Ultrasonic calls of bank vole pups isolated and exposed to cold or to nest odor

Bank vole pups produce ultrasounds when isolated from the nest, as other rodents do. The present study was intended to elucidate the possible interaction between the social stress of isolation from the mother and the physical stress of low ambient temperature during the nesting period. Although bank vole pups removed from nests and monitored at nest temperature vocalized at high frequency, the number and duration of signals increased at lower ambient temperature. In the tested voles it appears that exposure to cold was the most important stimulus of vocalization during the preweaning period. This effect can be enhanced by prolonged isolation from the mother, manifested as longer duration of calls. Moreover, vocalization was reduced not only by the odor from the home nest, but also by exposure to bedding of an alien lactating bank vole or even a lactating mouse fed the same diet. This suggests that the olfactory signals affecting the ultrasonic vocalization of bank vole pups probably are a mixture of volatile metabolites related to the physiological status and diet of rodent females. The reported experiments provide convincing evidence that the vocalization of bank vole pups is affected by isolation from the mother, by ambient temperature, and by olfactory signals released by lactating rodent females.     

Olfactory development in gerbil pups

In a 2-choice situation, Mongolian gerbil pups show a preference for home-cage bedding odor that appears during the 2nd postnatal week and is consistently high between Days 8 and 14. Pups show responses to certain nonanimal odors as early as Day 4, indicating that the motor capacity to orient to odors precedes the emergence of nest odor preference. Increases in pups' nest odor preference appear to parallel increases in the frequency of maternal nest-building, an activity which can eject pups from the nest. This coincidence suggests that olfaction helps displaced pups to return to their nests.     

Voluntary and involuntary maternal separation in guinea pig pups with mothers required to forage

Lactating guinea pigs required to leave a nest box to obtain food were observed to be separated from their pups almost 10% of the time on Days 13-15 postpartum. The duration of separation was greater in the dark than in the light, and was not different for mothers/litters exposed to low (LFD) versus high (HFD) foraging demand. Subsequently, LFD and HFD pups as well as pups reared under standard laboratory conditions (SLC) all exhibited vocalization and plasma cortisol responses to involuntary maternal separation. However, several effects of rearing were also observed. HFD pups vocalized less during separation and had higher resting cortisol levels than did SLC pups; LFD and HFD males spent less time in contact with the mother in a test cage than did SLC males. These effects are discussed in terms of the importance of the physical environment in shaping infant-mother interactions and the infant's perception of control.     

Anxiety, motor activation, and maternal-infant interactions in 5HT1B knockout mice.

This study describes the development of anxiety and motor activation in mice lacking the serotonin (5HT) 1B receptor and in wild type controls and characterizes their early mother-infant interactions. In the isolation-induced ultrasonic vocalization paradigm, 5HT1B knockout pups vocalized less and were hyperactive, rearing, jumping, and rolling more often than wild type pups. One week postpartum, 5HT1B knockout mothers spent 20% more of their time outside the nest and were also hyperactive, rearing and climbing to the edge of the cage more often than the wild type mothers. There were no genotype effects on pup retrieval. Knockout adults were less anxious in the elevated plus-maze, defecated less, and head-dipped more, although none of the standard measures of anxiety (time and entries in the open arms) were different. 5HT1B knockout mice of both sexes were hyperactive during both the light and the dark phases of the 24-hr cycle. Thus, 5HT1B knockout mice show reduced anxiety and are hyperactive throughout their life.     

Learned aversion to soiled bedding in male Mongolian gerbils

This study was designed to determine whether the conditioned aversion paradigm could be extended to aversion to soiled bedding in the male Mongolian gerbil. In Experiment 1, sixty subjects were exposed to a glass petri dish filled with soiled bedding placed in the center of a one-meter-square open field for two 5-min sessions 48 hours apart. Half of the subjects received an injection of lithium chloride immediately after session 1, while the rest received saline. The LiCl subjects learned to avoid the soiled bedding in session 2, as indicated by significantly longer latency to first approach and lower frequency of approach to the stimulus. Experiment 2 examined conditioned aversion to an empty petri dish. No aversion was formed, thus strengthening the argument that the gerbils were learning an aversion specific to soiled bedding. The research results demonstrate olfactory aversion of this type is possible in gerbils, and suggest that it may have an important influence on their social behavior.     

