Mother-young Contact Research Articles

Progressive weaning alters behaviour and biomarkers of stress in weaned lambs subjected to social isolation

The mother-young contact during suckling influences the development of the offspring and their stress-coping abilities. Progressive weaning reduces the stress response in lambs as the separation time increases gradually until permanent maternal deprivation. The aim of this study was to determine if repeated maternal deprivation in suckling lambs alters their behavioural, physiological and immunological responses to social isolation after weaning. Twenty-four Saint Croix single born-lambs remained with their mothers for their first 29 days of age. Thereafter, 12 lambs were temporarily separated from their mothers every day for 4 weeks, during 4 h/d the first week, increasing 4 h weekly until they were separated 16 h/day (progressive weaning group: PW). During the progressive separation, PW lambs were moved to an enclosed pen, where they did not have visual or olfactive communication with their mothers. The other 12 lambs remained in permanent contact with their mothers until the definitive separation of both groups at 61 days old (abrupt weaning group: AW). At day 90 of age, all lambs were individually isolated for 10 min in a novel place, alternating one lamb from each group. Lambs’ behaviour was video recorded during the test. Cortisol concentration and haematological measurements were determined before and after the test. The PW lambs crossed more lines (P = 0.007), attempted to escape more times (P = 0.009), displayed more freezing behaviour (P = 0.01) and tended to vocalise more than AW lambs (P = 0.054). The AW lambs tended to sniff more times (P = 0.09) than the PW lambs. Cortisol concentration and the percentage of monocytes were lower in PW than in AW lambs (P ≤ 0.04). In conclusion, lambs repeatedly deprived of their mother displayed a more intensive behavioural response to social isolation one month after the definitive separation from their mothers. Progressive weaning reduced the cortisol concentration and the percentage of monocytes. These results call attention to the importance of further studies being undertaken in reference to the short and long-term effects of different procedures applied in order to better improve mother and the lamb welfare before artificial weaning.

Bidirectional Effects of Mother-Young Contact on the Maternal and Neonatal Brains.

Adaptive plasticity occurs intensely during the early postnatal period through processes like proliferation, migration, differentiation, synaptogenesis, myelination and apoptosis. Exposure to particular stimuli during this critical period has long-lasting effects on cognition, stress reactivity and behavior. Maternal care is the main source of social, sensory and chemical stimulation to the young and is, therefore, critical to "fine-tune" the offspring's neural development. Mothers providing a low quantity or quality of stimulation produce offspring that will exhibit reduced cognitive performance, impaired social affiliation and increased agonistic behaviors. Transgenerational transmission of such traits occurs epigenetically, i.e., through mechanisms like DNA methylation and post-translational modification of nucleosomal histones, processes that silence or increase gene expression without affecting the DNA sequence. Reciprocally, providing maternal care profoundly affects the behavior, learning, memory and fine neuroanatomy of the adult female. Such effects are in many cases permanent and sometimes they involve the hormones of pregnancy and lactation. The above evidence supports the idea that the mother-young dyad exerts profound and permanent effects on the brains of both adult and developing organisms, respectively. Effects on the latter can be explained by the neural developmental processes taking place during the early postnatal period. In contrast, little is known about the mechanisms mediating the plasticity of the adult maternal brain. The bidirectional effects that mother and young exert on each other's brains exemplify a remarkable plasticity of this organ for organizing itself and provide an immense source of variability for adaptation and evolution in mammals.

Establishment of vocal communication and discrimination between ewes and their lamb in the first two days after parturition

In sheep, the mother-young relationship is characterized by an exclusive bond that relies on the rapid establishment of mutual recognition. However, the role of acoustic cues has been underestimated and neglected in this early discrimination. Therefore, the aim of the present study was (1) to characterize the vocal behavior of ewes and their lambs during the first 15 days postpartum and (2) to investigate the ability of newborn lambs and their mothers to discriminate each other from alien subjects within the first 48 hr postpartum on the basis of acoustic cues only. Ewes started to vocalize in the last 3 hr preceding parturition, emitting mainly high-pitched bleats. However, the bleating activity was highest during the first 3 hr following birth, consisting mainly of low-pitched bleats. Thereafter it decreased sharply until 24 hr postpartum, with most of the activity coming from the mother. In a two-choice test, ewes discriminated their own from an alien lamb on the basis of acoustic cues only at 24 hr postpartum, while lambs did so for their mother at 48 hr, which in both cases was much earlier than reported so far. We conclude that early vocal recognition between the ewe and her lamb may play an important role for the maintenance of mother-young contact.

