Effects of neonatal paternal deprivation or early deprivation on anxiety and social behaviors of the adults in mandarin voles

Jia, Rui; Tai, Fadao; An, Shu-Cheng; Zhang, Xia; Broders, Hugh G.

doi:10.1016/j.beproc.2009.07.006

Cited by 92 publications

(62 citation statements)

References 58 publications

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“…In socially monogamous and biparental species, deprivation of paternal care can result in reduced social recognition (Cao et al, 2014), altered development of play behavior , impaired pair-bonding , and increased anxiety-like behavior (Jia et al, 2009). These behavioral impairments are associated with paternal deprivation-induced neurobiological changes, including sex-specific effects on dopamine receptor gene expression in the nucleus accumbens , reductions in oxytocin receptor and ER alpha (ERa) levels (Cao et al, 2014), altered development of neuroendocrine pathways involved in the response to stress (Seidel et al, 2011), and reduced neuronal complexity (Braun et al, 2013;Pinkernelle et al, 2009).…”

Section: Studies Of Paternal Influences On Offspring Development In Rmentioning

confidence: 99%

Early-Life Experience, Epigenetics, and the Developing Brain

Kundaković

Champagne

2014

Neuropsychopharmacol

251

182

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Development is a dynamic process that involves interplay between genes and the environment. In mammals, the quality of the postnatal environment is shaped by parent-offspring interactions that promote growth and survival and can lead to divergent developmental trajectories with implications for later-life neurobiological and behavioral characteristics. Emerging evidence suggests that epigenetic factors (ie, DNA methylation, posttranslational histone modifications, and small noncoding RNAs) may have a critical role in these parental care effects. Although this evidence is drawn primarily from rodent studies, there is increasing support for these effects in humans. Through these molecular mechanisms, variation in risk of psychopathology may emerge, particularly as a consequence of early-life neglect and abuse. Here we will highlight evidence of dynamic epigenetic changes in the developing brain in response to variation in the quality of postnatal parent-offspring interactions. The recruitment of epigenetic pathways for the biological embedding of early-life experience may also have transgenerational consequences and we will describe and contrast two routes through which this transmission can occur: experience dependent vs germline inheritance. Finally, we will speculate regarding the future directions of epigenetic research and how it can help us gain a better understanding of the developmental origins of psychiatric dysfunction.

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Section: Studies Of Paternal Influences On Offspring Development In Rmentioning

confidence: 99%

Early-Life Experience, Epigenetics, and the Developing Brain

Kundaković

Champagne

2014

Neuropsychopharmacol

251

182

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“…In addition to the obvious influence of parental provisioning on offspring size and morphological traits, parental care can also exert substantial influence on offspring behavioural traits [1][2][3][4]. For example in rodents and non-human primates, offspring receiving low levels of parental care, or deprived of it altogether, develop more reactive stress response systems, thereby reducing their ability to cope with stressors and leading to increased anxiety [2,3,5,6]. This suggests that receiving adequate parental care is an important part of offspring development and its removal has long-lasting consequences for how offspring react to stressors.…”

Section: Introductionmentioning

confidence: 99%

Paternal care in a fish: epigenetics and fitness enhancing effects on offspring anxiety

McGhee

Bell

2014

Proc. R. Soc. B.

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In many animals, including humans, interactions with caring parents can have long-lasting effects on offspring sensitivity to stressors. However, whether these parental effects impact offspring fitness in nature is often unclear. In addition, despite evidence that maternal care can influence offspring behaviour via epigenetic alterations to the genome, it remains unclear whether paternal care has similar effects. Here, we show in three-spined sticklebacks, a fish in which fathers are the sole provider of offspring care, that the direct care provided by fathers affects offspring anxiety and the potential for epigenetic alterations to the offspring genome. We find that families are differentially vulnerable to early stress and fathers can compensate for this differential sensitivity with the quality of their care. This variation in paternal care is also linked to the expression in offspring brains of a DNA methyltransferase (Dnmt3a) responsible for de novo methylation. We show that these paternal effects are potentially adaptive and anxious offspring are unlikely to survive an encounter with a predator. By supplying offspring care, fathers reduce offspring anxiety thereby increasing the survival of their offspringnot in the traditional sense through resource provisioning but through an epigenetic effect on offspring behavioural development.