Olfactory preference for mother over home nest shavings by newborn rats

The developmental course and behavioral processes by which infant rats come to prefer one of two prominent natural odors within their rearing environment, those of their mother and home nest shavings, was studied. Pups as young as 4–5 days and as old as 9–10 days prefer their mother's odor over that of their home nest shavings in a two-choice test chamber; pups deprived overnight prior to testing express that preference more strongly than nondeprived littermates when the mother is awake, but not when anesthetized. Encountering maternal and shavings odors in a two-choice paradigm engages a behavioral sequence that progresses from arousal and active sampling of both odors during the establishment of preference to increased mouthing after the choice has been made. A .5°C thermal gradient augments the maternal preference response from 4–5 days of age on, and is necessary to it in 2-day-olds. One-day-old pups do not express a preference for their mothers in our test apparatus on the basis of odor even with the addition of a .5°C thermal gradient, suggesting that preference for the odor of mother over home shavings may be acquired between 1 and 2 days of age. © 1998 John Wiley & Sons, Inc. Dev Psychobiol 33: 5–20, 1998     

Effects of preweaning exposure to novel maternal odors on maternal responsiveness and selectivity in adulthood

We examined the effects of odor exposure in the nest on the offspring's subsequent adult responsivity to pups scented with the same odor or a different odor. It was hypothesized that animals receiving exposure to the odor in the nest would be more maternally responsive to pups scented with the (same) exposed odor than to unscented (water-scented) pups. In the first part of the study (Part A), Sprague-Dawley female rat pups (days 1-18 of age) either received exposure to an artificial lemon odor or to the natural (water) odor in the nest. In the second part of the study (Part B), rat pups were exposed daily to lemon or neutral odorants in an incubator at a distance from the mother and the nest. On day 21, animals received odor preference tests for lemon versus neutral pine bedding. On day 60, animals were mated and their pups were removed at 15-min intervals at the time of parturition. Animals were then tested for maternal behavior to foster pups on day 1 or 7 after parturition. Foster pups were scented either with the lemon odor or with water (unscented). Early exposure to lemon in the nest context enhanced animals' attraction to the lemon odor in juvenile tests. In adult maternal tests, exposure to odor on the mother and in the nest had two effects. It increased the latency for animals to express maternal behavior; however, once mothers expressed maternal behavior, they spent more time licking and crouching over pups scented with the same odorant to which they had been exposed earlier on their own mothers. Simple exposure to the lemon odorant out of context of the nest had no effect on adult maternal latencies or behavior.     

Thermoregulatory development in pups of the subterranean rodent Ctenomys talarum

The effect of the mother's contact and huddling with nest mates on the mass-specific metabolic rate (RMR) and body temperature (T(b)) of pups of Ctenomys talarum from 2 to 45 days of age was evaluated at ambient temperatures (T(a)) within and below the adult thermoneutrality range (25 and 19 degrees C, respectively, the latter corresponding to the one recorded in burrows during the spring, when pups are born). Under these conditions, we recorded the percentage of time that pups spent huddled with nest mates, with their mother and suckling. At 19 degrees C, huddling and contact with the mother significantly reduced pups' body heat loss until they were 15 days old but did not affect their RMR. Fifteen-day-old pups showed an increase in their RMR, associated with the onset of independent thermoregulation. Pups older than 15 days showed a less variable T(b) and their RMR decreased. 2- to 30-day-old pups spent 80% of the time in contact with their mother and, when she was absent, they spent 70% of the time huddled with their nest mates. However, these results did not differ between the two T(a) evaluated. Forty-five-day-old pups reached adult T(b) and spent significantly less time in contact with their mother and nest mates. Huddling did not have a significant effect on energy expenditure of young tuco-tucos, being this related to the stable thermal conditions found in natural burrows and pups' mode of development.     

