Oxytocin neurons enable social transmission of maternal behaviour

AbstractMaternal care, including by non-biological parents, is important for offspring survival1–8. Oxytocin1,2,9–15, which is released by the hypothalamic paraventricular nucleus (PVN), is a critical maternal hormone. In mice, oxytocin enables neuroplasticity in the auditory cortex for maternal recognition of pup distress15. However, it is unclear how initial parental experience promotes hypothalamic signalling and cortical plasticity for reliable maternal care. Here we continuously monitored the behaviour of female virgin mice co-housed with an experienced mother and litter. This documentary approach was synchronized with neural recordings from the virgin PVN, including oxytocin neurons. These cells were activated as virgins were enlisted in maternal care by experienced mothers, who shepherded virgins into the nest and demonstrated pup retrieval. Virgins visually observed maternal retrieval, which activated PVN oxytocin neurons and promoted alloparenting. Thus rodents can acquire maternal behaviour by social transmission, providing a mechanism for adapting the brains of adult caregivers to infant needs via endogenous oxytocin.

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Oxytocin Neurons Enable Social Transmission of Maternal Behavior

10.1101/845495 ◽

2019 ◽

Author(s):

Ioana Carcea ◽

Naomi López Caraballo ◽

Bianca J. Marlin ◽

Rumi Ooyama ◽

Justin S. Riceberg ◽

...

Keyword(s):

Social Interactions ◽

Paraventricular Nucleus ◽

Maternal Behavior ◽

Maternal Care ◽

Cortical Plasticity ◽

Social Transmission ◽

Infant Vocalizations ◽

Biological Parents ◽

Pup Retrieval ◽

Molecular Signal

AbstractMaternal care is profoundly important for mammalian survival, and non-biological parents can express it after experience with infants. One critical molecular signal for maternal behavior is oxytocin, a hormone centrally released by hypothalamic paraventricular nucleus (PVN). Oxytocin enables plasticity within the auditory cortex, a necessary step for responding to infant vocalizations. To determine how this change occurs during natural experience, we continuously monitored homecage behavior of female virgin mice co-housed for days with an experienced mother and litter, synchronized with recordings from virgin PVN cells, including from oxytocin neurons. Mothers engaged virgins in maternal care by ensuring their nest presence, and demonstrated maternal behavior in self-generated pup retrieval episodes. These social interactions activated virgin PVN and gated behaviorally-relevant cortical plasticity for pup vocalizations. Thus rodents can acquire maternal behavior by social transmission, and our results describe a mechanism for adapting brains of adult caregivers to infant needs via endogenous oxytocin.One Sentence SummaryMother mice help co-housed virgins become maternal by enacting specific behaviors that activate virgin oxytocin neurons.

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An acute dose of intranasal oxytocin rapidly increases maternal communication and maintains maternal care in primiparous postpartum California mice

PLoS ONE ◽

10.1371/journal.pone.0244033 ◽

2021 ◽

Vol 16 (4) ◽

pp. e0244033

Author(s):

Caleigh D. Guoynes ◽

Catherine A. Marler

Keyword(s):

Maternal Care ◽

Behavioral Changes ◽

Wire Mesh ◽

Offspring Survival ◽

Testing Chamber ◽

Pup Retrieval ◽

Normal Increase ◽

Physical Access ◽

California Mice ◽

Separation Test

Maternal-offspring communication and care are essential for offspring survival. Oxytocin (OXT) is known for its role in initiation of maternal care, but whether OXT can rapidly influence maternal behavior or ultrasonic vocalizations (USVs; above 50 kHz) has not been examined. To test for rapid effects of OXT, California mouse mothers were administered an acute intranasal (IN) dose of OXT (0.8 IU/kg) or saline followed by a separation test with three phases: habituation with pups in a new testing chamber, separation via a wire mesh, and finally reunion with pups. We measured maternal care, maternal USVs, and pup USVs. In mothers, we primarily observed simple sweep USVs, a short downward sweeping call around 50 kHz, and in pups we only observed pup whines, a long call with multiple harmonics ranging from 20 kHz to 50 kHz. We found that IN OXT rapidly and selectively enhanced the normal increase in maternal simple sweep USVs when mothers had physical access to pups (habituation and reunion), but not when mothers were physically separated from pups. Frequency of mothers’ and pups’ USVs were correlated upon reunion, but IN OXT did not influence this correlation. Finally, mothers given IN OXT showed more efficient pup retrieval/carrying and greater total maternal care upon reunion. Behavioral changes were specific to maternal behaviors (e.g. retrievals) as mothers given IN OXT did not differ from controls in stress-related behaviors (e.g. freezing). Overall, these findings highlight the rapid effects and context-dependent effect a single treatment with IN OXT has on both maternal USV production and offspring care.

