The impact of pre-adulthood urbanicity on hippocampal subfield volumes and neurocognitive abilities in young adults

Mengge Liu; Tong Han; Yue Wu; Jingliang Cheng; Longjiang Zhang; Bing Zhang; Xi-Nian Zuo; Wenzhen Zhu; Shijun Qiu; Zuojun Geng; Xiaochu Zhang; Guangbin Cui; Quan Zhang; Yongqiang Yu; Hui Zhang; Bo Gao; Xiaojun Xu; Zhenwei Yao; Wen Qin; Meng Liang; Feng Liu; Lining Guo; Qiang Xu; Jilian Fu; Jiayuan Xu; Jie Tang; Nana Liu; Kaizhong Xue; Peng Zhang; Wei Li; Dapeng Shi; Caihong Wang; Jia-Hong Gao; Su Lui; Zhihan Yan; Feng Chen; Jiance Li; Jing Zhang; Wen Shen; Yanwei Miao; Junfang Xian; Le Yu; Kai Xu; Meiyun Wang; Zhaoxiang Ye; Wei-Hua Liao; Dawei Wang; Chunshui Yu

doi:10.1016/j.envint.2023.107905

The impact of pre-adulthood urbanicity on hippocampal subfield volumes and neurocognitive abilities in young adults

Environ Int. 2023 Apr:174:107905. doi: 10.1016/j.envint.2023.107905. Epub 2023 Mar 30.

Authors

Mengge Liu¹, Tong Han², Yue Wu³, Jingliang Cheng⁴, Longjiang Zhang⁵, Bing Zhang⁶, Xi-Nian Zuo⁷, Wenzhen Zhu⁸, Shijun Qiu⁹, Zuojun Geng¹⁰, Xiaochu Zhang¹¹, Guangbin Cui¹², Quan Zhang¹³, Yongqiang Yu¹⁴, Hui Zhang¹⁵, Bo Gao¹⁶, Xiaojun Xu¹⁷, Zhenwei Yao³, Wen Qin¹, Meng Liang¹⁸, Feng Liu¹, Lining Guo¹, Qiang Xu¹, Jilian Fu¹, Jiayuan Xu¹, Jie Tang¹, Nana Liu¹, Kaizhong Xue¹, Peng Zhang¹⁹, Wei Li¹⁹, Dapeng Shi²⁰, Caihong Wang⁴, Jia-Hong Gao²¹, Su Lui²², Zhihan Yan²³, Feng Chen²⁴, Jiance Li²⁵, Jing Zhang²⁶, Wen Shen²⁷, Yanwei Miao²⁸, Junfang Xian²⁹, Le Yu³⁰, Kai Xu³¹, Meiyun Wang²⁰, Zhaoxiang Ye¹⁹, Wei-Hua Liao³², Dawei Wang³³, Chunshui Yu³⁴

