Neuroendocrine responses to social isolation and paternal deprivation at different postnatal ages in mandarin voles

Wang, Lu; Zhang, Wei; Wu, Ruiyong; Kong, Lingzhe; Feng, Weige; Cao, Yan; Tai, Fadao; Zhang, Xia

doi:10.1002/dev.21202

Cited by 18 publications

(9 citation statements)

References 73 publications

(122 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…However, induction of mRNA does not guarantee induction of protein (Maier et al 2009; Lodish et al 2007). It is extremely rare to observe such rapid changes in peptide expression, and, to our knowledge, this is the first report of PVN VP-ir or OT-ir changes occurring on the same timescale as Fos (but see Wang et al 2014; Cayetanot et al 2005). …”

Section: Discussionmentioning

confidence: 78%

Rapid nonapeptide synthesis during a critical period of development in the prairie vole: plasticity of the paraventricular nucleus of the hypothalamus

2018

View full text Add to dashboard Cite

Vasopressin (VP) and oxytocin (OT) are involved in modulating basic physiology and numerous social behaviors. Although the anatomical distributions of nonapeptide neurons throughout development have been described, the functional roles of VP and OT neurons during development are surprisingly understudied, and it is unknown whether they exhibit functional changes throughout early development. We utilized an acute social isolation paradigm to determine if VP and OT neural responses in eight nonapeptide cell groups differ at three different stages of early development in prairie voles. We tested pups at ages that are representative of the three rapid growth stages of the developing brain: postnatal day (PND)2 (closed eyes; poor locomotion), PND9 (eye opening; locomotion; peak brain growth spurt), and PND21 (weaning). Neural responses were examined in pups that (1) were under normal family conditions with their parents and siblings, (2) were isolated from their parents and siblings and then reunited, and (3) were isolated from their parents and siblings. We found that VP and OT neural activity (as assessed via Fos co-localization) did not differ in response to social condition across development. However, remarkably rapid VP and OT synthesis in response to social isolation was observed only in the paraventricular nucleus of the hypothalamus (PVN) and only in PND9 pups. These results suggest that PVN nonapeptide neurons exhibit distinct cellular properties during a critical period of development, allowing nonapeptide neurons to rapidly upregulate peptide production in response to stressors on a much shorter timescale than has been observed in adult animals.

show abstract

Section: Discussionmentioning

confidence: 78%

Rapid nonapeptide synthesis during a critical period of development in the prairie vole: plasticity of the paraventricular nucleus of the hypothalamus

2018

View full text Add to dashboard Cite

show abstract

“…It is plausible that PD altered neuroendocrine regulation, yet this was not assessed in the current study. Increased basal corticosterone has been observed throughout the postpartum period (Wang et al, 2014 ) and at weaning (Wang et al, 2012 ) in mandarin vole offspring following removal of the paternal male on PND 0 (i.e., day of birth). Mice with a history of stress, followed by exposure to the forced swim task, exhibit upregulation of genes in the hippocampus that are involved in chromatin modification and epigenetics (e.g., BDNF and GR).…”

Section: Discussionmentioning

confidence: 99%

Enduring Effects of Paternal Deprivation in California Mice (Peromyscus californicus): Behavioral Dysfunction and Sex-Dependent Alterations in Hippocampal New Cell Survival

Glasper

Hyer

Hunter

2018

Front. Behav. Neurosci.