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Seasonal plasticity of maternal behaviour in Peromyscus maniculatus

Behaviour ◽

10.1163/1568539x-00003211 ◽

2014 ◽

Vol 151 (11) ◽

pp. 1641-1662 ◽

Cited By ~ 6

Author(s):

Frances E.C. Stewart ◽

Andrew G. McAdam

Keyword(s):

Maternal Care ◽

Peromyscus Maniculatus ◽

Post Partum ◽

Laboratory Research ◽

Deer Mice ◽

Maternal Behaviour ◽

Wild Mice ◽

Seasonal Plasticity ◽

Laboratory Rodents ◽

Pup Retrieval

Individual variation in maternal care has been shown to have important consequences for offspring behaviour, development, and physiology. The proximate mechanisms associated with these maternal effects have been elegantly detailed in laboratory rodents where environmental variation is typically minimized. However, investigating the ultimate consequences of differences in maternal behaviour and factors that maintain variation in maternal care requires the extension of well established protocols for measuring maternal behaviour in the lab to a wild rodent species. In the present study we build on the important contributions of laboratory research by applying laboratory protocols for quantifying maternal behaviour, maternal provisioning, and maternal responsivity in laboratory rodents to wild-caught Peromyscus, which experience large fluctuations in environmental conditions. We temporarily transported wild-caught deer mice (Peromyscus maniculatus gracilis) to a field laboratory for parturition and the first week post partum and then returned individuals with their offspring to the wild. We demonstrate that the proportion of time spent nursing by wild-caught deer mice was similar to previous studies of laboratory rodents and was repeatable within litters. However, in contrast to prior studies of laboratory rodents, the proportion of time spent nursing by wild-caught deer mice was independent of the proportion of time spent licking and grooming and the latency to retrieve pups in a pup-retrieval test. Wild-caught deer mice also exhibited a high degree of seasonal plasticity in nursing behaviour; females that raised litters early in the season spent almost twice as much time nursing as those raising litters at the end of the season. The amount of time spent nursing offspring in captivity was negatively correlated with population density of wild mice in the field at the time of their capture, but such a seasonal decline in nursing could also be caused by other seasonal changes in their natural environment. These findings suggest the potential for much greater plasticity in maternal care by rodents than might otherwise be revealed from studies of animals born and raised under controlled laboratory conditions.

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The Ontogeny of Ultrasonic Vocalization in Microtus Montanus

Behaviour ◽

10.1163/156853977x00306 ◽

1977 ◽

Vol 60 (1-2) ◽

pp. 115-121 ◽

Cited By ~ 4

Author(s):

V.J. De Ghett

Keyword(s):

Short Duration ◽

Maternal Care ◽

Ultrasonic Vocalization ◽

Ultrasonic Vocalizations ◽

Developmental Changes ◽

Maternal Behaviour ◽

Postnatal Ontogeny ◽

Microtus Montanus ◽

Early Peak ◽

The Mean

AbstractDevelopmental changes in parameters of ultrasound production were investigated in M. montanus young. The rate of ultrasonic vocalization reached a peak on Day 2 of postnatal ontogeny and declined to zero on Day 15. A similar developmental pattern has been found in several other rodent species. However, the comparatively early peak rate is indicative of a degree of ontogenic precociousness. Other developmental changes, both behavioural and morphological, tend to confirm that M. montanus young are relatively precocious. The duration of ultrasonic vocalizations did not show a significant change across early development. The mean duration for each vocalization sampled was 22.92 msec. The distribution of these vocalizations showed that a considerable number of vocalizations were of very short duration (<30 msec). The developmental changes in the percentage of young emitting ultrasounds began to decline following Day 8 and reached zero percent on Day 15. This decline in the percentage of young vocalizing corresponded to changes in maternal behaviour. Both the rate of ultrasonic vocalization and the percentage of young vocalizing were significantly correlated with the age of the young. Being correlated with age, these parameters of ultrasound production have the possibility of having great communicative value for the purposes of maternal care.

