Birth of the blues: Emotional sound processing in infants exposed to prenatal maternal depression

Michael C. Craig; Vaheshta Sethna; Maria Gudbrandsen; Carmine M. Pariante; Trudi Seneviratne; Vladimira Stoencheva; Arjun Sethi; Marco Catani; Mick Brammer; Declan G.M. Murphy; Eileen Daly

doi:10.1017/S0033291720002688

Birth of the blues: Emotional sound processing in infants exposed to prenatal maternal depression

Michael C. Craig^*, Vaheshta Sethna, Maria Gudbrandsen, Carmine M. Pariante, Trudi Seneviratne, Vladimira Stoencheva, Arjun Sethi, Marco Catani, Mick Brammer, Declan G.M. Murphy, Eileen Daly

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

5 Citations (Scopus)

Abstract

Background Offspring exposed to prenatal maternal depression (PMD) are vulnerable to depression across their lifespan. The underlying cause(s) for this elevated intergenerational risk is most likely complex. However, depression is underpinned by a dysfunctional frontal-limbic network, associated with core information processing biases (e.g. attending more to sad stimuli). Aberrations in this network might mediate transmission of this vulnerability in infants exposed to PMD. In this study, we aimed to explore the association between foetal exposure to PMD and frontal-limbic network function in infancy, hypothesising that, in response to emotional sounds, infants exposed to PMD would exhibit atypical activity in these regions, relative to those not exposed to PMD. Method We employed a novel functional magnetic resonance imaging sequence to compare brain function, whilst listening to emotional sounds, in 78 full-Term infants (3-6 months of age) born to mothers with and without a diagnosis of PMD. Results After exclusion of 19 datasets due to infants waking up, or moving excessively, we report between-group brain activity differences, between 29 infants exposed to PMD and 29 infants not exposed to PMD, occurring in temporal, striatal, amygdala/parahippocampal and frontal regions (p < 0.005). The offspring exposed to PMD exhibited a relative increase in activation to sad sounds and reduced (or unchanged) activation to happy sounds in frontal-limbic clusters. Conclusions Findings of a differential response to positive and negative valanced sounds by 3-6 months of age may have significant implications for our understanding of neural mechanisms that underpin the increased risk for later-life depression in this population.

Original language	English
Pages (from-to)	2017-2023
Number of pages	7
Journal	Psychological Medicine
Volume	52
Issue number	11
DOIs	https://doi.org/10.1017/S0033291720002688
Publication status	Published - 4 Aug 2022

Keywords

Emotional sounds
fMRI
infants
prenatal maternal depression

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10.1017/S0033291720002688

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@article{08186babf56045fd99d209d80ae7584a,

title = "Birth of the blues: Emotional sound processing in infants exposed to prenatal maternal depression",

abstract = "Background Offspring exposed to prenatal maternal depression (PMD) are vulnerable to depression across their lifespan. The underlying cause(s) for this elevated intergenerational risk is most likely complex. However, depression is underpinned by a dysfunctional frontal-limbic network, associated with core information processing biases (e.g. attending more to sad stimuli). Aberrations in this network might mediate transmission of this vulnerability in infants exposed to PMD. In this study, we aimed to explore the association between foetal exposure to PMD and frontal-limbic network function in infancy, hypothesising that, in response to emotional sounds, infants exposed to PMD would exhibit atypical activity in these regions, relative to those not exposed to PMD. Method We employed a novel functional magnetic resonance imaging sequence to compare brain function, whilst listening to emotional sounds, in 78 full-Term infants (3-6 months of age) born to mothers with and without a diagnosis of PMD. Results After exclusion of 19 datasets due to infants waking up, or moving excessively, we report between-group brain activity differences, between 29 infants exposed to PMD and 29 infants not exposed to PMD, occurring in temporal, striatal, amygdala/parahippocampal and frontal regions (p < 0.005). The offspring exposed to PMD exhibited a relative increase in activation to sad sounds and reduced (or unchanged) activation to happy sounds in frontal-limbic clusters. Conclusions Findings of a differential response to positive and negative valanced sounds by 3-6 months of age may have significant implications for our understanding of neural mechanisms that underpin the increased risk for later-life depression in this population. ",

keywords = "Emotional sounds, fMRI, infants, prenatal maternal depression",

author = "Craig, {Michael C.} and Vaheshta Sethna and Maria Gudbrandsen and Pariante, {Carmine M.} and Trudi Seneviratne and Vladimira Stoencheva and Arjun Sethi and Marco Catani and Mick Brammer and Murphy, {Declan G.M.} and Eileen Daly",

note = "Funding Information: This current study was funded by a grant awarded to MCC by the Psychiatry Research Trust. MCC is also currently funded by the Medical Research Council UK (Grant MR/M013588). Funding also provided by EU-AIMS (European Autism Interventions)/EU AIMS-2-TRIALS, a European Innovative Medicines Joint Undertaking under Grant agreements No. 115300 and 777394, the resources of which are composed of financial contributions from the European Union's Seventh Framework Programme (Grant FP7/2007-2013). We would like to thank the National Institute for Health Research (NIHR) Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King's College London for their ongoing support. Publisher Copyright: Copyright {\textcopyright} The Author(s), 2020. Published by Cambridge University Press.",

year = "2022",

month = aug,

day = "4",

doi = "10.1017/S0033291720002688",

language = "English",

volume = "52",

pages = "2017--2023",

journal = "Psychological Medicine",

issn = "0033-2917",

publisher = "Cambridge University Press",

number = "11",

}

TY - JOUR

T1 - Birth of the blues

T2 - Emotional sound processing in infants exposed to prenatal maternal depression

AU - Craig, Michael C.

