Sex-specific association between infant caudate volumes and a polygenic risk score for major depressive disorder

doi:10.1002/jnr.24722

. 2020 Dec;98(12):2529-2540.

doi: 10.1002/jnr.24722. Epub 2020 Sep 9.

Sex-specific association between infant caudate volumes and a polygenic risk score for major depressive disorder

Henriette Acosta^{1

2}, Katri Kantojärvi^{3

4}, Jetro J Tuulari^{1

5

6

7}, John D Lewis⁸, Niloofar Hashempour¹, Noora M Scheinin^{1

5}, Satu J Lehtola¹, Vladimir S Fonov⁸, D Louis Collins⁸, Alan Evans⁸, Riitta Parkkola⁹, Tuire Lähdesmäki¹⁰, Jani Saunavaara¹¹, Harri Merisaari^{1

12

13}, Linnea Karlsson^{1

14}, Tiina Paunio^{3

4}, Hasse Karlsson^{1

5

14}

Affiliations

¹ FinnBrain Birth Cohort Study, Turku Brain and Mind Center, Department of Clinical Medicine, University of Turku, Turku, Finland.
² Department of Psychiatry and Psychotherapy, Philipps University of Marburg, Marburg, Germany.
³ Finnish Institute for Health and Welfare, Genomics and Biobank Unit, Helsinki, Finland.
⁴ Department of Psychiatry and SleepWell Research Program, Faculty of Medicine, University of Helsinki and Helsinki University Central Hospital, Helsinki, Finland.
⁵ Department of Psychiatry, University of Turku and Turku University Hospital, Turku, Finland.
⁶ Turku Collegium for Science and Medicine, University of Turku, Turku, Finland.
⁷ Department of Psychiatry, University of Oxford, Oxford, UK.
⁸ Montreal Neurological Institute, McGill University, Montreal, QC, Canada.
⁹ Department of Radiology, University of Turku and Turku University Hospital, Turku, Finland.
¹⁰ Department of Pediatric Neurology, University of Turku and Turku University Hospital, Turku, Finland.
¹¹ Department of Medical Physics, Turku University Hospital, Turku, Finland.
¹² Department of Future Technologies, University of Turku, Turku, Finland.
¹³ Center of Computational Imaging and Personalized Diagnostics, Case Western Reserve University, Cleveland, OH, USA.
¹⁴ Centre for Population Health Research, University of Turku and Turku University Hospital, Turku, Finland.

PMID: 32901998
DOI: 10.1002/jnr.24722

Free article

Sex-specific association between infant caudate volumes and a polygenic risk score for major depressive disorder

Henriette Acosta et al. J Neurosci Res. 2020 Dec.

Free article

. 2020 Dec;98(12):2529-2540.

doi: 10.1002/jnr.24722. Epub 2020 Sep 9.

Authors

Affiliations

¹ FinnBrain Birth Cohort Study, Turku Brain and Mind Center, Department of Clinical Medicine, University of Turku, Turku, Finland.
² Department of Psychiatry and Psychotherapy, Philipps University of Marburg, Marburg, Germany.
³ Finnish Institute for Health and Welfare, Genomics and Biobank Unit, Helsinki, Finland.
⁴ Department of Psychiatry and SleepWell Research Program, Faculty of Medicine, University of Helsinki and Helsinki University Central Hospital, Helsinki, Finland.
⁵ Department of Psychiatry, University of Turku and Turku University Hospital, Turku, Finland.
⁶ Turku Collegium for Science and Medicine, University of Turku, Turku, Finland.
⁷ Department of Psychiatry, University of Oxford, Oxford, UK.
⁸ Montreal Neurological Institute, McGill University, Montreal, QC, Canada.
⁹ Department of Radiology, University of Turku and Turku University Hospital, Turku, Finland.
¹⁰ Department of Pediatric Neurology, University of Turku and Turku University Hospital, Turku, Finland.
¹¹ Department of Medical Physics, Turku University Hospital, Turku, Finland.
¹² Department of Future Technologies, University of Turku, Turku, Finland.
¹³ Center of Computational Imaging and Personalized Diagnostics, Case Western Reserve University, Cleveland, OH, USA.
¹⁴ Centre for Population Health Research, University of Turku and Turku University Hospital, Turku, Finland.

