The maternal brain is more flexible and responsive at rest: effective connectivity of the parental caregiving network in postpartum mothers

Abstract

The field of neuroscience has largely overlooked the impact of motherhood on brain function outside the context of responses to infant stimuli. Here, we apply spectral dynamic causal modelling (spDCM) to resting-state fMRI data to investigate differences in brain function between a group of 40 first-time mothers at 1-year postpartum and 39 age- and education-matched women who have never been pregnant. Using spDCM, we investigate the directionality (top-down vs. bottom-up) and valence (inhibition vs excitation) of functional connections between six key left hemisphere brain regions implicated in motherhood: the dorsomedial prefrontal cortex, ventromedial prefrontal cortex, posterior cingulate cortex, parahippocampal gyrus, amygdala, and nucleus accumbens. We show a selective modulation of inhibitory pathways related to differences between (1) mothers and non-mothers, (2) the interactions between group and cognitive performance and (3) group and social cognition, and (4) differences related to maternal caregiving behaviour. Across analyses, we show consistent disinhibition between cognitive and affective regions suggesting more efficient, flexible, and responsive behaviour, subserving cognitive performance, social cognition, and maternal caregiving. Together our results support the interpretation of these key regions as constituting a parental caregiving network. The nucleus accumbens and the parahippocampal gyrus emerging as 'hub' regions of this network, highlighting the global importance of the affective limbic network for maternal caregiving, social cognition, and cognitive performance in the postpartum period.

Figure 1

(a.) Regions of interest. Six left-hemisphere Regions of Interest (ROIs), with MNI coordinates (x,y,z). Brain image created with BioRender. (b.) Previously reported differences in functional connectivity. Schematic diagram showing the extant functional connectivity literature in motherhood for selected regions of the parental caregiving brain network. Dashed lines represent connections which differ between mothers with and without postpartum depression, studies using task-based fMRI scans to derive connectivity are denoted with an asterisk. These known connections were used to formulate the study hypotheses. Abbreviations: PCC, posterior cingulate cortex; vmPFC, ventromedial prefrontal cortex; dmPFC, dorsomedial prefrontal cortex; PHG, parahippocampal gyrus; Amyg, amygdala; NAcc, nucleus accumbens.

Figure 2

Schematic diagram showing spDCM results for (a.) the main effect of group (mothers vs. non-mothers), (b.) the interaction effect of group-by-cognition, (c.) the interaction effect of group-by-social cognition, and (d.) the main effect of maternal caregiving in mothers only. Effect sizes, directionality and valence of all connections are reported in Tables 2, 3, 4, 5. All connections are inhibitory. Values represent effect sizes (see Tables 2, 3, 4, 5) in Hz. Blue lines depict decreased inhibition and red lines depict increased inhibition. Dashed lines represent connections that are attenuated when the model adjusts for wellbeing, and solid lines are connections which are present whether or not wellbeing is adjusted for. Abbreviations: PCC, posterior cingulate cortex; vmPFC, ventromedial prefrontal cortex; dmPFC, dorsomedial prefrontal cortex; PHG, parahippocampal gyrus; Amyg, amygdala; NAcc, nucleus accumbens.