View full text Add to dashboard Cite

Early-life experiences with caregivers can significantly affect offspring development in human and non-human animals. While much of our knowledge of parent-offspring relationships stem from mother-offspring interactions, increasing evidence suggests interactions with the father are equally as important and can prevent social, behavioral, and neurological impairments that may appear early in life and have enduring consequences in adulthood. In the present study, we utilized the monogamous and biparental California mouse (Peromyscus californicus). California mouse fathers provide extensive offspring care and are essential for offspring survival. Non-sibling virgin male and female mice were randomly assigned to one of two experimental groups following the birth of their first litter: (1) biparental care: mate pairs remained with their offspring until weaning; or (2) paternal deprivation (PD): paternal males were permanently removed from their home cage on postnatal day (PND) 1. We assessed neonatal mortality rates, body weight, survival of adult born cells in the dentate gyrus of the hippocampus, and anxiety-like and passive stress-coping behaviors in male and female young adult offspring. While all biparentally-reared mice survived to weaning, PD resulted in a ~35% reduction in survival of offspring. Despite this reduction in survival to weaning, biparentally-reared and PD mice did not differ in body weight at weaning or into young adulthood. A sex-dependent effect of PD was observed on new cell survival in the dentate gyrus of the hippocampus, such that PD reduced cell survival in female, but not male, mice. While PD did not alter classic measures of anxiety-like behavior during the elevated plus maze task, exploratory behavior was reduced in PD mice. This observation was irrespective of sex. Additionally, PD increased some passive stress-coping behaviors (i.e., percent time spent immobile) during the forced swim task—an effect that was also not sex-dependent. Together, these findings demonstrate that, in a species where paternal care is not only important for offspring survival, PD can also contribute to altered structural and functional neuroplasticity of the hippocampus. The mechanisms contributing to the observed sex-dependent alterations in new cell survival in the dentate gyrus should be further investigated.

show abstract

“…An especially relevant developmental period that has been described in rats, mice, mandarin voles and humans is the stress hyporesponsive period (SHRP) . For the purpose of the present review, much emphasis is given to the neonatal rat stress response, although a brief description in mice and human is also presented.…”

Section: Consequences Of Disruption Of the Mother‐infant Relationshipmentioning

confidence: 99%

Maternal regulation of the infant's hypothalamic‐pituitary‐adrenal axis stress response: Seymour ‘Gig’ Levine's legacy to neuroendocrinology

Suchecki

2018

J Neuroendocrinology

View full text Add to dashboard Cite

Thirty years ago, Seymour 'Gig' Levine published a serendipitous, yet, seminal finding with respect to the regulatory role of maternal presence on the corticosterone stress response of neonatal rats during the developmental period known as the stress hyporesponsive period. At the same time, his group of students also investigated the stress response of infant monkeys with respect to maternal separation, as a means of understanding the stress to the primary caregiver resulting from disruptions of attachment. Gig and his group of students and collaborators, mainly in the USA and the Netherlands, investigated how initial social relationships buffer the stress response of nonhuman primates and rodent infants. His work in rodents involved determining how prolonged deprivation of maternal care disinhibits the stress response of neonates and how maternal behaviours regulate specific aspects of the hypothalamic-pituitary-adrenal axis. Maternal deprivation for 24 hours was useful for determining the importance of nutrition in suppressing the corticosterone stress response, whereas anogenital licking and grooming inhibited stress-induced adrenocortoctrophic hormone release, with the combination of both behaviours preventing the effects of maternal deprivation on the central hypothalamic stress response. Levine's group also studied the consequences of maternal deprivation on basal and stress-induced activity of the hypothalamic-pituitary-adrenal axis in juveniles and the persistent effects of the replacement of maternal behaviours on these parameters. Gig's legacy allowed many groups around the world to use the 24-hour maternal deprivation paradigm as an animal model of vulnerability and resilience to stress-related psychiatric disorders, as well as in studies of the neurobiological underpinnings of disruption of the mother-infant relationship and loss of parental care, a highly prevalent condition in humans. This review pays homage to a great scientist and mentor, whose discoveries paved the way for the understanding of how early social relationsships build resilience or lead to susceptibility to emotional disorders later in life.

show abstract

Neuroendocrine responses to social isolation and paternal deprivation at different postnatal ages in mandarin voles

Cited by 18 publications

References 73 publications

Rapid nonapeptide synthesis during a critical period of development in the prairie vole: plasticity of the paraventricular nucleus of the hypothalamus

Rapid nonapeptide synthesis during a critical period of development in the prairie vole: plasticity of the paraventricular nucleus of the hypothalamus

Enduring Effects of Paternal Deprivation in California Mice (Peromyscus californicus): Behavioral Dysfunction and Sex-Dependent Alterations in Hippocampal New Cell Survival

Maternal regulation of the infant's hypothalamic‐pituitary‐adrenal axis stress response: Seymour ‘Gig’ Levine's legacy to neuroendocrinology

Contact Info

Product

Resources

About