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@INPROCEEDINGS{Lotter:1014626,
author = {Lotter, Leon and Saberi, Amin and Jansen, Justine Y. and
Misic, Bratislav and Barker, Gareth J. and Bokde, Arun L. W.
and Desrivíeres, Sylvane and Flor, Herta and Grigis,
Antoine and Garavan, Hugh and Gowland, Penny and Heinz,
Andreas and Brühl, Rüdiger and Martinot, Jean-Luc and
Paillére, Marie-Paure and Artiges, Eric and Orfanos,
Dimitri Papadopoulos and Paus, Tomáš and Poustka, Luise
and Hohmann, Sarah and Fröhner, Juliane H. and Smolka,
Michael N. and Vaidya, Nilakshi and Walter, Henrik and
Whelan, Robert and Schumann, Gunter and Nees, Frauke and
Banaschewski, Tobias and Eickhoff, Simon and Dukart,
Jürgen},
title = {{H}uman cortex development is shaped by molecular and
cellular brain systems},
reportid = {FZJ-2023-03331},
year = {2023},
abstract = {Introduction:Human cerebral cortex morphology is subject to
complex developmental changes, with developmental
trajectories varying across brain regions (Bethlehem et al.,
2022; Rutherford et al., 2022). Several biological factors
influencing cortical thickness (CT) development have been
discussed, but naturally, human data are scarce. As
especially neurodevelopmental disorders are characterized by
atypical cortex development (Bethlehem et al., 2020;
Rutherford et al., 2022), knowledge about drivers of typical
development may shed light on the pathophysiology of
deviating neurodevelopment. In this study, we demonstrate
that population-average and single-subject CT trajectories
colocalize with, and are explained by, spatial distributions
of brain metabolism and immunity features, neurotransmitter
systems, cortical myelin, as well as neuronal and glial cell
populations. We provide novel information on human cortex
development within a framework that facilitates easy
transfer to new cohorts, paving the way for individualized
and biologically interpretable brain-based
biomarkers.Methods:We included 49 atlases of molecular and
cellular brain systems derived from healthy adult data
(Hansen et al., 2022; Dukart et al., 2021; Hawrylycz et al.,
2012). Atlases were parcellated in 148 bilateral cortex
regions and reduced to 18 factors (factor analysis retaining
dimensions explaining ≥ $1\%$ of variance). First, we
extracted 50th percentile "representative" CT data from a
normative CT model estimated on 58,836 subjects from 82
sites (5-90 years) (Rutherford et al., 2022). To test for
relationships between CT change patterns and multilevel
brain systems, we (i) estimated the spatial colocalization
(Spearman's ρ) between each factor and CT at each timepoint
(Vidal-Pineiro et al., 2020) and (ii) fitted multivariate
linear models "predicting" CT change from the multilevel
factors using a sliding window approach (5-year-steps). The
results were validated in longitudinal CT data from the ABCD
(n = 6,315; 20 sites; ~10-12 years; Casey et al., 2018) and
IMAGEN (n = 985-1177; 8 sites; ~14-22 years; Schumann et
al., 2010) cohort studies. Analyses were performed with
JuSpyce (Lotter and Dukart, 2022), a toolbox for large-scale
spatial association analyses, using strict spatial
autocorrelation-preserving permutation testing and false
discovery rate correction.Results:Spatial Spearman
colocalization analyses between cross-selctional CT and
biological brain systems revealed diverse colocalization
trajectories with a general pattern of strongest changes in
early and late phases of life. The combined biological
systems at molecular and cellular levels explained up to
$54\%$ of the spatial variance in modeled CT changes across
the lifespan with peaks at about 20-35 (molecular) and 15-20
(cellular) years of age, respectively. Subsequent analyses
accounting for shared variance showed that the 9 strongest
associated brain systems jointly explained up to $58\%$ of
CT change. Of particular relevance for early cortex
development were D1/2 dopaminergic receptors, microglia, and
somatostatin-expressing interneurons, while dopaminergic and
cholinergic neurotransmission was associated with midlife CT
maturation patterns. Normative model-based results
replicated in single-subject data, albeit showing
considerably higher variance (cohort-average R2 = $25-56\%;$
individual R2 $9-18\%,$ range $0-59\%).Conclusions:Factors$
shaping human brain morphology over the lifespan are poorly
understood. Here we demonstrate that the complex patterns in
which the human cerebral cortex develops and matures
colocalize with specific biological systems on molecular and
cellular levels. Our findings support roles of the
dopaminergic system, microglia and somatostatin-expressing
interneurons in early CT development, whereas cholinergic
and dopaminergic neurotransmission are associated with CT
changes across adulthood. Our results not only have
implications for the study of typical neurodevelopment, but
also hold promise for the value of neurodevelopmental
cross-modal association analyses for future clinical
research applications.},
month = {Jul},
date = {2023-07-21},
organization = {Organization for Human Brain Mapping
(OHBM), Montreal (Canada), 21 Jul 2023
- 26 Jul 2023},
subtyp = {After Call},
cin = {INM-7},
cid = {I:(DE-Juel1)INM-7-20090406},
pnm = {5252 - Brain Dysfunction and Plasticity (POF4-525)},
pid = {G:(DE-HGF)POF4-5252},
typ = {PUB:(DE-HGF)24},
doi = {10.34734/FZJ-2023-03331},
url = {https://juser.fz-juelich.de/record/1014626},
}