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Neonatal mice exposed to a high-fat dietin uteroinfluence the behaviour of their nursing dam

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2018.1237 ◽

2018 ◽

Vol 285 (1891) ◽

pp. 20181237 ◽

Cited By ~ 1

Author(s):

Marine Baptissart ◽

Harold E. Lamb ◽

Kimberly To ◽

Christine Bradish ◽

Jesse Tehrani ◽

...

Keyword(s):

Environmental Factors ◽

In Utero ◽

Maternal Behaviour ◽

Physiological Changes ◽

Environmental Stressor ◽

High Fat ◽

Behavioural Characteristics ◽

Direct Exposure ◽

Pup Retrieval ◽

Cross Fostering

The behaviour of a nursing dam influences the development, physiology, and behaviour of her offspring. Maternal behaviours can be modulated both by environmental factors, including diet, and by physical or behavioural characteristics of the offspring. In most studies of the effects of the environment on maternal behaviour, F0dams nurse their own F1offspring. Because the F1are indirectly exposed to the environmental stressorin uteroin these studies, it is not possible to differentiate between effects on maternal behaviour from direct exposure of the dam and those mediated by changes in the F1as a consequence ofin uteroexposure. In this study, we used a mouse model of high-fat (HF) diet feeding, which has been shown to influence maternal behaviours, combined with cross-fostering to discriminate between these effects. We tested whether the diet of the F0dam or the exposure experienced by the F1pupsin uterois the most significant predictor of maternal behaviour. Neither factor significantly influenced pup retrieval behaviours. However, strikingly, F1in uteroexposure was a significant predictor of maternal behaviour in the 15 min immediately following pup retrieval while F0diet had no discernable effect. Our findings suggest thatin uteroexposure to HF diet programmes physiological changes in the offspring which influence the maternal behaviours of their dam after birth.

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Investigation of the relationship between farrowing environment, sex steroid concentrations and maternal aggression in gilts

Proceedings of the British Society of Animal Science ◽

10.1017/s1752756200592369 ◽

1996 ◽

Vol 1996 ◽

pp. 34-34

Author(s):

K.A. McLean ◽

A.B. Lawrence ◽

J.C. Petherick ◽

L. Deans ◽

J. Chirnside ◽

...

Keyword(s):

Sex Steroids ◽

Maternal Care ◽

Social Behaviour ◽

Social Rank ◽

Sex Steroid ◽

Maternal Behaviour ◽

Maternal Aggression ◽

The Relationship

Maternal oestrogen and progesterone have been shown to be important in the initiation of maternal behaviour (e.g. Shipka and Ford, 1991). It has also been suggested by Csermely and Nicosia (1991) that there is an association between social rank and the performance of maternal behaviour. This study investigated the relationships between social behaviour during pregnancy, levels of sex steroids around parturition and the level of maternal care shown by gilts. Sows and gilts are generally housed in farrowing crates during parturition and lactation. This study also ascertained whether or not the farrowing environment affected sex steroid concentrations.

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Corticotropin-releasing factor infusion in the bed nucleus of the stria terminalis of lactating mice alters maternal care and induces behavioural phenotypes in offspring

Scientific Reports ◽

10.1038/s41598-020-77118-7 ◽

2020 ◽

Vol 10 (1) ◽

Author(s):

Kerstin Camile Creutzberg ◽

Érika Kestering-Ferreira ◽

Thiago Wendt Viola ◽

Luis Eduardo Wearick-Silva ◽

Rodrigo Orso ◽

...