Affiliations

¹ Department of Radiology and Tianjin Key Laboratory of Functional Imaging, Tianjin Medical University General Hospital, 300052 Tianjin, China.
² Department of Radiology, Tianjin Huanhu Hospital, 300350 Tianjin, China.
³ Department of Radiology, Huashan Hospital, Fudan University, 200040 Shanghai, China.
⁴ Department of Magnetic Resonance Imaging, The First Affiliated Hospital of Zhengzhou University, 450052 Zhengzhou, China.
⁵ Department of Medical Imaging, Jinling Hospital, Medical School of Nanjing University, 210002 Nanjing, China.
⁶ Department of Radiology, Drum Tower Hospital, Medical School of Nanjing University, 210008 Nanjing, China.
⁷ IDG/McGovern Institute for Brain Research, Beijing Normal University, 100875 Beijing, China; Institute of Psychology, Chinese Academy of Sciences, 100101 Beijing, China.
⁸ Department of Radiology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, 430030 Wuhan, China.
⁹ Department of Medical Imaging, the First Affiliated Hospital of Guangzhou University of Traditional Chinese Medicine, 510405 Guangzhou, China.
¹⁰ Department of Medical Imaging, The Second Hospital of Hebei Medical University, 050000 Shijiazhuang, China.
¹¹ Division of Life Science and Medicine, University of Science & Technology of China, 230027 Hefei, China.
¹² Functional and Molecular Imaging Key Lab of Shaanxi Province & Department of Radiology, Tangdu Hospital, Air Force Medical University, 710038 Xi'an, China.
¹³ Department of Radiology, Characteristic Medical Center of Chinese People's Armed Police Force, 300162 Tianjin, China.
¹⁴ Department of Radiology, The First Affiliated Hospital of Anhui Medical University, 230022 Hefei, China.
¹⁵ Department of Radiology, The First Hospital of Shanxi Medical University, 030001 Taiyuan, China.
¹⁶ Department of Radiology, The Affiliated Hospital of Guizhou Medical University, 550004 Guiyang, China; Department of Radiology, Yantai Yuhuangding Hospital, 264000 Yantai, China.
¹⁷ Department of Radiology, The Second Affiliated Hospital of Zhejiang University, School of Medicine, 310009 Hangzhou, China.
¹⁸ School of Medical Imaging and Tianjin Key Laboratory of Functional Imaging, Tianjin Medical University, 300203 Tianjin, China.
¹⁹ Department of Radiology, Tianjin Medical University Cancer Institute and Hospital, 300060 Tianjin, China.
²⁰ Department of Radiology, Henan Provincial People's Hospital & Zhengzhou University People's Hospital, 450003 Zhengzhou, China.
²¹ Center for MRI Research, Academy for Advanced Interdisciplinary Studies, Peking University, 100871 Beijing, China.
²² Department of Radiology, the Center for Medical Imaging, West China Hospital of Sichuan University, 610041 Chengdu, China.
²³ Department of Radiology, The Second Affiliated Hospital and Yuying Children's Hospital of Wenzhou Medical University, 325027 Wenzhou, China.
²⁴ Department of Radiology, Hainan General Hospital (Hainan Affiliated Hospital of Hainan Medical University), 570311 Haikou, China.
²⁵ Department of Radiology, The First Affiliated Hospital of Wenzhou Medical University, 325000 Wenzhou, China.
²⁶ Department of Magnetic Resonance, Lanzhou University Second Hospital, 730030 Lanzhou, China; Gansu Province Clinical Research Center for Functional and Molecular Imaging, 730030 Lanzhou, China.
²⁷ Department of Radiology, Tianjin First Center Hospital, 300192 Tianjin, China.
²⁸ Department of Radiology, The First Affiliated Hospital of Dalian Medical University, 116011 Dalian, China.
²⁹ Department of Radiology, Beijing Tongren Hospital, Capital Medical University, 100730 Beijing, China.
³⁰ Ministry of Education Key Laboratory for Earth System Modeling, Department of Earth System Science, Tsinghua University, Beijing, China.
³¹ Department of Radiology, The Affiliated Hospital of Xuzhou Medical University, 221006 Xuzhou, China.
³² Department of Radiology, Xiangya Hospital, Central South University, 410008 Changsha, China; Molecular Imaging Research Center of Central South University, 410008 Changsha, China; National Clinical Research Center for Geriatric Disorders, Xiangya Hospital, Central South University, 410008 Changsha, China. Electronic address: ouwenliao@163.com.
³³ Department of Radiology, Qilu Hospital of Shandong University, 250012 Jinan, China. Electronic address: daweiwangtj@126.com.
³⁴ Department of Radiology and Tianjin Key Laboratory of Functional Imaging, Tianjin Medical University General Hospital, 300052 Tianjin, China; CAS Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, 200031 Shanghai, China. Electronic address: chunshuiyu@tmu.edu.cn.

PMID: 37019025
DOI: 10.1016/j.envint.2023.107905

Abstract

Background: Urbanicity refers to the conditions that are particular to urban areas and is a growing environmental challenge that may affect hippocampus and neurocognition. This study aimed to investigate the effects of the average pre-adulthood urbanicity on hippocampal subfield volumes and neurocognitive abilities as well as the sensitive age windows of the urbanicity effects.

Participants and methods: We included 5,390 CHIMGEN participants (3,538 females; age: 23.69 ± 2.26 years, range: 18-30 years). Pre-adulthood urbanicity of each participant was defined as the average value of annual night-time light (NL) or built-up% from age 0-18, which were extracted from remote-sensing satellite data based on annual residential coordinates of the participants. The hippocampal subfield volumes were calculated based on structural MRI and eight neurocognitive measures were assessed. The linear regression was applied to investigate the associations of pre-adulthood NL with hippocampal subfield volumes and neurocognitive abilities, mediation models were used to find the underlying pathways among urbanicity, hippocampus and neurocognition, and distributed lag models were used to identify sensitive age windows of urbanicity effect.

Results: Higher pre-adulthood NL was associated with greater volumes in the left (β = 0.100, 95%CI: [0.075, 0.125]) and right (0.078, [0.052, 0.103]) fimbria and left subiculum body (0.045, [0.020, 0.070]) and better neurocognitive abilities in information processing speed (-0.212, [-0.240, -0.183]), working memory (0.085, [0.057, 0.114]), episodic memory (0.107, [0.080, 0.135]), and immediate (0.094, [0.065, 0.123]) and delayed (0.087, [0.058, 0.116]) visuospatial recall, and hippocampal subfield volumes and visuospatial memory showed bilateral mediations for the urbanicity effects. Urbanicity effects were greatest on the fimbria in preschool and adolescence, on visuospatial memory and information processing from childhood to adolescence and on working memory after 14 years.

Conclusion: These findings improve our understanding of the impact of urbanicity on hippocampus and neurocognitive abilities and will benefit for designing more targeted intervention for neurocognitive improvement.

Keywords: Hippocampal subfields; Neurocognition; Neuroimaging; Remote sensing; Urban.

Publication types

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

MeSH terms

Adolescent
Adult
Child
Child, Preschool
Female
Hippocampus*
Humans
Infant
Infant, Newborn
Magnetic Resonance Imaging
Memory, Episodic*
Memory, Short-Term
Neuropsychological Tests
Young Adult