Morphine treatment and reproductive condition alter olfactory preferences for pup and adult male odors in female rats

Administration of morphine sulfate (MS) to pregnancy-terminated and postpartum lactating female rats disrupts both maternal behavior and postpartum aggression. Since the display of these behaviors may be heavily dependent on olfactory cues provided by the stimulus animals (rat pups and adult male rats, respectively), we examined whether MS was affecting the perception of the olfactory stimuli, and whether olfactory perception was modified by reproductive condition. In Experiment 1, lactating rats had their pups removed and were injected with MS (5.0 mg/kg, sc.) or saline. 60 min later they were placed into a two-choice apparatus, one side of which contained bedding soiled by neonates and the other clean bedding. Time spent on each side was recorded for a total of 5 min (300 s; chance = 150 s). Saline-treated mothers spent significantly more time on the pup-odor side, whereas MS-treated females spent significantly less. In Experiment 2, lactating females were treated with MS or saline and exposed to male odors (soiled bedding). MS significantly increased time spent on the side with male odors; when treated with saline, time spent was significantly reduced. Thus, in lactating rats. MS creates an aversion for pup odors while reducing the female's normal aversion toward male odors. In Experiment 3, ovariectomized (ovx) virgin females expressed neither an aversion nor a preference for the odor of pups following saline administration. After MS treatment, however, the virgins showed a distinct preference for pup odors. When exposed to male odors in Experiment 4 ovx virgins showed a marked preference for male odors after MS treatment, and neither a preference nor an aversion after saline. Experiment 5 examined pup odor preferences in intact virgins, early (Day 7), middle (Day 14), late-pregnant (Day 21), and prepartum (Day 22) rats. The pup odor preferences of virgin, Day 7, Day 14, and Day 21 pregnant rats were not different and generally were at chance levels. Day 22 pregnant females exhibited a marked preference for pup odors compared to chance levels, as well as compared to the other four groups. These findings suggest that opiates and endogenous opioids may regulate olfactory preferences and that alterations in this system may underlie normal behavioral changes toward conspecifics prepartum as well as during lactation.     

Stimuli from pups of adrenalectomized and malnourished female rats

The present study was designed to examine the effects of maternal adrenalectomy on pup cues. In Experiment 1, pituitary-adrenal activity of test mothers was differentially affected by cues from handled and shocked pups of adrenalectomized (ADX) and control (CON) mothers. The results suggest that the cues provided by pups of ADX mothers are less arousing to lactating females than are cues from pups of CON mothers. In Experiment 2, ultrasonic vocalizations in response to handling and shock were measured in pups of CON, ADX and malnourished (MAL) mothers. For all types of pups, shocking evoked more signaling than did handling on postnatal Days 8, 9 and 11. Pups of CON mothers showed a peak of vocalizations on Day 4. Pups of ADX and MAL mothers vocalized as frequently as did pups of CON mothers, but did not reach their peak of signaling until Day 11. This experiment demonstrates a retardation in the development of ultrasonic signaling in pups of ADX mothers. This effect appears to be due to the pup malnutrition that maternal adrenalectomy produces because pups of MAL mothers show a similar retardation.     

Potentiation and inhibition of ultrasonic vocalization of rat pups: Regulation by social cues

Eight- and 11- to 12-day-old rat pups were tested in isolation and in the presence of an anesthetized adult under cold conditions. Pups of both ages reduced rates of ultrasonic vocalization (USV) when an adult was placed into the test cage, independent of whether the adult was their dam or an unrelated male. However, afer removal of the dam, pups greatly increased their rates of USV over their first isolation period and in comparison with control pups. USV rates remained low after removal of the male. The temperature challenges faced by the pups in the two experimental conditions were the same. These phenomena are better explained by a hypothesis that postulates USV rate as being multiply determined, including by social cues, rather than a theory that considers thermal challenge only. © 1997 John Wiley & Sons, Inc. Dev Psychobiol 30: 195–200, 1997     

Temporal parameters of responsiveness to maternal pheromone in Acomys cahirinus

In a series of two-choice preference tests, 15-and 20-day-old A. cahirinus pups were found to prefer chemical cues produced by a lactating female over such cues emanating from a nonlactating female. Twenty-five-day-old pups, however, showed reliable preferences for bedding material soiled by a nonlactating female when paired against either lactating female-soiled bedding or clean bedding material. Although 25-day-old pups are no longer responsive to chemical stimuli produced by lactating females (maternal pheromone), 2-day-old pups are attracted to such cues emanating from lactating females as late as 35 and 38 days postpartum. Therefore, there does not appear to be close temporal synchrony between the waning of responsiveness to maternal pheromone and the production thereof.     