AU - Sethna, Vaheshta

AU - Gudbrandsen, Maria

AU - Pariante, Carmine M.

AU - Seneviratne, Trudi

AU - Stoencheva, Vladimira

AU - Sethi, Arjun

AU - Catani, Marco

AU - Brammer, Mick

AU - Murphy, Declan G.M.

AU - Daly, Eileen

N1 - Funding Information: This current study was funded by a grant awarded to MCC by the Psychiatry Research Trust. MCC is also currently funded by the Medical Research Council UK (Grant MR/M013588). Funding also provided by EU-AIMS (European Autism Interventions)/EU AIMS-2-TRIALS, a European Innovative Medicines Joint Undertaking under Grant agreements No. 115300 and 777394, the resources of which are composed of financial contributions from the European Union's Seventh Framework Programme (Grant FP7/2007-2013). We would like to thank the National Institute for Health Research (NIHR) Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King's College London for their ongoing support. Publisher Copyright: Copyright © The Author(s), 2020. Published by Cambridge University Press.

PY - 2022/8/4

Y1 - 2022/8/4

N2 - Background Offspring exposed to prenatal maternal depression (PMD) are vulnerable to depression across their lifespan. The underlying cause(s) for this elevated intergenerational risk is most likely complex. However, depression is underpinned by a dysfunctional frontal-limbic network, associated with core information processing biases (e.g. attending more to sad stimuli). Aberrations in this network might mediate transmission of this vulnerability in infants exposed to PMD. In this study, we aimed to explore the association between foetal exposure to PMD and frontal-limbic network function in infancy, hypothesising that, in response to emotional sounds, infants exposed to PMD would exhibit atypical activity in these regions, relative to those not exposed to PMD. Method We employed a novel functional magnetic resonance imaging sequence to compare brain function, whilst listening to emotional sounds, in 78 full-Term infants (3-6 months of age) born to mothers with and without a diagnosis of PMD. Results After exclusion of 19 datasets due to infants waking up, or moving excessively, we report between-group brain activity differences, between 29 infants exposed to PMD and 29 infants not exposed to PMD, occurring in temporal, striatal, amygdala/parahippocampal and frontal regions (p < 0.005). The offspring exposed to PMD exhibited a relative increase in activation to sad sounds and reduced (or unchanged) activation to happy sounds in frontal-limbic clusters. Conclusions Findings of a differential response to positive and negative valanced sounds by 3-6 months of age may have significant implications for our understanding of neural mechanisms that underpin the increased risk for later-life depression in this population.

AB - Background Offspring exposed to prenatal maternal depression (PMD) are vulnerable to depression across their lifespan. The underlying cause(s) for this elevated intergenerational risk is most likely complex. However, depression is underpinned by a dysfunctional frontal-limbic network, associated with core information processing biases (e.g. attending more to sad stimuli). Aberrations in this network might mediate transmission of this vulnerability in infants exposed to PMD. In this study, we aimed to explore the association between foetal exposure to PMD and frontal-limbic network function in infancy, hypothesising that, in response to emotional sounds, infants exposed to PMD would exhibit atypical activity in these regions, relative to those not exposed to PMD. Method We employed a novel functional magnetic resonance imaging sequence to compare brain function, whilst listening to emotional sounds, in 78 full-Term infants (3-6 months of age) born to mothers with and without a diagnosis of PMD. Results After exclusion of 19 datasets due to infants waking up, or moving excessively, we report between-group brain activity differences, between 29 infants exposed to PMD and 29 infants not exposed to PMD, occurring in temporal, striatal, amygdala/parahippocampal and frontal regions (p < 0.005). The offspring exposed to PMD exhibited a relative increase in activation to sad sounds and reduced (or unchanged) activation to happy sounds in frontal-limbic clusters. Conclusions Findings of a differential response to positive and negative valanced sounds by 3-6 months of age may have significant implications for our understanding of neural mechanisms that underpin the increased risk for later-life depression in this population.

KW - Emotional sounds

KW - fMRI

KW - infants

KW - prenatal maternal depression

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U2 - 10.1017/S0033291720002688

DO - 10.1017/S0033291720002688

M3 - Article

AN - SCOPUS:85137301170

SN - 0033-2917

VL - 52

SP - 2017

EP - 2023

JO - Psychological Medicine

JF - Psychological Medicine

IS - 11

ER -

Birth of the blues: Emotional sound processing in infants exposed to prenatal maternal depression

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Keywords

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