Illness duration–related developmental trajectory of progressive cerebral gray matter changes in schizophrenia_Journal of Biomedical Engineering

Authors：

CHANG Xin ^1,2 , YANG Zhihuan ^1,2 , TANG Yingjie ^1,2 , SUN Xiaoying ^1,2 , LUO Cheng ^1,2,3 ,  YAO Dezhong ^1,2,3

1. The Clinical Hospital of Chengdu Brain Science Institute, MOE Key Lab for Neuroinformation, School of Life Science and Technology, University of Electronic Science and Technology of China, Chengdu 611731, P. R. China;
2. Research Unit of NeuroInformation, Chinese Academy of Medical Sciences, 2019RU035, Chengdu 611731, P. R. China;
3. High-Field Magnetic Resonance Brain Imaging Key Laboratory of Sichuan Province, University of Electronic Science and Technology of China, Chengdu 611731, P. R. China;

Corresponding author：

YAO Dezhong, Email: dyao@uestc.edu.cn

Keywords：

Schizophrenia; Gray matter; Structural covariance network; Developmental trajectory

DOI：

10.7507/1001-5515.202401053

Video：

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In different stages of schizophrenia (SZ), alterations in gray matter volume (GMV) of patients are normally regulated by various pathological mechanisms. Instead of analyzing stage‐specific changes, this study employed a multivariate structural covariance model and sliding‐window approach to investigate the illness duration‐related developmental trajectory of GMV in SZ. The trajectory is defined as a sequence of brain regions activated by illness duration, represented as a sparsely directed matrix. By applying this approach to structural magnetic resonance imaging data from 145 patients with schizophrenia, we observed a continuous developmental trajectory of GMV from cortical to subcortical regions, with an average change occurring every 0.208 years, covering a time window of 20.176 years. The starting points were widely distributed across all networks, except for the ventral attention network. These findings provide insights into the neuropathological mechanism of SZ with a neuroprogressive model and facilitate the development of process for aided diagnosis and intervention with the starting points.