Keyword(s):

Locomotor Activity ◽

Maternal Care ◽

Corticotropin Releasing Factor ◽

Maternal Behaviour ◽

Stria Terminalis ◽

Bed Nucleus ◽

Plus Maze ◽

Maternal Brain ◽

Nesting Material ◽

Peripartum Period

AbstractThe peripartum period is accompanied by numerous physiological and behavioural adaptations organised by the maternal brain. These changes are essential for adequate expression of maternal behaviour, thereby ensuring proper development of the offspring. The corticotropin-releasing factor (CRF) plays a key role in a variety of behaviours accompanying stress, anxiety, and depression. There is also evidence that CRF contributes to maladaptations during the peripartum period. We investigated the effects of CRF in the bed nucleus of the stria terminalis (BNST) of lactating mice during maternal care and analysed locomotor activity and anxiety-like behaviour in the offspring. The BNST has been implicated in anxiety behaviour and regulation of the stress response. The effects of intra-BNST CRF administration were compared with those induced by the limited bedding (LB) procedure, a model that produces altered maternal behaviour. BALB/cJ dams were exposed to five infusions of CRF or saline into the BNST in the first weeks after birth while the LB dams were exposed to limited nesting material from postnatal days (P) 2–9. Maternal behaviour was recorded in intercalated days, from P1-9. Offspring anxiety-like behaviour was assessed during adulthood using the open-field, elevated plus-maze, and light/dark tests. Both intra-BNST CRF and LB exposure produced altered maternal care, represented by decreased arched-back nursing and increased frequency of exits from the nest. These changes in maternal care resulted in robust sex-based differences in the offspring’s behavioural responses during adulthood. Females raised by CRF-infused dams exhibited increased anxiety-like behaviour, whereas males presented a significant decrease in anxiety. On the other hand, both males and females raised by dams exposed to LB showed higher locomotor activity. Our study demonstrates that maternal care is impaired by intra-BNST CRF administrations, and these maladaptations are similar to exposure to adverse early environments. These procedures, however, produce distinct phenotypes in mice during young adulthood and suggest sex-based differences in the susceptibility to poor maternal care.

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Maternal behaviour in Border Leicester, Glen Vale (Border Leicester derived) and Merino sheep

Australian Journal of Experimental Agriculture ◽

10.1071/ea9900027 ◽

1990 ◽

Vol 30 (1) ◽

pp. 27 ◽

Cited By ~ 32

Author(s):

G Alexander ◽

D Stevens ◽

LR Bradley ◽

SA Barwick

Keyword(s):

Maternal Care ◽

Maternal Behaviour ◽

Selection Program ◽

Merino Sheep ◽

Lamb Survival

Ewe and lamb behaviour in traditional Border Leicesters, Glen Vale Border Leicesters of the NSW Agriculture and Fisheries, Glen Vale x Border Leicester crosses and medium-fine-wool Merinos, all running in paddocks of 3-4.5 ha, were compared in spring 1983 at Glen Innes, N.S.W. Twenty-eight aspects of behaviour with a known or reputed influence on lamb survival, especially of multiples, were examined in undisturbed and contrived situations. The Glen Vales and their crosses were superior to the Border Leicesters and Merinos in behaviour and lamb survival, particularly behaviour concerned with the ability of ewes to keep their lambs together. The study indicates that contrived twin-care tests could form the basis of a selection program to improve maternal care and survival of multiples.

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Anti-progesterone effects on maternal recognition and behaviour imprinted during first pregnancy in mice

Journal of Endocrinology ◽

10.1677/joe.0.1470331 ◽

1995 ◽

Vol 147 (2) ◽

pp. 331-337 ◽

Cited By ~ 5

Author(s):

D L Crombie ◽

J S Hayes ◽

R B Heap ◽

M-W Wang

Keyword(s):