Maternal and paternal pheromones in gerbils

Mongolian gerbil pups are attracted to maternal and parental nest odors. They approach these odors in preference to the odors of either virgin females or clean bedding. The pups do not distinguish between maternal or parental odors and odors of unfamiliar lactating females. Thus lactating female gerbils produce a maternal pheromone similar to that of rats and other rodents. Attraction to the pheromone develops by two weeks of age and persists for at least three weeks. The primary source of the pheromone is the mother's enlarged ventral scent gland. Removing this gland eliminates maternal attractiveness. Development of attraction to maternal scent gland odors depends on prior exposure to them. Pups raised by mothers lacking scent glands do not approach lactating females that have scent glands. The father's presence during development alters the responses of gerbil pups to odors of other males. Pups raised by both parents avoid odors of other pairs with young, whereas pups raised by their mothers only do not. Pups are not attracted to their father's odors.     

Neonatal social isolation alters both maternal and pup behaviors in rats

The development of emotional behavior is dependent on the early experiences of the infant and the quality of maternal care. In these experiments, the effects of social isolation during the preweaning period on both pup behavior and maternal responsivity were examined. In the first study, the number of ultrasonic vocalizations (USVs) emitted after brief maternal separation was measured in neonatal rats with differing histories of social isolation. The social isolation procedure consisted of 5 days of daily separation from the dam and littermates for either 3 or 6 hr. At both ages tested, socially isolated pups vocalized significantly less than control pups. In the second study, the effects of prior isolation either daily for 5 previous days (Chronic Isolation) or for 4 hr prior to testing (Acute Isolation) were examined in a T-maze choice test. Pup vocalizations in the presence of the dam and dams' maternal behavior were assessed. When the dam was confined to the start box or during the maternal free access period, both Chronic and Acute Isolates vocalized less than pups that had never left the home nest. Dams spent more time with and licked and groomed more frequently and for a longer time both Chronic and Acute Isolates compared to pups that had always been with dams in the home nest. These results suggest that early isolation experience can alter subsequent responses to separation stress in neonatal rats and that maternal behavior is sensitive to the prior experiences of offspring.     

Maturation of olfactory exploration in golden hamsters

Following placement into a test cage filled with pine shavings, a litter of 7-8 golden hamster pups (aged 3-18 days postnatal: P3-18) initially displays a period of locomotion which ends reliably in huddling. The latency to establish a huddle (i.e., the duration of locomotion) is significantly longer in the presence of novel odors (fresh or lemon shavings) than more familiar odors (slightly soiled fresh or lemon shavings) but only in pups aged P12 or older. Pups aged P9 or younger do not locomote differentially in the presence of novel or familiar odors. This age difference represents the emergence of olfactory exploration in hamsters between P9 and P12. Exploration of novel odors interferes with initial attempts to establish a single huddle site by a litter, but does not preclude the ultimate aggregation of all pups at a single site as guided by conspecific odors and possibly thermotactile cues as well. Such shifts in the control of behavior by non-nest and nest-related, conspecific stimuli correspond well with the first occurrence of nest exits at P11-12 (e.g., Dieterlen, 1959) coupled with the persistent return of hamster pups to the maternal nest for as long as it is maintained (Rowell, 1961).     

Ultrasonic vocalizations and maternal-infant interactions in a rat model of fetal alcohol syndrome

When isolated from their dams and littermates, rat pups emit ultrasonic vocalizations to elicit attention and retrieval from their dams. This study examined the effects of perinatal alcohol exposure on ultrasonic vocalizations and maternal-infant interactions. Alcohol was administered throughout gestation to the dams and during the early postnatal period to the pups. Control groups consisted of a nontreated control and an intubated, pair-fed control. Ultrasonic vocalizations were measured on postnatal day (PD) 5 under varying conditions of isolation. Maternal behaviors were examined on PD2, 4, 6, 8, and 10. Maternal behaviors were not significantly affected by prior alcohol administration to either the dams or the pups. However, ethanol-exposed rat pups vocalized more on PD5 than controls regardless of condition. The heightened vocalization response of the ethanol-exposed pups might be an underlying factor in the persistent effects of perinatal ethanol exposure on social behavior.     

