Paternal deprivation during infancy results in dendrite- and time-specific changes of dendritic development and spine formation in the orbitofrontal cortex of the biparental rodent Octodon degus

doi:10.1016/j.neuroscience.2009.07.008

Neuroscience

Volume 163, Issue 3, 20 October 2009, Pages 790-798

https://doi.org/10.1016/j.neuroscience.2009.07.008 Get rights and content

Abstract

The aim of this study in the biparental rodent Octodon degus was to assess the impact of paternal deprivation on neuronal and synaptic development in the orbitofrontal cortex, a prefrontal region which is essential for emotional and cognitive function. On the behavioral level the quantitative comparison of parental behaviors in biparental and single-mother families revealed that (i) degu fathers significantly participate in parental care and (ii) single-mothers do not increase their maternal care to compensate the lack of paternal care. On the brain structural level we show in three-week-old father-deprived animals that layer II/III pyramidal neurons in the orbitofrontal cortex displayed significantly lower spine densities on apical and basal dendrites. Whereas biparentally raised animals have reached adult spine density values at postnatal day 21, fatherless animals seem “to catch up” by a delayed increase of spine density until reaching similar values as biparentally raised animals in adulthood. However, in adulthood reduced apical spine numbers together with shorter apical dendrites were observed in father-deprived animals, which indicates that dendritic growth and synapse formation (seen in biparental animals between postnatal day 21 and adulthood) were significantly suppressed. These results demonstrate that paternal deprivation delays and partly suppresses the development of orbitofrontal circuits. The retarded dendritic and synaptic development of the apical dendrites of layer II/III pyramidal neurons in the orbitofrontal cortex of adult fatherless animals may reflect a reduced excitatory connectivity of this cortical subregion.

Section snippets

Animals

Degus (Octodon degus) were bred in our colony at the animal facility of the Leibniz Institute for Neurobiology in Magdeburg. Family groups (Fig. 1) consisting of an adult couple and their offspring were housed in wire cages (length×height×depth: 53×70×43 cm³) equipped with little burrows and climbing scaffolds. The animals were exposed to a 12-h light/dark cycle (6 am/6 pm). Fresh drinking water and rat diet pellets were available ad libitum, vegetables were also fed. The rooms were

Single mothers do not compensate for the lack of paternal care

In biparental families the fathers engaged significantly less (21% of total activity) frequently in LG their offspring compared to the mothers (79% of total activity, Fig. 2A). Degu fathers showed similar activity for huddling as the mothers (Fig. 2C).

Degu dams in single-mother families show similar frequency and quality of mother–pup interactions as mothers raising their pups together with their mate. Single-mothers displayed the same frequency of huddling, licking, grooming and nursing as

Discussion

We demonstrate here in the biparental species Octodon degus that the lack of paternal care significantly interferes with dendritic and synaptic maturation and refinement in OFC. At PND 21 the father-deprived animals displayed significantly lower spine densities on apical and basal dendrites compared to biparentally raised animals. However, the fatherless animals seem “to catch up” by a delayed increase of spine density until reaching similar values as biparentally raised animals in adulthood.

Acknowledgments

We thank Ute Kreher, Susann Becker, Aileen Schröter and Martin Nowak for technical assistance. This work was supported by a grant from the German Science Foundation (SFB 779), a doctoral fellowship from the Land Sachsen–Anhalt (K.S.) and a HFSP short-term postdoctoral fellowship (T.W.B. and K.B.).