Effects of restricted nursing on milk production and collection, kid growth and plasma prolactin and growth hormone concentrations in dairy goats

The milk production of dairy goats under various regimes of mother-young contact from day 4 post partum were studied during the first 2 months of lactation, together with the prolactin (PRL) and growth hormone (GH) responses to udder stimulation. In the control group, 13 goats and their kids were left in permanent contact and did not undergo milking. In two additional groups, goats were machine milked once a day in the morning (at 0800 h) and kids were allowed 10 hours (from 1000 to 2000 h; 10H group, n = 11) or 5 h (from 1000 to 2000 h; 5H group, n = 11) of mother-young interaction per day. In the last group (MO, n = 10), mothers were permanently separated from their kids on day 4 post partum and milked once a day. Milk production during a 24-h period at 37 days post partum performed by controlled nursing and weighing of the kids (groups with kids) or by two machine milking 12 h apart (milking only group) revealed a higher production in the three groups with some mother-young contact than in the MO group. Total milk collected by milking over the 2 months of the study did not differ between the three groups that underwent milking. Kid weights at 2 months were 3.4 to 4.8 kg. lighter in the groups that underwent milking than in the control group. Hormonal profiles were significantly affected by restricted mother-young contact, with highest pre-stimulation concentrations of PRL and GH in the 5H group. Restricting mother-young contact from the first week postpartum can permit an early collection of milk without major effects on kid growth, when compared with one daily milking in goats totally separated from their young.

Social recognition memory requires protein synthesis after reactivation.

Recent evidence indicates that reactivation of consolidated memories returns them to a protein-synthesis-dependent state called reconsolidation. The hypothesis that memories reconsolidate has never been assessed in social memory. The authors tested whether sheep (Ovis aries) mothers' memory of their lambs undergoes reconsolidation upon reactivation. After 7 days of mother-young contact, ewes were separated from their lambs for 8 hr, after which the lambs were reintroduced to their mothers for a 10-min reactivation session. Before reactivation, mothers received a subcutaneous injection of either the protein-synthesis inhibitor cycloheximide (CY, 1 mg/kg) or vehicle. Mothers' lamb memory was tested 1 hr (short-term memory [STM]) or 16 hr (long-term memory [LTM]) after reactivation. Mothers treated with CY exhibited intact STM but deficient LTM. CY injection without reactivation or before presentation of an alien lamb induced no deficit in LTM. CY-induced LTM deficit was alleviated by (a) introducing a reminder just before the LTM test, (b) extending mother-young contact, and (c) preventing suckling by the familiar lamb during reactivation. Thus, reconsolidation can be shown to exist in social memory, and some of its boundary conditions are discussed.

From birth to colostrum: early steps leading to lamb survival

New-born lambs have limited energy reserves and need a rapid access to colostrum to maintain homeothermy and survive. In addition to energy, colostrum provides immunoglobulins which ensure passive systemic immunity. Therefore, getting early access to the udder is essential for the neonate. The results from the literature reviewed here highlight the importance of the birth site as the location where the mutual bonding between the mother and her young takes place. Attraction to birth fluids by the periparturient ewe leads to intense licking of the lamb. Grooming not only dries, cleans and stimulates the newborn it also facilitates bonding through learning of its individual odour. Ewes having twins should ideally stay on the birth site for at least six hours in order to establish a strong bond with both lambs and favour lambs survival. However, primiparous ewes or ewes having high levels of emotivity are more likely to exhibit poor maternal behaviour. In addition, difficult parturition and weather conditions have an indirect effect on the behaviour of the mother and are other major causes of lamb death. On the lamb's side, rapid access to the udder and early suckling are extremely important. Delayed lactation or insufficient colostrum yield may be fatal especially since suckling has strong rewarding properties in the establishment of a preference for the mother, which in turn increases lamb survival. Insufficient access to the udder in mothers leaving the birth site too soon after parturition, especially in twin-bearing ewes, could also partly account for the high incidence of loss of mother-young contact and subsequent death in such lambs. Strategies to improve neonatal survival should be aimed at maximising lamb vigour, colostrum production, and mutual mother-young bonding through adequate feeding in late pregnancy and selection on behaviour.

