Paternal Deprivation and Female Biparental Family Rearing Induce Dendritic and Synaptic Changes in Octodon degus: I. Medial Prefrontal Cortex

Abstract

In most mammalian species parent-offspring interactions during early life periods primarily comprise social contacts with the mother, whereas the role of males in parental care is one of the most overlooked and understudied topics. The present study addressed the hypothesis that the complete deprivation of paternal care delays or permanently retards synaptic connectivity in the brain, particularly in the medial prefrontal cortex (mPFC) of the offspring in a sex-specific manner. Another aim of this study was to address the question whether and in which way replacing the father with a female caregiver (in our experiments the "aunt") can "buffer" the detrimental effects of paternal deprivation on neuronal development. The comparison of: (a) single mother rearing; (b) biparental rearing by father and mother; and (c) biparental rearing by two female caregivers revealed that: (i) paternal care represents a critical environmental factor for synaptic and dendritic development of pyramidal neurons in the vmPFC of their offspring; (ii) a second female caregiver ("aunt") does not "buffer" the neuronal consequences of paternal deprivation; and that (iii) neuronal development in the vmPFC is differentially affected in male and female offspring in response to different family constellations.

Paternal Deprivation and Female Biparental Family Rearing Induce Dendritic and Synaptic Changes in Octodon degus: II. Nucleus Accumbens

“…In line with these findings, we experimentally addressed this issue in more detail by replacing the father with a second female caregiver (the “aunt”), resulting in a female biparental family. The results of the present study on MSNs in the NAc and of our previous study on neurons in the mPFC [44] show that in our degu model, a female caregiver cannot “protect” from or compensate for the neurostructural and synaptic changes induced by growing up in a fatherless environment. Instead, the presence of a second female caregiver induces different changes particularly in the vmPFC of female offspring but fails to compensate for the effects in the NAc in both sexes.…”

“…Within the reward circuit, the NAc receives prominent excitatory input from the mPFC and the hippocampus, and specifically, the mPFC exerts top-down control of reward-related behaviors. Our analysis in the same animals revealed significantly reduced spine densities on pyramidal neurons in the mPFC of father-deprived male offspring [44], which together with the reduced synaptic densities in the NAc indicates that paternal care significantly promotes the development of functional neuronal networks within reward pathways.…”

“…(1) To assess whether spine changes are confined to specific areas of the dendritic field, the natural branches (segments) of the dendritic trees were numbered consecutively (primary, secondary, tertiary, etc.) from proximal to distal [44, 52] shown in Figure 1c. Spine frequency was calculated (i) as average of the complete dendrite and (ii) as average of the individual branching orders.…”

Childhood separation from parents with cognitive and psychopathological outcomes in adolescence

“…The cognitive pathologies observed in father-absent children likely arise from a socio-emotionally impoverished family setting resulting in functional deficits within specific brain circuits. Indeed, the development and functional maturation of brain regions such as the orbitofrontal cortex (OFC) and the anterior cingulate cortex (ACC) are particularly sensitive towards paternal input as revealed in previous studies (de Schultz et al, 2020;Feldman et al, 2019;van 't Veer et al, 2019). Another possible reason for the differential effect of parental absence is that they take separate duties and play their respective roles in the family.…”

How early maternal deprivation changes the brain and behavior?

“…Female California mice exposed to paternal deprivation exhibit reduced cell survival in the hippocampal dentate gyrus, indicating increased hippocampal vulnerability and greater deficits in cognitive performance in females than males (Glasper et al., 2018). Studies in degus demonstrated that deprivation of paternal care alters neuronal connections in the limbic system and reduces the density of symmetric shaft synapses in the offspring (Ovtscharoff et al., 2006; de Schultz et al., 2020). Furthermore, deficits in OXT expression and poor communication between the prelimbic cortex and paraventricular nucleus have been found in both sexes of mandarin voles exposed to paternal deprivation, consistent with studies in humans and other animals (Bambico et al., 2015; He et al., 2017; Nephew, 2012; Rutter et al., 2001).…”