Sibling inhibition of hoarding in postweaning hamster pups (Mesocricetus auratus)

If hamster pups are placed in individual cages at weaning (21 days of age) they begin to hoard food immediately; within 2-6 days, they hoard 90% of the food they take from their food dish in the course of a 1-hr test, consuming only 10% of it. Pups that remain with their littermates after weaning in large group cages do not hoard food until they are placed in individual cages, when hoarding starts immediately. The inhibitory effect of littermates is just as pronounced in hamsters that have been allowed to hoard food in individual cages for 14 days after weaning and are then regrouped into litters. If litters are housed in divided cages that prevent physical interactions among littermates, but allow the interchange of olfactory, auditory, and some visual cues, hoarding is suppressed to an intermediate level. These results show that the presence of siblings inhibits the expression of hoarding, partly as a result of direct physical interactions and partly through the agency of sensory cues. The onset of hoarding following the dispersal of young from the nest cannot be explained as a motivational consequence of the young no longer having access to the mother's food hoard.     

Influence of the odorization of the rearing environment on the development of odor-guided behavior in rat pups

The study describes a phenomenon in which attraction of rat pups to artificial odors disappeared after the first week of life. In experiment 1, pups were continually exposed to either: (1) the normal odors present in the litter or (2) the same odors enriched with one of four artificial odors present in the dam's food. Pups were tested daily with the odors of normal or adulterated soiled shavings from their nests. The results show that attraction to the normal test shavings lasted throughout the testing period (PN 1-7). However, pups raised on odorized shavings exhibited an attraction to the artificial odor until day 6 only, not on day 7. In experiment 2, pups were tested with dam's artificially adulterated food. The results show that the artificial odor, and not the food odor, was responsible for the lack of attraction on day 7. Experiment 3 was carried out to determine whether the date on which attraction to artificial odors changed might be specific to postnatal day 7 or whether the duration of odor exposure in test conditions was the important factor. The results suggest that the age of pup is the more important variable.     

Factors influencing cortisol and behavioral responses to maternal separation in guinea pigs

Infant guinea pigs recently were found to respond to brief maternal separation with an increase in plasma cortisol levels. The present experiments were conducted to further characterize this response and compare it with the cortisol separation response previously observed in primates. In Experiment 1, separation of guinea pig pups from their mothers did not elevate the plasma cortisol levels of the pups at either 30 or 180 min when they remained alone in their home cages during the separation. Experiment 2 showed that cortisol levels of pups placed alone in a novel cage were greater at 30, 90, and 180 min than were those of pups placed in the cages together with their mothers. In contrast, the separated pups vocalized more than did pups tested with their mothers during the initial 30 min only. In Experiment 3, pups raised on inanimate surrogates responded less intensely to rearing-figure separation in terms of both cortisol and vocalizations than did mother-reared controls. Taken together, these results indicate both differences (response to home cage separation) and similarities (dissociation of cortisol and vocalization responses, effect of surrogate separation) in the separation responses of guinea pig and primate infants. The guinea pig model may provide a useful adjunct to primate studies for examining particular issues concerning physiological effects of brief separation from an attachment object.     

Maternal pheromone in the spiny mouse (Acomys cahirinus)

One day old spiny-mouse pups (Acomys cahirinus) were found to prefer bedding material which had been soiled by a 3–5 day postpartum lactating female to bedding soiled by an adult male or litter of conspecific neonates. Further tests indicate that pups are still attracted to bedding soiled by a 27–30 day postpartum female providing that the female is lactating and has been allowed to interact with her preweanling offspring. Production of the maternal pheromone in Acomys c. may therefore be mediated by the hormone(s) which controls lactation, and the prolonged emission of this pheromone appears to be related to the communal mothering shown by group housed animals.