PMID: 32901998
DOI: 10.1002/jnr.24722

Abstract

Polygenic risk scores for major depressive disorder (PRS-MDD) have been identified in large genome-wide association studies, and recent findings suggest that PRS-MDD might interact with environmental risk factors to shape human limbic brain development as early as in the prenatal period. Striatal structures are crucially involved in depression; however, the association of PRS-MDD with infant striatal volumes is yet unknown. In this study, 105 Finnish mother-infant dyads (44 female, 11-54 days old) were investigated to reveal how infant PRS-MDD is associated with infant dorsal striatal volumes (caudate, putamen) and whether PRS-MDD interacts with prenatal maternal depressive symptoms (Edinburgh Postnatal Depression Scale, gestational weeks 14, 24, 34) on infant striatal volumes. A robust sex-specific main effect of PRS-MDD on bilateral infant caudate volumes was observed. PRS-MDD were more positively associated with caudate volumes in boys compared to girls. No significant interaction effects of genotype PRS-MDD with the environmental risk factor "prenatal maternal depressive symptoms" (genotype-by-environment interaction) nor significant interaction effects of genotype with prenatal maternal depressive symptoms and sex (genotype-by-environment-by-sex interaction) were found for infant dorsal striatal volumes. Our study showed that a higher PRS-MDD irrespective of prenatal exposure to maternal depressive symptoms is associated with smaller bilateral caudate volumes, an indicator of greater susceptibility to major depressive disorder, in female compared to male infants. This sex-specific polygenic effect might lay the ground for the higher prevalence of depression in women compared to men.

Keywords: Gene-environment interaction; MRI; brain development; prenatal programming; striatum.

PubMed Disclaimer

Cited by

Subcortical brain volumes in young infants exposed to antenatal maternal depression: Findings from a South African birth cohort.
Groenewold NA, Wedderburn CJ, Pellowski JA, Fouché JP, Michalak L, Roos A, Woods RP, Narr KL, Zar HJ, Donald KA, Stein DJ. Groenewold NA, et al. Neuroimage Clin. 2022;36:103206. doi: 10.1016/j.nicl.2022.103206. Epub 2022 Sep 19. Neuroimage Clin. 2022. PMID: 36162238 Free PMC article.
Sex-Specific Effects of Birth Weight on Longitudinal Behavioral Outcomes: A Mendelian Randomization Approach Using Polygenic Scores.
Byg LM, Wang C, Attia J, Whitehouse A, Pennell C. Byg LM, et al. Biol Psychiatry Glob Open Sci. 2024 Aug 26;4(6):100387. doi: 10.1016/j.bpsgos.2024.100387. eCollection 2024 Nov. Biol Psychiatry Glob Open Sci. 2024. PMID: 39483322 Free PMC article.
Genetic Influences on the Developing Young Brain and Risk for Neuropsychiatric Disorders.
Alex AM, Buss C, Davis EP, Campos GL, Donald KA, Fair DA, Gaab N, Gao W, Gilmore JH, Girault JB, Grewen K, Groenewold NA, Hankin BL, Ipser J, Kapoor S, Kim P, Lin W, Luo S, Norton ES, O'Connor TG, Piven J, Qiu A, Rasmussen JM, Skeide MA, Stein DJ, Styner MA, Thompson PM, Wakschlag L, Knickmeyer R; ENIGMA ORIGINs group. Alex AM, et al. Biol Psychiatry. 2023 May 15;93(10):905-920. doi: 10.1016/j.biopsych.2023.01.013. Epub 2023 Jan 28. Biol Psychiatry. 2023. PMID: 36932005 Free PMC article. Review.
Depressive symptoms during the transition to adolescence: Left hippocampal volume as a marker of social context sensitivity.
Martinez M, Cai T, Yang B, Zhou Z, Shankman SA, Mittal VA, Haase CM, Qu Y. Martinez M, et al. Proc Natl Acad Sci U S A. 2024 Sep 10;121(37):e2321965121. doi: 10.1073/pnas.2321965121. Epub 2024 Sep 3. Proc Natl Acad Sci U S A. 2024. PMID: 39226358 Free PMC article.
Maternal depressive symptoms, neonatal white matter, and toddler social-emotional development.
Lautarescu A, Bonthrone AF, Pietsch M, Batalle D, Cordero-Grande L, Tournier JD, Christiaens D, Hajnal JV, Chew A, Falconer S, Nosarti C, Victor S, Craig MC, Edwards AD, Counsell SJ. Lautarescu A, et al. Transl Psychiatry. 2022 Aug 9;12(1):323. doi: 10.1038/s41398-022-02073-y. Transl Psychiatry. 2022. PMID: 35945202 Free PMC article.

See all "Cited by" articles

References

REFERENCES

1. Acosta, H., Kantojärvi, K., Hashempour, N., Pelto, J., Scheinin, N. M., Lehtola, S. J., … Tuulari, J. J. (2020). Partial support for an interaction between a polygenic risk score for major depressive disorder and prenatal maternal depressive symptoms on infant right amygdalar volumes. Cerebral Cortex. https://doi.org/10.1093/cercor/bhaa158
1. Acosta, H., Tuulari, J. J., Scheinin, N. M., Hashempour, N., Rajasilta, O., Lavonius, T. I., … Karlsson, H. (2019). Maternal pregnancy-related anxiety is associated with sexually dimorphic alterations in amygdala volume in four-year-old children. Frontiers in Behavioral Neuroscience, 13, 175. https://doi.org/10.3389/FNBEH.2019.00175
1. Amemori, K., Amemori, S., Gibson, D. J., & Graybiel, A. M. (2018). Striatal microstimulation induces persistent and repetitive negative decision-making predicted by striatal beta-band oscillation. Neuron, 99(4), 829-841. https://doi.org/10.1016/j.neuron.2018.07.022
1. Andersen, S. L., Thompson, A. P., Krenzel, E., & Teicher, M. H. (2002). Pubertal changes in gonadal hormones do not underlie adolescent dopamine receptor overproduction. Psychoneuroendocrinology, 27(6), 683-691. https://doi.org/10.1016/S0306-4530(01)00069-5
1. Arnone, D., McIntosh, A. M., Ebmeier, K. P., Munafò, M. R., & Anderson, I. M. (2012). Magnetic resonance imaging studies in unipolar depression: Systematic review and meta-regression analyses. European Neuropsychopharmacology, 22(1), 1-16. https://doi.org/10.1016/j.euroneuro.2011.05.003

