Cortico-striatal-thalamic loop as a neural correlate of neuroticism in the mind-body interface

Seishu Nakagawa; Hikaru Takeuchi; Yasuyuki Taki; Rui Nouchi; Yuka Kotozaki; Takamitsu Shinada; Tsukasa Maruyama; Atsushi Sekiguchid; Kunio Iizuka; Ryoichi Yokoyama; Yuki Yamamoto; Sugiko Hanawa; Tsuyoshi Araki; Carlos Makoto Miyauchi; Daniele Magistro; Kohei Sakaki; Hyeonjeong Jeong; Ryuta Kawashima

doi:10.1016/j.jpsychores.2021.110590

Cortico-striatal-thalamic loop as a neural correlate of neuroticism in the mind-body interface

J Psychosom Res. 2021 Oct:149:110590. doi: 10.1016/j.jpsychores.2021.110590. Epub 2021 Jul 31.

Authors

Seishu Nakagawa¹, Hikaru Takeuchi², Yasuyuki Taki³, Rui Nouchi⁴, Yuka Kotozaki⁵, Takamitsu Shinada⁶, Tsukasa Maruyama⁶, Atsushi Sekiguchid⁷, Kunio Iizuka⁸, Ryoichi Yokoyama⁹, Yuki Yamamoto⁶, Sugiko Hanawa⁶, Tsuyoshi Araki¹⁰, Carlos Makoto Miyauchi¹¹, Daniele Magistro¹², Kohei Sakaki¹¹, Hyeonjeong Jeong¹³, Ryuta Kawashima¹⁴

Affiliations

¹ Division of Psychiatry, Tohoku Medical and Pharmaceutical University, Sendai, Japan; Department of Human Brain Science, Institute of Development, Ageing and Cancer, Tohoku University, Sendai, Japan. Electronic address: seishu.nakagawa.e8@tohoku.ac.jp.
² Division of Developmental Cognitive Neuroscience, Institute of Development, Ageing and Cancer, Tohoku University, Sendai, Japan.
³ Division of Developmental Cognitive Neuroscience, Institute of Development, Ageing and Cancer, Tohoku University, Sendai, Japan; Division of Medical Neuroimaging Analysis, Department of Community Medical Supports, Tohoku Medical Megabank Organization, Tohoku University, Sendai, Japan; Department of Nuclear Medicine and Radiology, Institute of Development, Ageing and Cancer, Tohoku University, Sendai, Japan.
⁴ Creative Interdisciplinary Research Division, Frontier Research Institute for Interdisciplinary Science (FRIS), Tohoku University, Sendai, Japan; Smart Ageing International Research Center, Institute of Development, Ageing and Cancer, Tohoku University, Sendai, Japan.
⁵ Smart Ageing International Research Center, Institute of Development, Ageing and Cancer, Tohoku University, Sendai, Japan.
⁶ Department of Human Brain Science, Institute of Development, Ageing and Cancer, Tohoku University, Sendai, Japan.
⁷ Division of Medical Neuroimaging Analysis, Department of Community Medical Supports, Tohoku Medical Megabank Organization, Tohoku University, Sendai, Japan; Department of Behavioral Medicine, National Institute of Mental Health, National Center of Neurology and Psychiatry, Kodaira, Tokyo, Japan.
⁸ Department of Psychiatry, Tohoku University Graduate School of Medicine, Sendai, Japan.
⁹ Japanese Red Cross Society, Suwa Hospital, Suwa, Japan.
¹⁰ ADVANTAGE Risk Management Co., Ltd, Tokyo, Japan.
¹¹ Advanced Brain Science, Institute of Development, Ageing and Cancer, Tohoku University, Sendai, Japan.
¹² Department of Sport Science, School of Science and Technology, Nottingham Trent University, Nottingham, United Kingdom.
¹³ Department of Human Brain Science, Institute of Development, Ageing and Cancer, Tohoku University, Sendai, Japan; Graduate School of International Cultural Studies, Tohoku University, Sendai, Japan.
¹⁴ Division of Developmental Cognitive Neuroscience, Institute of Development, Ageing and Cancer, Tohoku University, Sendai, Japan; Smart Ageing International Research Center, Institute of Development, Ageing and Cancer, Tohoku University, Sendai, Japan; Advanced Brain Science, Institute of Development, Ageing and Cancer, Tohoku University, Sendai, Japan.

PMID: 34385032
DOI: 10.1016/j.jpsychores.2021.110590

Abstract

Objective: Although brain structural studies have demonstrated the neural correlates of neuroticism, the outcomes are not easily identified because of the various possible brain regions involved, low statistical power (low number of subjects), and brain structural measures available, such as mean diffusivity (MD), which are more suitable than standard regional measures of grey and white-matter volume (rGMV, rWMV) and fractional anisotropy (FA). We hypothesized that neuroticism neural correlates could be detected by MD and differentially identified using other measures. We aimed to visualize the neural correlates of neuroticism.

Methods: A voxel-by-voxel regression analysis was performed using the MD, rGMV, rWMV, or FA value as the dependent variable and with neuroticism scores based on the NEO-FFI and its confounding factors as independent variables in 1207 (693 men and 514 women; age, 20.7 ± 1.8, 18-27 years), non-clinical students in a cross-sectional study.

Results: MD in the cortico- (orbitofrontal cortex, anterior cingulate cortex, and posterior insula) striatal- (caudate and putamen) thalamic loop regions, including the right posterior limb of the internal capsule, were positively associated with neuroticism using the threshold-free cluster enhancement method with a family-wise error-corrected threshold of P < 0.0125 (0.05/4, Bonferroni correction for four types of MRI data [MD, rGMV, rWMV, and FA]) at the whole-brain level.

Conclusions: An increased MD has generally been associated with reduced neural tissues and possibly area function. Accordingly, this finding helps elucidate the mechanism of somatization in neuroticism because the regions related to neuroticism are considered neural correlates of somatoform disorders.

Keywords: Cortico-striatal-thalamic loop; Mean diffusivity; Neuroticism; Posterior limb of the internal capsule.

Publication types

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

MeSH terms

Anisotropy
Brain*
Cross-Sectional Studies
Diffusion Magnetic Resonance Imaging*
Female
Humans
Male
Neuroticism