Associations between different dimensions of prenatal distress, neonatal hippocampal connectivity, and infant memory

Dustin Scheinost,Laraine Mcdonough,Bradley S Peterson,Marisa N Spann,Catherine Monk

doi:10.1038/s41386-020-0677-0

Abstract

Prenatal maternal distress—an umbrella concept encompassing multiple negative psychological states including stress, anxiety, and depression—is a substantial prenatal exposure. Consistent across preclinical and human studies, the hippocampus displays alterations due to prenatal distress. Nevertheless, most prenatal distress studies do not focus on multiple dimensions of, have not examined hippocampal functional connectivity in association with, and do not consider observer-based functional outcomes related to distress. We investigated the effects of different dimensions of prenatal distress in pregnant adolescents, a population at high risk for distress, in association with neonatal hippocampal connectivity and infant memory. In pregnant adolescents (n = 42), we collected four measures of distress (perceived stress, depression, pregnancy-specific distress, and 24-h ambulatory salivary cortisol) during the 2nd and 3rd trimesters. Resting-state imaging data were acquired in their infants at 40–44 weeks post-menstrual age. Functional connectivity was measured from hippocampal seeds. Memory abilities were obtained at 4 months using the mobile conjugate reinforcement task. Shared across different dimensions of maternal distress, increased 3rd trimester maternal distress associated with weaker hippocampal–cingulate cortex connectivity and stronger hippocampal–temporal lobe connectivity. Perceived stress inversely correlated while hippocampal–cingulate cortex connectivity positively correlated with infant memory. Increased cortisol—collected during the 2nd, but not the 3rd, trimester—associated with weaker hippocampal–cingulate cortex connectivity and stronger hippocampal–temporal lobe connectivity. Different dimensions of prenatal maternal distress likely contribute shared and unique effects to shaping infant brain and behavior.

Highlights

A broad range of studies have documented the sequelae of exposure to different types of prenatal distress—an umbrella concept encompassing multiple negative psychological states including stress, anxiety, and depression
With the exception of a small cluster of overlap between the maternal depression and pregnancy-specific distress clusters in the right temporal lobe (96 voxel; 53 mm3), all clusters were spatially distinct (Fig. S3). In this prospective study, we investigated the effects of different dimensions of prenatal maternal distress on hippocampal functional connectivity in neonates and infant memory at 4 months
As different dimensions of prenatal distress have been associated with distinct cognitive process, these results suggest that effects of prenatal distress on the developing brain could occur within different sub-pathways of the temporal lobe, with the mediating biological pathways and associated genes of risk to be determined

Summary

Introduction

A broad range of studies have documented the sequelae of exposure to different types of prenatal distress—an umbrella concept encompassing multiple negative psychological states including stress, anxiety, and depression. The hippocampus is a common candidate for investigations of the brain correlates of prenatal distress [17] It plays an important role in response inhibition, memory, and spatial cognition [18], is altered in many psychiatric disorders [19], and contains high levels of glucocorticoid receptors [17], which regulate distress-related homeostasis. In humans, increased prenatal maternal anxiety has been associated with smaller left hippocampus volumes in schoolage children [26] and slower growth of both hippocampi between birth and age 6 months [3] Despite this interest, previous studies have not examined hippocampal functional connectivity—or how the hippocampus functionally interacts with other brain regions— in neonates with respect to multiple dimensions of prenatal maternal distress. The functional interaction between anatomically distinct brain regions provides a powerful predictor of individual differences in cognition, behavior, and risk [27]

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