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2.	Murray R M, Bhavsar V, Tripoli G, et al. 30 years on: How the neurodevelopmental hypothesis of schizophrenia morphed into the developmental risk factor model of psychosis. Schizophr Bull, 2017, 43(6): 1190-1196.
3.	Vita A, De Peri L, Deste G, et al. Progressive loss of cortical gray matter in schizophrenia: a meta-analysis and meta-regression of longitudinal MRI studies. Transl Psychiatry, 2012, 2(11): e190.
4.	Rapoport J L, Giedd J N, Gogtay N. Neurodevelopmental model of schizophrenia: update 2012. Mol Psychiatry, 2012, 17(12): 1228-1238.
5.	Shen C L, Tsai S J, Lin C P, et al. Progressive brain abnormalities in schizophrenia across different illness periods: a structural and functional MRI study. Schizophrenia (Heidelb), 2023, 9(1): 2.
6.	Jiang Y C, Luo C, Li X, et al. Progressive reduction in gray matter in patients with schizophrenia assessed with MR imaging by using causal network analysis. Radiology, 2018, 287(2): 633-642,729.
7.	Howes O D, Cummings C, Chapman G E, et al. Neuroimaging in schizophrenia: an overview of findings and their implications for synaptic changes. Neuropsychopharmacology, 2023, 48(1): 151-167.
8.	Prasad K, Rubin J, Mitra A, et al. Structural covariance networks in schizophrenia: A systematic review Part I. Schizophr Res, 2022, 240: 1-21.
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10.	Palaniyappan L, Park B, Balain V, et al. Abnormalities in structural covariance of cortical gyrification in schizophrenia. Brain Struct Funct, 2015, 220(4): 2059-2071.
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12.	Prasad K M R, Patel A R, Muddasani S, et al. The entorhinal cortex in first-episode psychotic disorders: A structural magnetic resonance imaging study. Am J Psychiatry, 2004, 161(9): 1612-1619.
13.	Dazzan P, Arango C, Fleischacker W, et al. Magnetic resonance imaging and the prediction of outcome in first-episode schizophrenia: A review of current evidence and directions for future research. Schizophr Bull, 2015, 41(3): 574-583.
14.	Evans A C. Networks of anatomical covariance. NeuroImage, 2013, 80: 489-504.
15.	Chen X, Jiang Y C, Chen L, et al. Altered hippocampo-cerebello-cortical circuit in schizophrenia by a spatiotemporal consistency and causal connectivity analysis. Front Neurosci, 2017, 11: 25.
16.	Fan L, Li H, Zhuo J, et al. The human brainnetome atlas: A new brain atlas based on connectional architecture. Cereb Cortex, 2016, 26(8): 3508-3526.
17.	Shiskin J, Moore G H. Composite indexes of leading, coinciding, and lagging indicators, 1948-67// Supplement to NBER Report One. Cambridge: NBER, 1968: 1-8.
18.	Di X, Zhang Z G, Biswal B B. Understanding psychophysiological interaction and its relations to beta series correlation. Brain Imaging Behav, 2021, 15(2): 958-973.
19.	Yeo B T T, Krienen F M, Sepulcre J, et al. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol, 2011, 106(3): 1125-1165.
20.	Zhang Z Q, Liao W, Xu Q, et al. Hippocampus-associated causal network of structural covariance measuring structural damage progression in temporal lobe epilepsy. Hum Brain Mapp, 2017, 38(2): 753-766.
21.	Malchow B, Keeser D, Keller K, et al. Effects of endurance training on brain structures in chronic schizophrenia patients and healthy controls. Schizophr Res, 2016, 173(3): 182-191.
22.	Thompson P M, Bartzokis G, Hayashi K M, et al. Time-lapse mapping of cortical changes in schizophrenia with different treatments. Cereb Cortex, 2009, 19(5): 1107-1123.
23.	Emsley R, Asmal L, du Plessis S, et al. Brain volume changes over the first year of treatment in schizophrenia: relationships to antipsychotic treatment. Psycholog Med, 2017, 47(12): 2187-2196.
24.	Dietsche B, Kircher T, Falkenberg I. Structural brain changes in schizophrenia at different stages of the illness: A selective review of longitudinal magnetic resonance imaging studies. Aust N Z J Psychiatry, 2017, 51(5): 500-508.
25.	Liloia D, Brasso C, Cauda F, et al. Updating and characterizing neuroanatomical markers in high-risk subjects, recently diagnosed and chronic patients with schizophrenia: A revised coordinate-based meta-analysis. Neurosci Biobehav Rev, 2021, 123: 83-103.
26.	Luo N, Tian L, Calhoun V D, et al. Brain function, structure and genomic data are linked but show different sensitivity to duration of illness and disease stage in schizophrenia. Neuroimage Clin, 2019, 23: 101887.
27.	Feng A C, Luo N, Zhao W T, et al. Multimodal brain deficits shared in early-onset and adult-onset schizophrenia predict positive symptoms regardless of illness stage. Hum Brain Mapp, 2022, 43(11): 3486-3497.
28.	Torres U S, Duran F L S, Schaufelberger M S, et al. Patterns of regional gray matter loss at different stages of schizophrenia: A multisite, cross-sectional VBM study in first-episode and chronic illness. Neuroimage Clin, 2016, 12: 1-15.
29.	Zhao C, Zhu J J, Liu X Y, et al. Structural and functional brain abnormalities in schizophrenia: A cross-sectional study at different stages of the disease. Prog Neuropsychopharmacol Biol Psychiatry, 2018, 83: 27-32.

