Association between duration of breastfeeding based on maternal reports and dorsal and ventral striatum and medial orbital gyrus volumes in early adolescence

Daisuke Koshiyama; Naohiro Okada; Shuntaro Ando; Shinsuke Koike; Noriaki Yahata; Kentaro Morita; Kingo Sawada; Susumu Morita; Shintaro Kawakami; Sho Kanata; Shinya Fujikawa; Noriko Sugimoto; Rie Toriyama; Mio Masaoka; Tsuyoshi Araki; Yukiko Kano; Kaori Endo; Syudo Yamasaki; Atsushi Nishida; Mariko Hiraiwa-Hasegawa; Kiyoto Kasai

doi:10.1016/j.neuroimage.2020.117083

Association between duration of breastfeeding based on maternal reports and dorsal and ventral striatum and medial orbital gyrus volumes in early adolescence

Neuroimage. 2020 Oct 15:220:117083. doi: 10.1016/j.neuroimage.2020.117083. Epub 2020 Jun 25.

Authors

Daisuke Koshiyama¹, Naohiro Okada², Shuntaro Ando³, Shinsuke Koike⁴, Noriaki Yahata⁵, Kentaro Morita¹, Kingo Sawada⁶, Susumu Morita¹, Shintaro Kawakami¹, Sho Kanata⁷, Shinya Fujikawa¹, Noriko Sugimoto¹, Rie Toriyama¹, Mio Masaoka¹, Tsuyoshi Araki¹, Yukiko Kano⁸, Kaori Endo⁹, Syudo Yamasaki⁹, Atsushi Nishida⁹, Mariko Hiraiwa-Hasegawa¹⁰, Kiyoto Kasai¹¹

Affiliations

¹ Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan.
² Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan; The International Research Center for Neurointelligence (WPI-IRCN), University of Tokyo Institutes for Advanced Study (UTIAS), The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan.
³ Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan; Department of Psychiatry and Behavioral Sciences, Tokyo Metropolitan Institute of Medical Science, 2-1-6 Kamikitazawa, Setagaya-ku, Tokyo, 156-8506, Japan.
⁴ Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan; The International Research Center for Neurointelligence (WPI-IRCN), University of Tokyo Institutes for Advanced Study (UTIAS), The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan; University of Tokyo Institute for Diversity & Adaptation of Human Mind (UTIDAHM), 3-8-1, Komaba, Meguro-ku, Tokyo, 153-8902, Japan; Center for Evolutionary Cognitive Sciences, Graduate School of Art and Sciences, The University of Tokyo, 3-8-1, Komaba, Meguro-ku, Tokyo, 153-8902, Japan.
⁵ Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan; Institute for Quantum Life Science, National Institutes for Quantum and Radiological Science and Technology, 4-9-1 Anagawa, Inage-ku, Chiba, 263-8555, Japan; Department of Molecular Imaging and Theranostics, National Institute of Radiological Sciences, National Institutes for Quantum and Radiological Science and Technology, 4-9-1 Anagawa, Inage-ku, Chiba, 263-8555, Japan.
⁶ Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan; Office for Mental Health Support, University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan.
⁷ Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan; Department of Psychiatry, Teikyo University School of Medicine 2-11-1 Kaga Itabashi-ku, Tokyo, 173-8605, Japan.
⁸ Department of Child Psychiatry, Graduate School of Medicine, The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan.
⁹ Department of Psychiatry and Behavioral Sciences, Tokyo Metropolitan Institute of Medical Science, 2-1-6 Kamikitazawa, Setagaya-ku, Tokyo, 156-8506, Japan.
¹⁰ Department of Evolutionary Studies of Biosystems, School of Advanced Sciences, The Graduate University for Advanced Studies (SOKENDAI), Shonan Village, Hayama, Kanagawa, 240-0193, Japan.
¹¹ Department of Neuropsychiatry, Graduate School of Medicine, The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo, 113-8655, Japan; The International Research Center for Neurointelligence (WPI-IRCN), University of Tokyo Institutes for Advanced Study (UTIAS), The University of Tokyo, 7-3-1, Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan. Electronic address: kasaik-tky@umin.net.

PMID: 32593803
DOI: 10.1016/j.neuroimage.2020.117083

Abstract

Maternal breastfeeding has an impact on motor and emotional development in children of the next generation. Elucidating how breastfeeding during infancy affects brain regional structural development in early adolescence will be helpful for promoting healthy development. However, previous studies that have shown relationships between breastfeeding during infancy and cortical brain regions in adolescence are usually based on maternal retrospective recall of breastfeeding, and the accuracy of the data is unclear. In this study, we investigated the association between breastfeeding duration and brain regional volume in a population-neuroimaging study of early adolescents in Japan (N = 207; 10.5-13.4 years) using voxel-based morphometry, which enabled us to analyze the whole brain. We evaluated breastfeeding duration as indexed by maternal and child health handbook records during infancy. The results showed a significant positive correlation between the duration of breastfeeding and gray matter volume in the dorsal and ventral striatum and the medial orbital gyrus. Post hoc exploratory analyses revealed that the duration of breastfeeding was significantly correlated with emotional behavior. Additionally, the volume in the medial orbital gyrus mediated an association between breastfeeding duration and emotional behavior. This is the first study to evaluate the effect of breastfeeding during infancy on regional brain volumes in early adolescence based on maternal and child health handbook records. Our findings shed light upon the importance of maternal breastfeeding for brain development related to emotional and motivational processing in early adolescence.

Keywords: Breastfeeding; Dorsal and ventral striatum; Emotional behavior; Maternal and child health handbook; Medial orbital gyrus; Voxel-based morphometry (VBM).

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Adolescent
Breast Feeding*
Child
Corpus Striatum / diagnostic imaging*
Female
Gray Matter / diagnostic imaging*
Humans
Image Processing, Computer-Assisted
Magnetic Resonance Imaging
Male
Organ Size / physiology
Prefrontal Cortex / diagnostic imaging*
Retrospective Studies
Time Factors