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Testosterone (T), estrogen receptor alpha (ERα), and androgen receptor (AR) play a significant role in the regulation of paternal behavior. We determined the effects of deprivation of paternal care on alterations in paternal behavior, T concentrations in plasma, and the presence of ERα and AR in the medial preoptic area (mPOA), bed nucleus of the stria terminalis (BNST), medial amygdala (MeA), and olfactory bulb (OB), as well as the corticosterone (CORT) concentrations in plasma caused by deprivation of paternal care in the Mongolian gerbil (Meriones unguiculatus). Twenty pairs of gerbils were formed; the pups were deprived of paternal care (DPC) in 10 pairs. In another 10 pairs, the pups received paternal care (PC). Ten males raised in DPC condition and 10 males raised in PC conditions were mated with virgin females. When they became fathers, each DPC male and PC male was subjected to tests of paternal behavior on day three postpartum. Blood samples were obtained to quantify T and CORT concentrations, and the brains were removed for ERα and AR immunohistochemistry analyses. DPC males gave less care to their pups than PC males, and they had significantly lower T concentrations and levels of ERα and AR in the mPOA and BNST than PC males. DPC males also had higher CORT concentrations than PC males. These results suggest that in the Mongolian gerbil father’s absence causes a decrease in paternal care in the offspring, which is associated with alterations in the neuroendocrine mechanisms that regulate it.
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However, in a number of monogamous rodents such as degus (Octodon degus), California mice (Peromycus californicus), paternal care also plays an important role in the survival and development of offspring [1,2]. For example, early paternal deprivation was found to impair social cognition [3], increase the level of anxiety [4–7], inhibit the formation of pair bonding [8], reduce the levels of both sociability [4,9] and paternal care [5], reduce apical spine numbers, and shorten apical dendrites in the orbitofrontal cortex [10] in mandarin voles (Microtus mandarinus),California mice and degus respectively. However, although the importance of paternal care has received widespread focus, the manner in which paternal care is initiated and maintained and the underlying neural mechanisms remain unclear.
Like mothers, fathers play a vital role in the development of the brain and behavior of offspring in mammals with biparental care. Unlike mothers, fathers do not experience the physiological processes of pregnancy, parturition, or lactation before their first contact with offspring. Whether pup exposure can induce the onset of paternal behavior and the underlying neural mechanisms remains unclear. By using Slc:ICR male mice exhibiting maternal-like parental care, the present study found that repeated exposure to pups for six days significantly increased the total duration of paternal behavior and shortened the latency to retrieve and care for pups. Repeated pup exposure increased c-Fos-positive neurons and the levels of dopamine- and TH-positive neurons in the nucleus accumbens (NAc). In addition, inhibition of dopamine projections from the ventral tegmental area to the NAc using chemogenetic methods reduced paternal care induced by repeated pup exposure. In conclusion, paternal behavior in virgin male ICR mice can be initiated by repeated pup exposure via sensitization, and the dopamine system may be involved in this process.
How stress physically re-shapes the brain: Impact on brain cell shapes, numbers and connections in psychiatric disorders
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Severe stress is among the most robust risk factors for the development of psychiatric disorders. Imaging studies indicate that life stress is integral to shaping the human brain, especially regions involved in processing the stress response. Although this is likely underpinned by changes to the cytoarchitecture of cellular networks in the brain, we are yet to clearly understand how these define a role for stress in human psychopathology. In this review, we consolidate evidence of macro-structural morphometric changes and the cellular mechanisms that likely underlie them. Focusing on stress-sensitive regions of the brain, we illustrate how stress throughout life may lead to persistent remodelling of the both neurons and glia in cellular networks and how these may lead to psychopathology. We support that greater translation of cellular alterations to human cohorts will support parsing the psychological sequalae of severe stress and improve our understanding of how stress shapes the human brain. This will remain a critical step for improving treatment interventions and prevention outcomes.
Octodon degus: a natural model of multimorbidity for ageing research
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Impact on brain circuits and neurochemistry. Several studies have demonstrated that early life events have an impact on the individual neurochemical configuration and on the establishment of brain circuits and neuronal connections (Braun et al., 2013, 2011, 2000; Helmeke et al., 2009, 2001a, 2001b; Pinkernelle et al., 2009; Jezierski et al., 2007; Ovtscharoff & Braun, 2001; Poeggel et al., 2000). Particularly, serotonergic and dopaminergic projections are altered by social and parental interactions in the cingulate cortex, subregions of the medial and orbital prefrontal cortex, the CA1 region of the hippocampus, the nucleus accumbens and the amygdala of O. degus (Braun et al., 2013; Gos et al., 2006; Poeggel et al., 2003a, 2003b; Ziabreva et al., 2003).
Integrating the multifactorial processes co-occurring in both physiological and pathological human conditions still remains one of the main challenges in translational investigation. Moreover, the impact of age-associated disorders has increased, which underlines the urgent need to find a feasible model that could help in the development of successful therapies. In this sense, the Octodon degus has been indicated as a ‘natural’ model in many biomedical areas, especially in ageing. This rodent shows complex social interactions and high sensitiveness to early-stressful events, which have been used to investigate neurodevelopmental processes. Interestingly, a high genetic similarity with some key proteins implicated in human diseases, such as apolipoprotein-E, β-amyloid or insulin, has been demonstrated. On the other hand, the fact that this animal is diurnal has provided important contribution in the field of circadian biology. Concerning age-related diseases, this rodent could be a good model of multimorbidity since it naturally develops cognitive decline, neurodegenerative histopathological hallmarks, visual degeneration, type II diabetes, endocrinological and metabolic dysfunctions, neoplasias and kidneys alterations. In this review we have collected and summarized the studies performed on the Octodon degus through the years that support its use as a model for biomedical research, with a special focus on ageing.
Severe childhood and adulthood stress associates with neocortical layer-specific reductions of mature spines in psychiatric disorders
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Severe stress exposure causes the loss of dendritic spines on cortical pyramidal neurons and induces psychiatric-like symptoms in rodent models. These effects are strongest following early-life stress and are most persistent on apical dendrites. However, the long-term impacts and temporal effects of stress exposure on the human brain remain poorly understood. Using a novel postmortem cohort of psychiatric cases with severe stress experienced in childhood, adulthood, or no severe stress, and matched controls, we aimed to determine the impact of stress timing on pyramidal neuron structure in the human orbitofrontal cortex (OFC). We performed Golgi Cox staining and manually measured the morphology and density of over 22,000 dendritic spines on layer-specific pyramidal neuron apical dendrites. We also quantified glucocorticoid receptor mRNA and protein as a marker of stress dysregulation. Both childhood and adulthood stress were associated with large reductions in mature mushroom spine density (up to 56% loss) in both the superficial (II/III) and deeper layers (V) of the OFC. However, childhood stress caused more substantial reductions to both total and mature mushroom spines. No difference in glucocorticoid receptor mRNA and protein were seen between groups, although both negatively correlated with total spine density within the whole cohort. These findings indicate that severe stress, especially when experienced during childhood, persistently affects the fine morphological properties of neurons in the human OFC. This may impact on cell connectivity in this brain area, and at least partly explain the social and emotional symptoms that originate in the OFC in psychiatric disorders.