Mapping of brain networks involved in consolidation of lamb recognition memory

In sheep, ewes at parturition are responsive to any newborn lamb, but within less than 1 h, mothers learn to recognize the odor of their lamb and restrict maternal care to their own offspring (maternal selectivity). In a first experiment, we investigated the long-term retention of maternal selectivity after various mother-young contact and separation durations. After 4 h of contact, 36 h of separation leads to a total loss of selectivity. Increasing contact duration to 7 days prior to this separation maintains selectivity. These data suggest that lamb memory after going through an initial labile state after parturition, is consolidated over time into a more stable long-term memory. Fos immunohistochemistry reveals that reintroduction of the lamb after 4 h of mother-young contact and 3 h of separation activates different maternal brain regions than reintroduction of the lamb after 7 days of mother-young contact and 3 h of separation. While the piriform cortex shows an enhanced activation at both times, a selective enhancement of activation is observed in the frontal medial and orbitofrontal cortices only after 7 days of mother-young contact. These data suggest that as consolidation occurs, the neurobiological networks sustaining lamb memory involve different structures.

Maternal experience influences the establishment of visual/auditory, but not olfactory recognition of the newborn lamb by ewes at parturition.

Maternal behavior in sheep is characterized by the rapid establishment of individual recognition of the lamb through the use of different sensory modalities. Olfactory recognition mediates acceptance at suckling whereas visual/auditory cues are involved in recognition from a distance. This study investigates (a) the timing of both types of recognition and (b) whether they can be influenced by maternal experience. Olfactory recognition was assessed at lambing, 30 min, 1, 2, or 4 hr postpartum by presenting successively an alien and the familiar lamb. Recognition at a distance was assessed at 6, 8, and 12 hr postpartum by using a two-choice test between the familiar and an alien lamb. A majority (33/51) of ewes showed selectivity at suckling as early as 30 min after parturition, and no differences due to maternal experience were observed. By contrast, in the two-choice recognition test, multiparous ewes showed a preference for their familiar lamb at 6 hr whereas primiparous mothers did so only after 24 hr of mother-young contact: The performance of biparous mothers was intermediate. Thus, both types of recognition can be rapidly established after parturition, and maternal experience has a differential effect on the dynamics of these learning processes.

Thermal control of mother–young contact revisited: Hyperthermic rats nurse normally

Morphine (MOR) is known to inhibit maternal behavior and induce hyperthermia; at appropriate doses, concurrent administration of naloxone (NAL) counteracts its disruption of maternal behavior but not the hyperthermia. We used these findings to evaluate the view that lactating rats terminate nursing due to intolerable hyperthermia. After a dam–litter separation of 4 h on Day 7 postpartum (PP), mother–litter interactions were observed continuously for 1 h. One hour before reunion, the dams received two injections (1 ml/kg ip each) of saline (SAL), MOR (20 mg/kg) and/or NAL (1 mg/kg) in the following combinations ( n=7 each): SAL+SAL, SAL+NAL, MOR+SAL or MOR+NAL. MOR profoundly disrupted maternal behavior, thereby preventing litter weight gains; these effects were completely counteracted by NAL, which alone had no discernible effects. In contrast, MOR-induced hyperthermia (∼0.7 °C increase in each hour, before and after reunion with pups) was not antagonized by NAL at the doses used. Thus, an additional 0.7–1.4 °C of body temperature (T) did not delay the onset or reduce the duration of nursing compared with SAL-treated controls. Further, there were no group differences in behaviors displayed both shortly before and after a nursing bout that included milk ejections or in the resumption of nursing. Together with earlier methodological and empirical criticisms of the thermal control theory, as well as knowledge about the somatosensory determinants of nursing, the present results suggest that nursing bouts in lactating rats are not limited by the mother's T.

