Bi-Parental Care Contributes to Sexually Dimorphic Neural Cell Genesis in the Adult Mammalian Brain

Abstract

Early life events can modulate brain development to produce persistent physiological and behavioural phenotypes that are transmissible across generations. However, whether neural precursor cells are altered by early life events, to produce persistent and transmissible behavioural changes, is unknown. Here, we show that bi-parental care, in early life, increases neural cell genesis in the adult rodent brain in a sexually dimorphic manner. Bi-parentally raised male mice display enhanced adult dentate gyrus neurogenesis, which improves hippocampal neurogenesis-dependent learning and memory. Female mice display enhanced adult white matter oligodendrocyte production, which increases proficiency in bilateral motor coordination and preference for social investigation. Surprisingly, single parent-raised male and female offspring, whose fathers and mothers received bi-parental care, respectively, display a similar enhancement in adult neural cell genesis and phenotypic behaviour. Therefore, neural plasticity and behavioural effects due to bi-parental care persist throughout life and are transmitted to the next generation.

Chronic early life stress alters developmental and adult neurogenesis and impairs cognitive function in mice

“…Strikingly, ES affected levels of survival of adult‐born neurons exclusively in males associated with (and determinant for) a more severely impaired cognitive performance in adult ES‐male mice compared with females. This is in line with previous clinical and preclinical studies indicating a higher sensitivity of males to ES (Llorente et al, ; Oomen et al, ; Frodl et al, ; Mak et al, ; Loi et al, ), again reinforcing the translational value of this ES model. It indeed appears that males are more vulnerable to develop mental diseases after exposure to ES.…”

“…A final issue that needs clarification is the emerging evidence for a sex-dependent effect of ES on hippocampal structure and function (Llorente et al, 2009;Oomen et al, 2009Oomen et al, , 2010Oomen et al, , 2011Frodl et al, 2010;Mak et al, 2013) with males generally being more vulnerable to ES. This phenomenon might underlie existing sex differences in stress-related psychopathologies such as schizophrenia and depression (Bale et al, 2010).…”

Fathering in rodents: Neurobiological substrates and consequences for offspring

“…They interpreted this as indicating higher neuroplasticity in the biparental species and higher glial plasticity in the uniparental species. Finally, a fascinating series of studies in the uniparental house mouse ( Mus ) indicated that interactions of adult male mice with their own pups stimulated neurogenesis in the father’s subventricular zone and dentate gyrus under the influence of prolactin signaling (Mak et al, 2013; Mak and Weiss, 2010). Some of the new cells matured into olfactory interneurons in the olfactory bulb, where they responded preferentially to offspring odors and appeared to subserve later recognition of mature offspring.…”

Maternal separation induces hippocampal changes in cadherin-1 (CDH-1) mRNA and recognition memory impairment in adolescent mice

“…In addition, considering data derived from studies that investigated the effects of MS on biological markers, it was demonstrated that differential patterns of neurobiological modifications in response to MS, such as high peripheral corticosterone levels, and reduced mRNA expression of glucocorticoid receptor MATERNAL SEPARATION, RECOGNITION MEMORY AND CADHERIN mRNA 5 and neurotrophins in brain areas related to learning and memory (Tractenberg et al, 2016). In addition, there are studies indicating that early-life experiences across the lifespan have longterm consequences on hippocampal structure and function (Lajud, Roque, Cajero, Gutiérrez-Ospina, & Torner, 2012;Lajud & Torner, 2015;Naninck et al, 2015), and other reports demonstrate that males are more susceptible to ELS than females (Loi, Koricka, Lucassen, & Joëls, 2014;Mak, Antle, Dyck, & Weiss, 2013). Although the exact sex-dependent mechanism that underlies ELS-induced effects on structural and functional plasticity of the hippocampus is not completely understood, the dynamic fluctuation of adult neurogenesis in hippocampal development in response to stress could promote spatiotemporal changes in synaptic interconnected networks, remaining functionally different throughout life (Mirescu, Peters, & Gould, 2004).…”