendritic impairment induced by neonatal maternal deprivation in the medial prefrontal cortex of the rat. In addition, the anxiety-like behavior was assessed in the elevated plus-maze. Repeated maternal separation between postnatal days 6-21 (3 hours daily) significantly reduced the dendritic material in layer II/III pyramidal neurons and induced anxiety-like behaviors in the elevated plus maze. Furthermore, environmental stimulation (twice a day, 1 h each) during 12 consecutive days (postnatal days 23-35) failed to recover the neuronal and behavioral disorders induced by neonatal maternal separation. The results demonstrated that (i) neonatal maternal separation severely altered pyramidal dendritic outgrowth in close association with anxiety-like behavior assessed in the elevated plus maze, and (ii) postweaning environmental complexity was unable to recover neither the prefrontocortical neuronal impairment nor the novelty-induced anxiety-like behavior triggered by early maternal deprivation.     

Long-lasting effects of neonatal stimulation on the behavior of rats

The present study aimed to analyze the effects of neonatal stimulation on species-specific behaviors (defensive reactions to a predator and social interactions) in adult male and female rats. Handling and an unpredictable sequence of aversive stimuli were applied to male and female pups from the 1st to the 10th day after delivery; behavioral inhibition, aggression, and sexual behavior were evaluated in adulthood. Results showed that either neonatal handling or aversive stimulation decreased behavioral inhibition in a novel and potentially harmful situation (open field with a predator) in both male and female rats and increased maternal aggressive behavior. Sexual behavior in both males and females decreased, which could affect reproductive capability. The results could cast doubts on the generalization of beneficial effects of neonatal stimulation on the behavior of adult rats.     

The early presence of food-oriented appetitive behavior in developing rats.

The appetitive behavior of 3- to 6-day-old rat pups was studied by testing their ability to direct their ingestive behavior to a restricted food source. We found that, from 3 days of age, pups were able to feed efficiently from such a source. More specifically, pups that were deprived of nutrition but not of maternal care as well as pups that were dehydrated ingested significantly more than nondeprived animals, and did so whether liquid diet was spread over the entire floor surface beneath them or restricted to a fraction of the floor surface. However, pups that had been nutritionally and maternally deprived were not able to direct their feeding. The general locomotor activation of pups in this latter group appeared to interfere with their ability to direct their behavior to the restricted source. These results indicate that from early ages, developing rats possess the appetitive competence to guide their behavior and suggest that previous findings of poorly directed behavior were a confound of the behavioral activation shown by pups tested in a state of maternal deprivation.     

Milk intakes of genetically obese (ob/ob) and lean mouse pups differ with enhanced milk supply

Although obese (C57Bl/6J, ob/ob) pups have greater avidity for nonnutritive suckling than leans as early as 15 days postpartum, previous research has not found differences in milk intake between ob/ob and lean mice during the preweaning period. Because ob/ob pups suckle longer than leans, their perseveration should enhance their opportunity to ingest milk if (a) maternal milk supply is not limited and (b) longer sucking durations reflect increased pup willingness to ingest milk. Accordingly, the present study was designed to evaluate the milk intake of ob/ob and lean pups when they had access to an enhanced supply of maternal milk. Intact litters of pups, from heterozygous lean (ob/+) parents, were randomly assigned to be tested at either 6, 12, or 18 days. Pups were neither dam- nor milk-deprived before being cross-fostered successively to milk-replete surrogate dams for 60 min each. Obese pups showed a greater percentage body weight gain (the index of milk intake) than leans did, with younger pups showing larger increments than 18-day-olds. Although early adiposity in ob/ob pups may not rely on increased intake in the single-dam, nest situation, these data emphasize an early predisposition to overeating in this mutant.     

Within-litter variation in maternal care received by individual pups correlates with adolescent social play behavior in male rats

Maternal care represents an essential environmental factor during the first post-natal week(s) of rodents and is known to have lasting consequences for neuronal structure, brain function as well as behavioral outcome later in life, including social functions and reward-related processes. Previous experiments have shown that the amount of maternal care received by individual pups varies substantially, even within one litter. During adolescence, mammals display high levels of social play behavior, a rewarding form of social interaction that is of great importance for social and cognitive development. In order to investigate how maternal care influences adaptive social behavior later in life, we here examined whether individual differences in maternal licking and grooming (%LG) received during the first postnatal week affect social play behavior during adolescence. We observed that %LG received by male rats early in life correlates positively with the frequency and duration of pouncing and pinning, the two most characteristic behavioral expressions of social play behavior in rats. The latency to engage in social exploration also correlated with %LG. In female rats we observed no correlation between %LG and any social parameter. The data indicate that subtle variations in maternal care received early in life influence social interactions in male adolescent rats. These changes in social play likely have repercussions for the social development of male rats, suggesting that maternal care can have both direct and indirect effects on the behavioral development of the offspring.     

Pre- and postpuberal medial preoptic area lesions and maternal behavior in the rat

The ability of female rats to express maternal behavior following pre- or postpuberally-administered lesions of the medial preoptic area (MPOA) was investigated. Female Sprague-Dawley rats were electrolytically or sham-lesioned at either 28-30 days of age or 65-70 days of age and housed together in groups of 6-8 in "enriched" environments. Subsequently, the animals were mated and moved to individual cages just prior to parturition. Indices of maternal proficiency included nest ratings, pup retrieval time, percentage of pups with milk in their stomachs, and percentage of pup mortality. All animals in which lesions had substantially damaged the MPOA demonstrated significant deficits in all indices. Age at which the lesion was administered had no effect. In contrast to the recovery of male sexual behavior that has been reported for rats following prepuberally administered MPOA lesions, no recovery of maternal behaviors was seen in this study. Reasons for this lack of recovery may include the greater complexity of physiological and behavioral processes involved in maternal behavior in comparison to the rather stereotypical response patterns of male sexual behavior.