Publication types

Actions

MeSH terms

Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions

Grants and funding

CIHR/Canada

LinkOut - more resources

Full Text Sources
Medical
- MedlinePlus Health Information

[1] Acosta, H., Kantojärvi, K., Hashempour, N., Pelto, J., Scheinin, N. M., Lehtola, S. J., … Tuulari, J. J. (2020). Partial support for an interaction between a polygenic risk score for major depressive disorder and prenatal maternal depressive symptoms on infant right amygdalar volumes. Cerebral Cortex. https://doi.org/10.1093/cercor/bhaa158

[2] Acosta, H., Kantojärvi, K., Hashempour, N., Pelto, J., Scheinin, N. M., Lehtola, S. J., … Tuulari, J. J. (2020). Partial support for an interaction between a polygenic risk score for major depressive disorder and prenatal maternal depressive symptoms on infant right amygdalar volumes. Cerebral Cortex. https://doi.org/10.1093/cercor/bhaa158

[3] Acosta, H., Tuulari, J. J., Scheinin, N. M., Hashempour, N., Rajasilta, O., Lavonius, T. I., … Karlsson, H. (2019). Maternal pregnancy-related anxiety is associated with sexually dimorphic alterations in amygdala volume in four-year-old children. Frontiers in Behavioral Neuroscience, 13, 175. https://doi.org/10.3389/FNBEH.2019.00175

[4] Acosta, H., Tuulari, J. J., Scheinin, N. M., Hashempour, N., Rajasilta, O., Lavonius, T. I., … Karlsson, H. (2019). Maternal pregnancy-related anxiety is associated with sexually dimorphic alterations in amygdala volume in four-year-old children. Frontiers in Behavioral Neuroscience, 13, 175. https://doi.org/10.3389/FNBEH.2019.00175

[5] Amemori, K., Amemori, S., Gibson, D. J., & Graybiel, A. M. (2018). Striatal microstimulation induces persistent and repetitive negative decision-making predicted by striatal beta-band oscillation. Neuron, 99(4), 829-841. https://doi.org/10.1016/j.neuron.2018.07.022

[6] Amemori, K., Amemori, S., Gibson, D. J., & Graybiel, A. M. (2018). Striatal microstimulation induces persistent and repetitive negative decision-making predicted by striatal beta-band oscillation. Neuron, 99(4), 829-841. https://doi.org/10.1016/j.neuron.2018.07.022

[7] Andersen, S. L., Thompson, A. P., Krenzel, E., & Teicher, M. H. (2002). Pubertal changes in gonadal hormones do not underlie adolescent dopamine receptor overproduction. Psychoneuroendocrinology, 27(6), 683-691. https://doi.org/10.1016/S0306-4530(01)00069-5

[8] Andersen, S. L., Thompson, A. P., Krenzel, E., & Teicher, M. H. (2002). Pubertal changes in gonadal hormones do not underlie adolescent dopamine receptor overproduction. Psychoneuroendocrinology, 27(6), 683-691. https://doi.org/10.1016/S0306-4530(01)00069-5

[9] Arnone, D., McIntosh, A. M., Ebmeier, K. P., Munafò, M. R., & Anderson, I. M. (2012). Magnetic resonance imaging studies in unipolar depression: Systematic review and meta-regression analyses. European Neuropsychopharmacology, 22(1), 1-16. https://doi.org/10.1016/j.euroneuro.2011.05.003

[10] Arnone, D., McIntosh, A. M., Ebmeier, K. P., Munafò, M. R., & Anderson, I. M. (2012). Magnetic resonance imaging studies in unipolar depression: Systematic review and meta-regression analyses. European Neuropsychopharmacology, 22(1), 1-16. https://doi.org/10.1016/j.euroneuro.2011.05.003

Save citation to file

Email citation

Add to Collections

Add to My Bibliography

Your saved search

Create a file for external citation management software

Your RSS Feed

Sex-specific association between infant caudate volumes and a polygenic risk score for major depressive disorder

Affiliations

Sex-specific association between infant caudate volumes and a polygenic risk score for major depressive disorder

Authors

Affiliations

Abstract

Similar articles

Cited by

References

REFERENCES

Publication types

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources

Medical

Abstract

Similar articles

Cited by

References

REFERENCES

Publication types

MeSH terms

Related information

Grants and funding

LinkOut - more resources

Full Text Sources

Medical