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Maternal cortisol is associated with neonatal amygdala microstructure and connectivity in a sexually dimorphic manner
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Abstract
The mechanisms linking maternal stress in pregnancy with infant neurodevelopment in a sexually dimorphic manner are poorly understood. We tested the hypothesis that maternal hypothalamic-pituitary-adrenal axis activity, measured by hair cortisol concentration (HCC), is associated with microstructure, structural connectivity, and volume of the infant amygdala. In 78 mother-infant dyads, maternal hair was sampled postnatally, and infants underwent magnetic resonance imaging at term-equivalent age. We found a relationship between maternal HCC and amygdala development that differed according to infant sex. Higher HCC was associated with higher left amygdala fractional anisotropy (β = 0.677, p=0.010), lower left amygdala orientation dispersion index (β = −0.597, p=0.034), and higher fractional anisotropy in connections between the right amygdala and putamen (β = 0.475, p=0.007) in girls compared to boys. Furthermore, altered amygdala microstructure was only observed in boys, with connectivity changes restricted to girls. Maternal cortisol during pregnancy is related to newborn amygdala architecture and connectivity in a sexually dimorphic manner. Given the fundamental role of the amygdala in the emergence of emotion regulation, these findings offer new insights into mechanisms linking maternal health with neuropsychiatric outcomes of children.
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In the citing paper
“negative associations between maternal cortisol and bilateral amygdala fractional anisotropy”
From Prenatal Social Determinants of Health: Narrative review of maternal environments and neonatal brain development (2024) · cites this paper as [56]
In the citing paper
“positive associations with right amygdala mean diffusivity”
From Prenatal Social Determinants of Health: Narrative review of maternal environments and neonatal brain development (2024) · cites this paper as [56]
In the citing paper
“No term vs. preterm effects, nor main effects of hair cortisol on structural connectivity measures, were observed.”
From Prenatal Social Determinants of Health: Narrative review of maternal environments and neonatal brain development (2024) · cites this paper as [56]
In the citing paper
“and right amygdala neurite density”
From Prenatal Social Determinants of Health: Narrative review of maternal environments and neonatal brain development (2024) · cites this paper as [56]
In the citing paper
“and orientation dispersion index in male infants only.”
From Prenatal Social Determinants of Health: Narrative review of maternal environments and neonatal brain development (2024) · cites this paper as [56]
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NODDI: Practical in vivo neurite orientation dispersion and density imaging of the human brain
Zhang, H., Schneider, T., Wheeler-Kingshott, C. A., & Alexander, D. C. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.03.072 · Cited by 3,288
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Potential problems with the interpretation of hair analysis results
Wennig, R. (2000) · Forensic Science International · doi:10.1016/s0379-0738(99)00146-2 · Cited by 677
Neurite dispersion: a new marker of multiple sclerosis spinal cord pathology?
Grussu, F., Schneider, T., Tur, C., Yates, R. L., Tachrount, M., Ianuş, A., Yiannakas, M. C., Newcombe, J., Zhang, H., Alexander, D. C., et al. (2017) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.445 · Cited by 291
Prenatal maternal depression associates with microstructure of right amygdala in neonates at birth.
Rifkin-Graboi, A., Bai, J., Chen, H., Hameed, W. B., Sim, L. W., Tint, M. T., Leutscher-Broekman, B., Chong, Y.-S., Gluckman, P. D., Fortier, M. V., et al. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2013.06.019 · Cited by 258
Graham, A. M., Rasmussen, J. M., Entringer, S., Ben Ward, E., Rudolph, M. D., Gilmore, J. H., Styner, M., Wadhwa, P. D., Fair, D. A., & Buss, C. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2018.06.023 · Cited by 203
Carpenter, T., Grecian, S. M., & Reynolds, R. M. (2017) · Journal of Developmental Origins of Health and Disease · doi:10.1017/s204017441600074x · Cited by 191
Self-citationWen, D. J., Poh, J. S., Ni, S. N., Chong, Y.-S., Chen, H., Kwek, K., Shek, L. P., Gluckman, P. D., Fortier, M. V., Meaney, M. J., et al. (2017) · Translational Psychiatry · doi:10.1038/tp.2017.74 · Cited by 186
Alterations in amygdala–prefrontal circuits in infants exposed to prenatal maternal depression
Posner, J., Cha, J., Roy, A. K., Peterson, B. S., Bansal, R., Gustafsson, H. C., Raffanello, E., Gingrich, J., & Monk, C. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.146 · Cited by 184 · cited 2×
“…from studies that have characterised maternal stress by symptomatology of depression and/or anxiety, which report alterations in amygdala volume (Wen et al., 2017), microstructure (Rifkin-Graboi et al., 2013), and functional and structural connectivity among offspring (Posner et al., 2016).”
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Lautarescu, A., Bonthrone, A. F., Pietsch, M., Batalle, D., Cordero-Grande, L., Tournier, J.-D., Christiaens, D., Hajnal, J. V., Chew, A., Falconer, S., et al. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02073-y · Cited by 29
Herzberg, M. P., & Smyser, C. D. (2024) · Pediatric Research · doi:10.1038/s41390-024-03345-7 · Cited by 22
Hashempour, N., Tuulari, J. J., Merisaari, H., Acosta, H., Lewis, J. D., Pelto, J., Scheinin, N. M., Fonov, V. S., Collins, D. L., Lehtola, S. J., et al. (2023) · European Journal of Neuroscience · doi:10.1111/ejn.15989 · Cited by 20
Metadata
- Authors
- Stoye, D. Q., Blesa, M., Sullivan, G., Galdi, P., Lamb, G. J., Black, G. S., Quigley, A. J., Thrippleton, M. J., Bastin, M. E., Reynolds, R. M., & Boardman, J. P.
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2020-11-24
- Volume
- 9
- ISSN
- 2050-084X
- Cited by
- 62
- References
- 14
- Language
- en
- Licence
- Funders
- Theirworld
- Medical Research Council (MRC G1002033)
- British Heart Foundation (RE/18/5/34216)
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