Extensive immunolesions of basal forebrain cholinergic system impair offspring recognition in sheep

The involvement of the basal forebrain cholinergic system has been extensively investigated in instrumental learning but little is known of its participation in social memory, especially in the memorization of individual traits of a conspecific. The present study tested in sheep its contribution to both instrumental learning and individual offspring recognition. Six weeks before parturition, ewes received injections of a specific cholinergic immunotoxin (ME20.4 IgG-saporin) into the lateral ventricles (150 μg) and in some cases additional immunotoxin injections into the nucleus basalis (11 μg/side). After 3 weeks of recovery, ewes were trained on a classical instrumental visual discrimination task known to be sensitive to cholinergic deficits. The formation of memory of offspring was assessed through both olfactory and visual/auditory recognition tasks. Olfactory recognition was tested by presenting at suckling successively an alien and the familiar lamb at 2 and 4 h after parturition. Visual/auditory recognition of the lamb was performed using a non-olfactory discrimination test between the familiar and an alien lamb after 12 h of mother–young contact. The lesion extent was assessed by counting choline acetyltransferase-immunopositive neurons in the basal forebrain and measuring the density of acetylcholinesterase fibers in different target areas. Results showed that immunotoxic lesions delayed acquisition of the instrumental visual discrimination. Moreover, olfactory recognition of the lamb was severely impaired while visual/auditory lamb recognition was marginally altered. There was no evidence for sensorimotor or motivational deficits. Importantly, impairment was observed in animals for which loss of basal forebrain cholinergic neurons and their efferent fibers was higher than 75%, while striatal cholinergic neurons and Purkinje cells were unaffected. This study provides evidence that the basal forebrain cholinergic system contributes not only to instrumental but also to social learning. In addition, the cholinergic modulation seems of importance for processing visual and olfactory modalities. However, since only extensive lesions affect performance, this indicates that the basal forebrain cholinergic system possesses substantial reserve capacity to sustain cognitive functions.

Postacquisition scopolamine treatments reveal the time course for the formation of lamb odor recognition memory in parturient ewes.

Institut National de Recherche Agronomique/Centre National de la Recherche Scientifique Within 4 hr after parturition, ewes learn to recognize the odor of their lamb. Whether scopolamine, a muscarinic antagonist, interferes with lamb odor retention was studied. After 4 hr of mother-young contact, ewes were separated from their lambs for 3 hr. During separation, they received intramuscular injections of saline, methylscopolamine (peripheral muscarinic antagonist), or scopolamine. Only scopolamine (100 microg/kg) prevented subsequent lamb recognition. To assess whether this effect depended on the duration of the learning phase, mothers remained with their lambs for 4, 8, or 16 hr before the 3-hr separation period and the scopolamine treatments. Ewes treated after 4 or 8 hr of contact displayed disturbed lamb recognition, whereas those having 16 hr of contact did not. Activation of central muscarinic receptors is therefore important for the formation of lamb odor recognition memory during a critical period of less than 16 hr postpartum.

Scopolamine impairs the ability of parturient ewes to learn to recognise their lambs.

Within a 4-h period after parturition, the ewe learns the odor of her lamb that will later allow recognition of her offspring from an alien lamb. This study investigated the involvement of the cholinergic system in this olfactory learning. At parturition and 2 h later, ewes received IM injections of saline (C group, n = 21), scopolamine methylbromide (METSCOP group, 100 micrograms/kg, n = 14) a peripherally acting muscarinic antagonist, a low dose of scopolamine hydrobromide (SCOP32 group, 32 micrograms/kg, n = 15) or a higher dose of scopolamine hydrobromide (SCOP100 group, 100 micrograms/kg, n = 18). Maternal behavior was observed at parturition and selective behavior was tested after 4 h of mother-young contact. No differences in maternal behavior at parturition were found between groups. By contrast, the proportion of ewes showing selectivity was significantly lower in the SCOP100 group (7/18) than in the METSCOP group (12/14, P = 0.01), SCOP32 group (12/15, P = 0.03), or C group (17/21, P = 0.01). In addition, saline-treated ewes, after having established their selective bond, received 100 micrograms/kg scopolamine and were again tested for selectivity 20 min later. Only one out of the 17 tested ewes failed to recognize their lambs after this treatment. These results indicate that intact central muscarinic transmission of the brain is required for the learning of individual lamb odor at parturition but not for the recall of this information.

