Maternal experience and adult neurogenesis in mammals: Implications for maternal care, cognition, and mental health

Abstract

The transition to motherhood encompasses physiological and behavioral adaptations essential for the initiation and maintenance of offspring care and feeding and includes widespread changes throughout the brain. The growth of new neurons occurs across the lifespan in distinct regions of mammalian brains and changes dynamically across reproductive events in female mammals. The subventricular zone (SVZ) and dentate gyrus (DG) of the hippocampus undergo high rates of neurogenesis in adulthood and are sensitive to hormonal fluctuations. Pregnancy and the postpartum period are associated with increased cell proliferation in the SVZ and interneuron survival in the olfactory bulb. In mice, peripartum prolactin signaling mediates SVZ neurogenesis and is important for enhanced olfactory recognition of offspring and maternal care. In contrast, cell proliferation and immature neuron survival decrease in the DG during the postpartum period. High baseline glucocorticoid concentrations suppress hippocampal neurogenesis, potentially representing an energetic trade-off accompanying a reduced need for spatial navigation early postpartum. In women, hippocampal volume decline during pregnancy and partial recovery during the postpartum period could contribute to the risk of psychiatric illness. New evidence indicates that the dorsal raphe nucleus (DR) is an additional site for adult neurogenesis sensitive to reproductive experience and offspring contact. In this review, we discuss the initial and lasting impact of maternal experience on adult neurogenesis. Because neurogenesis has been implicated in a variety of psychiatric and neurodegenerative illnesses, understanding how reproductive experience alters new neuron production in maternal mammals has far-reaching implications for women's health and wellness across the lifespan.

Diacylglycerol lipase alpha in astrocytes is involved in maternal care and affective behaviors

“…All available astrocyte specific promoters, including the GLAST, GFAP and Aldh1l1 promoters, are active in neural progenitor cells of aduIt mice (Foo & Dougherty, 2013; Mori et al, 2006). It is therefore possible that deletion of Dagla in these cells modulates affective behaviors (Gao et al, 2010; Jenniches et al, 2016; Medina & Workman, 2018; Miller & Hen, 2015). To exclude this alternative hypothesis an inducible Cre‐deleter strain that is exclusively active in neuronal progenitor cells would be required.…”

Pregnancy Promotes Maternal Hippocampal Neurogenesis in Guinea Pigs

“…Neuroplasticity in association with pregnancy and postpartal experience consists of an important subject of research in reproductive neurobiology, which may be relevant to mental health in humans even at old ages [36, 81–83]. Although the basic hormonal and neuroendocrine mechanisms regulating reproduction would be very likely conserved through evolution, there exist remarkable differences between mammalian species or even substrains of the same species regarding motherhood (or more generally parenthood) behavior [25, 33, 84–90]. Therefore, it is important to explore basic issues of neuroplasticity in partnership with pregnancy, such as adult neurogenesis, in multiple animal species.…”

“…Future studies are needed to further explore the alteration of adult hippocampal neurogenesis during pregnancy among mammalian species, as well as the regulatory mechanism and implications thereof. For instances, adult neurogenesis, cognitive functions, and behavior are related to or modified by age and likely motherhood experience [3, 25, 106–109]. Because our experiments were carried out in primigravidas at young adulthood, it remains unknown if such an effect exists in multiparous females.…”

“…Motherhood is a dramatic life event in female and is associated with extensive neurobiological, cognitive, and behavioral changes involving multiple functional aspects such as learning and memory, development of mother-young bond, and nurture and anxious protection for the offspring [30–35]. These changes are facilitated by complex modulation in neuroanatomical, neurochemical, endocrinal, and immunological systems during pregnancy and after giving birth, ultimately to promote species survival and flourish [25, 36]. Reciprocal influences between maternal reproductive experience and neuroplasticity in various brain regions have been demonstrated or proposed in animal and human studies [31, 37–45].…”

Toward improved research on peripartum depression

“…Their review synthesizes the extensive cross‐species literature, pointing to increased cell proliferation in certain parts of the hippocampus and the olfactory bulb, and decreased neuron survival in other areas of the hippocampus in the postpartum period. In addition, the authors also discuss how the pregnancy‐induced changes tie to maternal behavior and mental health (Medina & Workman, 2018). These findings are incredibly important as we are just starting to unravel structural brain changes also in newly delivered women.…”