Latency Period ◽

Negative Influence ◽

Full Length ◽

Residual Effects ◽

Maternal Behaviour ◽

Neural Pathways ◽

Progesterone Treatment ◽

Maternal Rejection ◽

Pup Retrieval ◽

Retrieval Latency

Abstract Anti-progesterone treatment using specific anti-progesterone antibodies or a progesterone receptor (PR) antagonist during first pregnancy impairs postpartum maternal behaviour in mice. This effect is demonstrable only if the treatment is given during pregnancy but not immediately after parturition. The purpose of the present studies was to investigate if maternal behaviour is also impaired by anti-progesterone treatment in subsequent pregnancies. Studies with a monoclonal antibody to progesterone (DB3; 4·5 nmol/mouse) showed that injection of females on day 17 of second pregnancy did not cause maternal rejection but the latency of pup retrieval was prolonged especially during the first 3 days of lactation. This phenomenon was not observed in animals that had previous experience of full length lactation. Experiments were carried out with mifepristone (RU486; 10 μg/mouse) injected at day 17 of first, second or third pregnancies. Pup rejection (22·5% vs 12·3%) and prolongation of the retrieval latency (62·3 ± 13·3 vs 19·7 ± 6·5 s; P<0·02) were observed following the first pregnancy. No abnormal behavioural effects were found in mothers treated in second or third pregnancy who had prior full length lactation experience. Control females subjected to only one pup retrieval test after first delivery rejected their pups if treated in their second pregnancy (27.3% vs 4·4%; P<0·001) and displayed a marginal prolongation of the retrieval latency period (20·9 ± 7·0 vs 7·4 ± 2·6 s). Anti-progesterone treatment had no negative influence when administered during third pregnancy. To determine whether treatment with RU486 (50 μg/mouse, day 17) during first pregnancy has any residual effects, maternal response was monitored after completion of second pregnancy where no treatment was given. Females who exhibited both maternal rejection and prolonged retrieval latency following first pregnancy did not demonstrate any carryover effects during second lactation, indicating that there is no long-term consequence of RU486 treatment. These results suggest that: (i) anti-progesterone treatment of pregnant mice prevents maternal recognition and disrupts postpartum behaviour in females who had no, or very limited, nursing experience; (ii) there is a progesterone-dependent imprinting mechanism during the first pregnancy that is disrupted by anti-progesterone antibody or PR antagonist; and (iii) this imprinting mechanism and first lactation are important components of the consolidation of neural pathways that are associated with the establishment of normal maternal behaviour. Journal of Endocrinology (1995) 147, 331–337

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Experimental evidence for convergent evolution of maternal care heuristics in industrialized and small-scale populations

Royal Society Open Science ◽

10.1098/rsos.140518 ◽

2015 ◽

Vol 2 (6) ◽

pp. 140518 ◽

Cited By ~ 1

Author(s):

Geoff Kushnick ◽

Ben Hanowell ◽

Jun-Hong Kim ◽

Banrida Langstieh ◽

Vittorio Magnano ◽

...

Keyword(s):

Maternal Care ◽

Convergent Evolution ◽

National Level ◽

Decision Rules ◽

Third Party ◽

Current Evidence ◽

Small Scale ◽

Maternal Behaviour ◽

Scale Population ◽

Vignette Experiment

Maternal care decision rules should evolve responsiveness to factors impinging on the fitness pay-offs of care. Because the caretaking environments common in industrialized and small-scale societies vary in predictable ways, we hypothesize that heuristics guiding maternal behaviour will also differ between these two types of populations. We used a factorial vignette experiment to elicit third-party judgements about likely caretaking decisions of a hypothetical mother and her child when various fitness-relevant factors (maternal age and access to resources, and offspring age, sex and quality) were varied systematically in seven populations—three industrialized and four small-scale. Despite considerable variation in responses, we found that three of five main effects, and the two severity effects, exhibited statistically significant industrialized/ small-scale population differences. All differences could be explained as adaptive solutions to industrialized versus small-scale caretaking environments. Further, we found gradients in the relationship between the population-specific estimates and national-level socio-economic indicators, further implicating important aspects of the variation in industrialized and small-scale caretaking environments in shaping heuristics. Although there is mounting evidence for a genetic component to human maternal behaviour, there is no current evidence for interpopulation variation in candidate genes. We nonetheless suggest that heuristics guiding maternal behaviour in diverse societies emerge via convergent evolution in response to similar selective pressures.

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