Nursing behavior in rats is impaired in a small nestbox and with hyperthermic pups.

The supine nursing posture, which occurs increasingly as growing pups initiate nursing from their recumbent dam, was demonstrated to require more space than that provided in earlier studies of mother-young contact (e.g., Leon, Croskerry, & Smith, 1978). Further, hyperthermic rat pups were shown to be deficient in eliciting normal nursing behavior. During a 4-hr separation from their dam, 7-day-old rat pups were incubated at 34 degrees C (nest temperature) or at 39 degrees C (WARM). Compared to controls, WARM-litter dams showed increased licking of and hovering over pups and decreased upright crouching, while WARM litters showed decreased nipple attachment and weight gain. On Day 13, similar effects occurred after incubation at 39 degrees C (vs. 34 degrees C), but not at 36 or 38 degrees C. The results stress the need for ethologically meaningful conditions and direct behavioral observations to reveal the importance of pup activity in the mother-young dyad.

Olfaction mediates the establishment of selective bonding in goats

Nine pregnant goats of the Creole breed were rendered anosmic 3 weeks before parturition by irrigating their olfactory mucosa with zinc sulfate, and nine additional pregnant goats were left intact. At parturition, interactions between all females and their young were observed for 1 h. No differences were found in mother-young relationships between intact and anosmic mothers during this time, except that kids from anosmic females were slower to suck than controls. After 4 h of uninterrupted mother-young contact, mothers underwent three successive-5-min tests in a predetermined order to study selective bonding: with their own kid, an alien kid of similar coat color and pattern, and an alien kid of dissimilar coat color and pattern. Intact goats readily discriminated between kids, and rejected the two aliens while accepting their own. By contrast, anosmic mothers showed no signs of discrimination and accepted the three types of kids. It is concluded that during the first postpartum hours of contact, mother goats memorize individual olfactory characteristics of their kid that serve as a basis for selective suckling and exclusive bonding. Furthermore, at this early stage, visual characteristics of the young do not appear able to compensate for the loss of olfactory cues.

Early maternal discrimination of alien kids by post-parturient goats

Dwarf Creole goats ( n = 6) and mixed blood goats of dairy breeds ( n = 13) were tested for their ability to show selective care for their kids after post-partum mother-young contact ranging from 2.5 to 12 h (mean: 5.0 h). 18 out of 19 mothers were found to be selective and to reject alien young presented to them. Rejection was independent of the age of the alien (range: 3 to 28 h; mean 9.3 h) and of duration of mother-young contact prior to the test. Last we found that only one mother of multiple young ( n = 13) showed signs of recognition of litter size. Our results indicate that goat mothers can establish a selective bond as rapidly as sheep, and that they reject alien kids younger than the time necessary for the development of labelling as reported previously. Additional mechanisms may also be involved in the establishment of early maternal selectivity in goats.

Nest temperature: Effects on maternal behavior, pup development, and interactions with handling

These studies compared the patterns of mother-young contact under different thermal environments and assessed the implications of the differing patterns of contact for pup development and the dam's behavior. In the first experiment, the warm surface dramatically reduced the total amount of contact time between dams and litters and the dam's food intake, but the effects on the pups were limited to smaller adrenal glands. A replication of the first experiment in which daily weighing and handling of the pups was eliminated produced no differences in development. In a third experiment, during which dams had access to a warm surface outside of the next area and the daily weighing and handling was resumed, the pups showed smaller adrenal glands, lower body temperatures and less thermoregulatory ability. A comparison of results suggests that handling increased the weight of adrenal glands of pups reared under the unmanipulated condition, but not the warm-rearing condition.

