Interrelated effects of age and parenthood on whole-brain controllability: protective effects of parenthood in mothers

Abstract

Background: Controllability is a measure of the brain's ability to orchestrate neural activity which can be quantified in terms of the properties of the brain network connectivity. Evidence from the literature suggests that aging can exert a general effect on whole-brain controllability. Mounting evidence, on the other hand, suggests that parenthood and motherhood in particular lead to long-lasting changes in brain architecture that effectively slow down brain aging. We hypothesize that parenthood might preserve brain controllability properties from aging. Methods: In a sample of 814 healthy individuals (aged 33.9 ± 12.7 years, 522 females), we estimate whole-brain controllability and compare the aging effects in subjects with vs. those without children. We use diffusion tensor imaging (DTI) to estimate the brain structural connectome. The level of brain control is then calculated from the connectomic properties of the brain structure. Specifically, we measure the network control over many low-energy state transitions (average controllability) and the network control over difficult-to-reach states (modal controllability). Results and conclusion: In nulliparous females, whole-brain average controllability increases, and modal controllability decreases with age, a trend that we do not observe in parous females. Statistical comparison of the controllability metrics shows that modal controllability is higher and average controllability is lower in parous females compared to nulliparous females. In men, we observed the same trend, but the difference between nulliparous and parous males do not reach statistical significance. Our results provide strong evidence that parenthood contradicts aging effects on brain controllability and the effect is stronger in mothers.

Protective role of parenthood on age-related brain function in mid- to late-life

“…Critically, we find that for both females and males, patterns of parenthood-related brain function are in the opposite direction to those associated with aging, which showed lower functional connectivity across the somato/motor network and higher connectivity within cortico-subcortical systems with age. Our findings closely align with past human [26][27][28][29][30][31][32][33] and animal [34][35][36][37] work suggesting long-term neuroprotection related to parenthood throughout the lifespan.…”

“…This finding, though striking, is in line with our hypothesis, as well as the current understanding of the enduring impact of parenthood on the parental brain in humans [27][28][29][30][31][32] and animals [34][35][36] . Indeed, a growing literature examining brain structure in later life parenthood demonstrates 'younger-looking' brains in adults with more children [27][28][29][30][31][32][33] , painting a consistent picture of parity-related protection for the structure of the adult brain. These studies similarly show an association between parity and 'younger-looking' grey matter [27][28][29][30][31] and white matter 32,33 for mothers, as well as grey matter for fathers 30 .…”

“…Indeed, a growing literature examining brain structure in later life parenthood demonstrates 'younger-looking' brains in adults with more children [27][28][29][30][31][32][33] , painting a consistent picture of parity-related protection for the structure of the adult brain. These studies similarly show an association between parity and 'younger-looking' grey matter [27][28][29][30][31] and white matter 32,33 for mothers, as well as grey matter for fathers 30 . In gestational mothers, similar evidence of this 'youngerlooking' brain structure has been shown as early as 4-6 weeks following birth 78 .…”

Controlling target brain regions by optimal selection of input nodes

“…Thus, a replication in a different data set involving a larger cohort and longer recordings may considerably strengthen our analysis. A larger cohort would possibly allow linking control properties (such as driver and target energies) with individual traits, e.g., demographic data, allowing to look for age-, sex- and parenthood-related effects ([ 71 , 90 ]). Parcellation .…”

Network controllability measures of subnetworks: implications for neurosciences

“…For this and similar questions, assuming linear temporal dynamics, network control theory provides a set of measures that mathematically quantify the relevance of the nodes 17 . Specifically, average-, and modal-controllability are among the most widely measures used in neurosciences to study neural 9,10,[18][19][20] as well as psychological symptom dynamics 21,22 and are suggested to measure the overall power of nodes to affect network dynamics (see Karrer et. al.…”