Abstract
Reproduction induces changes within the brain to prepare for gestation and motherhood. However, the dynamic of these central changes and their relationships with the development of maternal behavior remain poorly understood. Here, we describe a longitudinal morphometric neuroimaging study in female mice between pre-gestation and weaning, using new magnetic resonance imaging (MRI) resources comprising a high-resolution brain template, its associated tissue priors (60-µm isotropic resolution) and a corresponding mouse brain atlas (1320 regions of interest). Using these tools, we observed transient hypertrophies not only within key regions controlling gestation and maternal behavior (medial preoptic area, bed nucleus of the stria terminalis), but also in the amygdala, caudate nucleus and hippocampus. Additionally, unlike females exhibiting lower levels of maternal care, highly maternal females developed transient hypertrophies in somatosensory, entorhinal and retrosplenial cortices among other regions. Therefore, coordinated and transient brain modifications associated with maternal performance occurred during gestation and lactation.
Highlights
Motherhood is among the most transformative experiences in the lives of female mammals
Decades of scientific research dedicated to the maternal brain have revealed a core neural circuitry that includes the medial preoptic area and the adjoining ventral part of the bed nucleus of the stria terminalis (BNSTv), which are highly critical for the onset of maternal behavior (Bridges, 2015; Kohl et al, 2017; Kohl and Dulac, 2018; Numan and Insel, 2003)
These internal factors induce rewiring of the maternal brain, Abbreviations: AC-PC, anterior commissure-posterior commissure; Australian Mouse Brain Mapping Consortium (AMBMC), Australian mouse brain mapping consortium; AOB, accessory olfactory bulb; BNST, bed nucleus of the stria terminalis; CNS, central nervous system; CSF, cerebrospinal fluid; DARTEL, diffeomorphic anatomical registration using exponentiated lie algebra; df, degree of freedom; FA, flip angle; FLASE, fast large-angle spin-echo; FoV, field of view; MRI, magnetic resonance imaging; MOB, main olfactory bulb; mPOA, medial preoptic area; GM, gray matter; GMC, gray matter concentration; PVN, paraventricular nucleus of the hypothalamus; RARE, rapid acquisition with relaxation enhancement; ROC, receiver operating characteristic; ROI, region of interest; TE, echo time; TR, repetition time; VBM, voxel-based morphometry; WM, white matter
Summary
Motherhood is among the most transformative experiences in the lives of female mammals. Functional modulations of the mPOA/BNSTv consistently disrupt maternal motivation and expression in numerous species (Lévy and Keller, 2009; Lonstein et al, 2015; Numan and Insel, 2003) This core maternal circuitry regulates maternal behavior through its direct projections to the ventral tegmental area, which promotes reward system activation (Numan and Insel, 2003; Numan and Stolzenberg, 2009), as well as through its connections with cortical regions, including the prefrontal cortex (Afonso et al, 2007; Febo, 2011; Pereira and Morrell, 2011). These internal factors induce rewiring of the maternal brain, Abbreviations: AC-PC, anterior commissure-posterior commissure; AMBMC, Australian mouse brain mapping consortium; AOB, accessory olfactory bulb; BNST, bed nucleus of the stria terminalis; CNS, central nervous system; CSF, cerebrospinal fluid; DARTEL, diffeomorphic anatomical registration using exponentiated lie algebra; df, degree of freedom; FA, flip angle; FLASE, fast large-angle spin-echo; FoV, field of view; MRI, magnetic resonance imaging; MOB, main olfactory bulb; mPOA, medial preoptic area; GM, gray matter; GMC, gray matter concentration; PVN, paraventricular nucleus of the hypothalamus; RARE, rapid acquisition with relaxation enhancement; ROC, receiver operating characteristic; ROI, region of interest; TE, echo time; TR, repetition time; VBM, voxel-based morphometry; WM, white matter
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