Abstract

Depression and anxiety are the most common mental health conditions during pregnancy and can impair the normal development of mother-infant interactions. These adversities are associated with low birth weight and increased risk of behavioural disorders in children. We recently reported reduced expression of the imprinted gene PATERNALLY EXPRESSED GENE 3 (PEG3) in placenta of human infants born to depressed mothers. Expression of Peg3 in the brain has previously been linked maternal behaviour in rodents, at least in some studies, with mutant dams neglecting their pups. However, in our human study decreased expression was in the placenta derived from the fetus. Here, we examined maternal behaviour in response to reduced expression of Peg3 in the feto-placental unit. Prenatally we found novelty reactivity was altered in wild-type females carrying litters with a null mutation in Peg3. This behavioural alteration was short-lived and there were no significant differences the transcriptomes of either the maternal hypothalamus or hippocampus at E16.5. In contrast, while maternal gross maternal care was intact postnatally, the exposed dams were significantly slower to retrieve their pups and displayed a marked increase in anxiety. We also observed a significant reduction in the isolation-induced ultrasonic vocalizations (USVs) emitted by mutant pups separated from their mothers. USVs are a form of communication known to elicit maternal care suggesting Peg3 mutant pups drive the deficit in maternal behaviour. These data support the hypothesis that reduced placental PEG3 in human pregnancies occurs as a consequence of prenatal depression but leaves scope for feto-placental Peg3 dosage, during gestation, influencing aspects of maternal behaviour.

Highlights

  • A recent UK study estimated that perinatal mental health problems cost the UK £8.1 billion each year with nearly threequarters of this cost related to adverse impacts on the child [1].Depression and anxiety are the most common mental health conditions associated with pregnancy, estimated to affect as many as one in five women [2,3] with the highest risk in women with a history of mental illness and those exposed to adverseReceived: November 13, 2017

  • ultrasonic vocalizations (USVs) are a form of communication known to elicit maternal care suggesting Peg3 mutant pups drive the deficit in maternal behaviour

  • We found no gross differences in quality of nest built after 1 h between WTWT, WTPeg3KO dams and nonpregnant females [v(2) 1⁄4 3.123, P 1⁄4 0.21; Fig. 1D]

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Summary

Introduction

A recent UK study estimated that perinatal mental health problems cost the UK £8.1 billion each year with nearly threequarters of this cost related to adverse impacts on the child [1].Depression and anxiety are the most common mental health conditions associated with pregnancy, estimated to affect as many as one in five women [2,3] with the highest risk in women with a history of mental illness and those exposed to adverseReceived: November 13, 2017. A recent UK study estimated that perinatal mental health problems cost the UK £8.1 billion each year with nearly threequarters of this cost related to adverse impacts on the child [1]. Depression and anxiety are the most common mental health conditions associated with pregnancy, estimated to affect as many as one in five women [2,3] with the highest risk in women with a history of mental illness and those exposed to adverse. Accepted: November 21, 2017 VC The Author(s) 2017.

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