Mammalian parenting: biochemical, neurobiological, and behavioral determinants

Norman A. Krasnegor: Biological and behavioral determinants of parenting in mammals: An introduction Part I. Four perspectives on parental behavior: Leon Eisenberg: The biosocial context of parenting in human families Martin Daly: Evolutionary theory and parental motives Jay S. Rosenblatt: Landmarks in the physiological study of maternal behavior with special reference to the rat Roger A. Gorski: Structural sexual dimorphisms in the brain: implications for parental behavior Part II. Biochemical correlates of parenting: Robert S. Bridges: Endocrine regulation of parenting behavior in rats Bruce B. Svare: Maternal aggression: hormonal, genetic, and developmental determinants Pascal Poindron, & Frederic Levy: Physiological, sensory, and experimental determinants of maternal behavior in sheep and goats C.L. Coe: Psychobiology of parental behavior in nonhuman primates Alison S. Fleming: Hormonal and experiential correlates of maternal responsiveness in human mothers Michelle P. Warren, & Barbara Shortle: Endocrine correlates of human parenting: a clinical perspective Part III. Neurobiological correlates of parenting: Michael Numan: Neural control of maternal behavior Thomas R. Insel: Oxytocin and maternal behavior E. Barry Keverne, & K.M. Kendrick: Neurochemical changes accompanying parturition and their significance for maternal behavior Barbara K. Modney, & Glenn I. Hatton: Motherhood modifies magnocellular neuronal interrelationships in functionally meaningful ways C.E. Grosvenor, G.V. Shah, & W.R. Crowley: Role of neurogenic stimuli and milk production in the regulation of prolactin secretion during lactation Part IV. Biobehavioral correlatesof parenting: Craig H. Kinsley: Prenatal and postnatal influences upon parental behavior in rodents Susan A. Brunelli, & Myron A. Hofer: Parental behavior in juvenile rats: environmental and biological determinants M. Leon, R. Coopersmith, L.J. Beasley, & R.*M. Sullivan: The role of mother-young contact in maternal care Jeffrey R. Alberts, & David J. Gubernick: Functional organization of dyadic and triadic parent-offspring systems Warren G. Holmes: Parent-offspring recognition in mammals: a proximate and ultimate perspective M.W. Yogman: Male parental behavior in humans and nonhuman primates Part V. Future directions in research research on mammalian parenting

Effects of litter age, litter size, and ambient temperature on the milk ejection reflex in lactating rats.

Under a number of circumstances the duration of mother-young contact in the rat can be drastically reduced while pup growth is maintained. We investigated the possibility that under some of these conditions the timing of milk delivery is changed. We assessed the time of onset and pattern of milk delivery over a nest bout in litters of two different ages (Day 4 or Day 10) and three different sizes (4, 8, or 12 pups). Ambient temperature fluctuated over the course of the study and was found to correlate significantly with the latency to the first milk ejection (ME). Specifically, the warmer the ambient temperature, the quicker the first ME occurred. Durations between successive MEs correlated with ambient temperature in a similar fashion. Analysis of covariance revealed that the onset of the first ME occurred earlier in Day 10 litters than in Day 4 litters, but litter size had no effect. Durations between successive MEs were not affected by either litter age or litter size. These data indicate one possible mechanism by which adequate milk delivery can be maintained despite some reduction in mother-young contact.

Thermal control of mother-young contact in Norway rats: Factors mediating the chronic elevation of maternal temperature

The chronically elevated heat production of lactating Norway rats makes them vulnerable to acute hyperthermia during pup contact and thereby limits the duration of such interactions. High lactational levels of progesterone and corticosterone may act in concert to increase maternal heat load. Specifically, progesterone appears to increase maternal thermal set point and corticosterone is necessary for the increase in maternal heat production. Thyroid hormones and brown adipose tissue do not seem to contribute to the chronic increase in maternal heat production. While mammary tissue does contribute to maternal heat load, it is no more hypermetabolic than other maternal tissues.

Thermal limitation of mother--young contact in Norway rats.

Thermal limitation of mother--young contact in Norway rats.