Paternal deprivation alters the development of catecholaminergic innervation in the prefrontal cortex and related limbic brain regions

Braun, Katharina; Seidel, Katja; Holetschka, R.; Groeger, Nicole; Poeggel, Gerd

doi:10.1007/s00429-012-0434-1

Cited by 28 publications

(21 citation statements)

References 80 publications

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“…They revealed that the impact of ELS on TH immunoreactivity was strongly dependent on stress severity and developmental time when measuring TH‐IR fiber density. For example, an increase in the density of TH‐IR fibers was observed in the PLC and Acb of juvenile (PND 21) males and in the PLC of adult males after paternal deprivation (Braun et al, 2013). However, prolonged maternal and parental separation reduced the density of TH‐IR fibers in the PLC of adolescent (PND 41) (Braun et al, 2000) and adult males (Kunzler et al, 2015), respectively.…”

Section: Discussionmentioning

confidence: 99%

The effects of early‐life stress on dopamine system function in adolescent female rats

Majcher-Maślanka

Solarz

Wędzony

et al. 2017

Intl J of Devlp Neuroscience

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During adolescence, many neural systems, including the dopamine system, undergo essential remodeling and maturation. It is well known that early-life stress (ELS) increases the risk for many psychopathologies during adolescence and adulthood. It is hypothesized that ELS interferes with the maturation of the dopamine system. There is a sex bias in the prevalence of stress-related mental disorders. Information regarding the effects of ELS on brain functioning in females is very limited. In the current study, maternal separation (MS) procedures were carried out to study the effects of ELS on dopamine system functioning in adolescent female rats. Our study showed that MS increased the density of tyrosine hydroxylase immunoreactive fibers in the prelimbic cortex (PLC) and nucleus accumbens (Acb). These changes were accompanied by a decrease in the level of D5 receptor mRNA and an increase in D2 receptor mRNA expression in the PLC of MS females. Conversely, D1 and D5 receptor mRNA levels were augmented in the caudate putamen (CPu), while the expression of the D3 dopamine receptor transcript was reduced in MS females. Additionally, in the Acb, MS elicited a decrease in D2 receptor mRNA expression. At the behavioral level, MS increased apomorphine-induced locomotion; however, it did not change locomotor responses to selective D1/D5 receptor agonist and attenuated D2/D3 receptor agonist-triggered locomotion. Moreover, MS decreased D1/D5 receptor agonist-induced grooming behavior. These results indicate that ELS disrupts dopamine receptor function in the PLC and basal ganglia during adolescence in females and may predispose them to psychopathologies during adolescence and adulthood.

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Section: Discussionmentioning

confidence: 99%

The effects of early‐life stress on dopamine system function in adolescent female rats

Majcher-Maślanka

Solarz

Wędzony

et al. 2017

Intl J of Devlp Neuroscience

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“…Tyrosine hydroxylase fibers, indicating catecholaminergic innervations, were elevated at PND21 in many areas in paternally deprived male degus, including the NAcc, CeA, and CA1. These elevations remained in adulthood in the hippocampus, but the effect was reversed in the NAcc (Braun et al, 2013). Paternal deprivation in degus also results in widespread developmental changes in interneuron expression patterns (Braun et al, 2011), reduced dendritic spine numbers in the somatosensory neurons (Pinkernelle et al, 2009), as well as in the neurons of the anterior cingulate cortex (Outscharoff et al, 2006).…”

Section: Effects Of Male Parenting On Offspringmentioning

confidence: 99%

Fathering in rodents: Neurobiological substrates and consequences for offspring

Bales

Saltzman

2016

Hormones and Behavior

130

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Paternal care, though rare among mammals, is routinely displayed by several species of rodents. Here we review the neuroanatomical and hormonal bases of paternal behavior, as well as the behavioral and neuroendocrine consequences of paternal behavior for offspring. Fathering behavior is subserved by many of the same neural substrates which are also involved in maternal behavior (for example, the medial preoptic area of the hypothalamus). While gonadal hormones such as testosterone, estrogen, and progesterone, as well as hypothalamic neuropeptides such as oxytocin and vasopressin, and the pituitary hormone prolactin, are implicated in the activation of paternal behavior, there are significant gaps in our knowledge of their actions, as well as pronounced differences between species. Removal of the father in biparental species has long-lasting effects on behavior, as well as on these same neuroendocrine systems, in offspring. Finally, individual differences in paternal behavior can have similarly long-lasting, if more subtle, effects on offspring behavior. Future studies should examine similar outcome measures in multiple species, including both biparental species and closely related uniparental species. Careful phylogenetic analyses of the neuroendocrine systems presumably important to male parenting, as well as their patterns of gene expression, will also be important in establishing the next generation of hypotheses regarding the regulation of male parenting behavior.

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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). In the biparental California mouse, paternal behavior has been shown to alter the development of neural systems involved in aggression, with implications for variation in paternal behavior in male offspring (Frazier et al, 2006;Gleason and Marler, 2013).…”

Section: Studies Of Paternal Influences On Offspring Development In Rmentioning

confidence: 99%

Early-Life Experience, Epigenetics, and the Developing Brain

Kundaković

Champagne

2014

Neuropsychopharmacol

257

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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Paternal deprivation alters the development of catecholaminergic innervation in the prefrontal cortex and related limbic brain regions

Cited by 28 publications

References 80 publications

The effects of early‐life stress on dopamine system function in adolescent female rats

The effects of early‐life stress on dopamine system function in adolescent female rats

Fathering in rodents: Neurobiological substrates and consequences for offspring

Early-Life Experience, Epigenetics, and the Developing Brain

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