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¹: The first two authors contributed equally to this work.

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Cellular NeuroscienceResearch PaperPaternal deprivation during infancy results in dendrite- and time-specific changes of dendritic development and spine formation in the orbitofrontal cortex of the biparental rodent Octodon degus

Abstract

Section snippets

Animals

Single mothers do not compensate for the lack of paternal care

Discussion

Acknowledgments

Neuroscience

Horm Behav

Horm Behav

Anim Behav

Biol Psychiatry

Neuroscience

Neuroscience

Neurobiol Aging

Brain Cogn

Prog Brain Res

Horm Behav

Neuropharmacology

Brain Res

Behav Proc

Brain Res

Brain Cogn

Behav Brain Res

Behav Brain Res

Reprod Toxicol

Behav Processes

Trends Neurosci

Horm Behav

Horm Behav

The politics of fatherhood

Pol Sci Polit

Blockade of N-methyl-D-aspartate receptor activation suppresses learning-induced synaptic elimination

Proc Natl Acad Sci U S A

Influence of experience on the representation of the “mothering call” in frontoparietal and auditory cortex of pups of the rodent Octodon degus: FDG mapping

J Comp Physiol A

Effect of resource availability on biparental care, and offspring neural and behavioral development in the California mouse (Peromyscus californicus)

Eur J Neurosci

Deprived somatosensory-motor experience in stumptailed monkey neocortex: dendritic spine density and dendritic branching of layer IIIB pyramidal cells

J Comp Neurol

Epigenetic programming of phenotypic variations in reproductive strategies in the rat through maternal care

J Neuroendocrinol

Limbic corticostriatal systems and delayed reinforcement

Ann N Y Acad Sci

Of human bonding: newborns prefer their mothers' voices

Science

Paternal behavior in rodents

Am Zool

Communal burrowing in the hystricognath rodent, Octodon degus: a benefit of sociality?

Behav Ecol Sociobiol

Do female degus communally nest and nurse their pups?

J Ethol

Grouping increases the ability of the social rodent, Octodon degus, to detect predators when using exposed microhabitats

Oikos

Cellular Neuroscience
Research Paper
Paternal deprivation during infancy results in dendrite- and time-specific changes of dendritic development and spine formation in the orbitofrontal cortex of the biparental rodent Octodon degus