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“…Hence, it is possible that the behavior of prairievole mothers in our study altered her adult sons' stress responses. Although we did not record the mother's behavior following the father's removal, we think this is an unlikely scenario because previous studies under laboratory or semi-natural conditions in prairie and mandarin voles have shown that the mother does not compensate when the father is removed from the nest (McGuire et al, 2007;Jia et al, 2009;Ahern et al, 2011). However, because voles are biparental, it is possible that reduction in total overall care that is usually provided by both parents affected the sons' behavior later in life .…”

Section: Discussionmentioning

confidence: 98%

“…Our results are contrary to some of the previous research in monogamous rodents. In mandarin voles, removal of the father immediately after birth or separation of young from their littermates increased adulthood anxiety levels measured in an empty open-field testing arena (Jia et al, 2009). Exposure of mandarin voles to paternal loss as neonates also lowered their sociality, particularly in females.…”

Section: Discussionmentioning

confidence: 99%

Socio-Ecological Disruptions at Critical Periods During Development Alter Stress Responses and Hippocampal Dendritic Morphology of Prairie Voles: Implications for Social Monogamy

et al. 2018

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Emotions are often associated with the evolution of monogamy. For example, fear of cuckoldry has been recently proposed as the driving force for human monogamy. We used prairie voles (Microtus ochrogaster) as a model of human behavior to study how stress reactivity is shaped by socio-ecological disruptions experienced as neonates and as subadults. We hypothesized that social disruptions would have a greater impact on the vole's stress levels than ecological disruptions, and that females would be more susceptible to the experience than males. At 6 days postpartum, the housing conditions were manipulated to have offspring raised by: (1) both parents under a protective cover (NoDisrupt); (2) Both parents uncovered (EcoDisrupt); (3) Mother alone covered (SocDisrupt); (4) Mother alone uncovered (SocEcoDisrupt). To experience disruptions as subadults, offspring were weaned then housed either alone (Isolate) or with a same-sex sibling (Social). As adults, each offspring was placed in an open-field arena and tested over 3 consecutive days to measure its behavior in response to an empty space (Day1), a same-sex vole in a container (Day2), and an empty container (Day3). The brain of a subgroup of subjects was processed for Golgi staining to assess the impact of disruptions on hippocampal dendritic morphology in adulthood. Males that experienced social disruption in early life displayed lower stress levels on Day2 of testing than males and females in other groups. This effect was only evident in males that did not experience social disruptions as subadults. Socio-ecological disruptions at postpartum had an unanticipated impact on the hippocampus of the voles. The apical dendrites of the CA3 neurons in male and female voles that experienced either social or ecological disruptions in early life and remained socially isolated as subadults were longer than those in undisturbed voles. Our results suggest that social disruptions experienced in early life modulate the male's stress-related behaviors and may thus influence his monogamous tendencies. Exposure to disruptions may also impact the memory circuits of the brain that monogamous animals use to make mating decisions.

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Effects of neonatal paternal deprivation or early deprivation on anxiety and social behaviors of the adults in mandarin voles

Cited by 92 publications

References 58 publications

Early-Life Experience, Epigenetics, and the Developing Brain

Early-Life Experience, Epigenetics, and the Developing Brain

Paternal care in a fish: epigenetics and fitness enhancing effects on offspring anxiety

Socio-Ecological Disruptions at Critical Periods During Development Alter Stress Responses and Hippocampal Dendritic Morphology of Prairie Voles: Implications for Social Monogamy

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