1. Kendler K S. The development of Kraepelin's mature diagnostic concept of catatonic dementia praecox: A close reading of relevant texts. Schizophr Bull, 2020, 46(3): 471-483.
2. Murray R M, Bhavsar V, Tripoli G, et al. 30 years on: How the neurodevelopmental hypothesis of schizophrenia morphed into the developmental risk factor model of psychosis. Schizophr Bull, 2017, 43(6): 1190-1196.
3. Vita A, De Peri L, Deste G, et al. Progressive loss of cortical gray matter in schizophrenia: a meta-analysis and meta-regression of longitudinal MRI studies. Transl Psychiatry, 2012, 2(11): e190.
4. Rapoport J L, Giedd J N, Gogtay N. Neurodevelopmental model of schizophrenia: update 2012. Mol Psychiatry, 2012, 17(12): 1228-1238.
5. Shen C L, Tsai S J, Lin C P, et al. Progressive brain abnormalities in schizophrenia across different illness periods: a structural and functional MRI study. Schizophrenia (Heidelb), 2023, 9(1): 2.
6. Jiang Y C, Luo C, Li X, et al. Progressive reduction in gray matter in patients with schizophrenia assessed with MR imaging by using causal network analysis. Radiology, 2018, 287(2): 633-642,729.
7. Howes O D, Cummings C, Chapman G E, et al. Neuroimaging in schizophrenia: an overview of findings and their implications for synaptic changes. Neuropsychopharmacology, 2023, 48(1): 151-167.
8. Prasad K, Rubin J, Mitra A, et al. Structural covariance networks in schizophrenia: A systematic review Part I. Schizophr Res, 2022, 240: 1-21.
9. Alexander-Bloch A, Giedd J N, Bullmore E T. Imaging structural co-variance between human brain regions. Nat Rev Neurosci, 2013, 14(5): 322-336.
10. Palaniyappan L, Park B, Balain V, et al. Abnormalities in structural covariance of cortical gyrification in schizophrenia. Brain Struct Funct, 2015, 220(4): 2059-2071.
11. Goodkind M, Eickhoff S B, Oathes D J, et al. Identification of a common neurobiological substrate for mental illness. JAMA Psychiatry, 2015, 72(4): 305-315.
12. Prasad K M R, Patel A R, Muddasani S, et al. The entorhinal cortex in first-episode psychotic disorders: A structural magnetic resonance imaging study. Am J Psychiatry, 2004, 161(9): 1612-1619.
13. Dazzan P, Arango C, Fleischacker W, et al. Magnetic resonance imaging and the prediction of outcome in first-episode schizophrenia: A review of current evidence and directions for future research. Schizophr Bull, 2015, 41(3): 574-583.
14. Evans A C. Networks of anatomical covariance. NeuroImage, 2013, 80: 489-504.
15. Chen X, Jiang Y C, Chen L, et al. Altered hippocampo-cerebello-cortical circuit in schizophrenia by a spatiotemporal consistency and causal connectivity analysis. Front Neurosci, 2017, 11: 25.
16. Fan L, Li H, Zhuo J, et al. The human brainnetome atlas: A new brain atlas based on connectional architecture. Cereb Cortex, 2016, 26(8): 3508-3526.
17. Shiskin J, Moore G H. Composite indexes of leading, coinciding, and lagging indicators, 1948-67// Supplement to NBER Report One. Cambridge: NBER, 1968: 1-8.
18. Di X, Zhang Z G, Biswal B B. Understanding psychophysiological interaction and its relations to beta series correlation. Brain Imaging Behav, 2021, 15(2): 958-973.
19. Yeo B T T, Krienen F M, Sepulcre J, et al. The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol, 2011, 106(3): 1125-1165.
20. Zhang Z Q, Liao W, Xu Q, et al. Hippocampus-associated causal network of structural covariance measuring structural damage progression in temporal lobe epilepsy. Hum Brain Mapp, 2017, 38(2): 753-766.
21. Malchow B, Keeser D, Keller K, et al. Effects of endurance training on brain structures in chronic schizophrenia patients and healthy controls. Schizophr Res, 2016, 173(3): 182-191.
22. Thompson P M, Bartzokis G, Hayashi K M, et al. Time-lapse mapping of cortical changes in schizophrenia with different treatments. Cereb Cortex, 2009, 19(5): 1107-1123.
23. Emsley R, Asmal L, du Plessis S, et al. Brain volume changes over the first year of treatment in schizophrenia: relationships to antipsychotic treatment. Psycholog Med, 2017, 47(12): 2187-2196.
24. Dietsche B, Kircher T, Falkenberg I. Structural brain changes in schizophrenia at different stages of the illness: A selective review of longitudinal magnetic resonance imaging studies. Aust N Z J Psychiatry, 2017, 51(5): 500-508.
25. Liloia D, Brasso C, Cauda F, et al. Updating and characterizing neuroanatomical markers in high-risk subjects, recently diagnosed and chronic patients with schizophrenia: A revised coordinate-based meta-analysis. Neurosci Biobehav Rev, 2021, 123: 83-103.
26. Luo N, Tian L, Calhoun V D, et al. Brain function, structure and genomic data are linked but show different sensitivity to duration of illness and disease stage in schizophrenia. Neuroimage Clin, 2019, 23: 101887.
27. Feng A C, Luo N, Zhao W T, et al. Multimodal brain deficits shared in early-onset and adult-onset schizophrenia predict positive symptoms regardless of illness stage. Hum Brain Mapp, 2022, 43(11): 3486-3497.
28. Torres U S, Duran F L S, Schaufelberger M S, et al. Patterns of regional gray matter loss at different stages of schizophrenia: A multisite, cross-sectional VBM study in first-episode and chronic illness. Neuroimage Clin, 2016, 12: 1-15.
29. Zhao C, Zhu J J, Liu X Y, et al. Structural and functional brain abnormalities in schizophrenia: A cross-sectional study at different stages of the disease. Prog Neuropsychopharmacol Biol Psychiatry, 2018, 83: 27-32.

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