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Human cortical folding across regions within individual brains follows universal scaling law.

ABSTRACT: Different cortical regions vary systematically in their morphology. Here we investigate if the scaling law of cortical morphology, which was previously demonstrated across both human subjects and mammalian species, still holds within a single cortex across different brain regions. By topologically correcting for regional curvature, we could analyse how different morphological parameters co-vary within single cortices. We show in over 1500 healthy individuals that, despite their morphological diversity, regions of the same cortex obey the same universal scaling law, and age morphologically at similar rates. In Alzheimer's disease, we observe a premature ageing in the morphological parameters that was nevertheless consistent with the scaling law. The premature ageing effect was most dramatic in the temporal lobe. Thus, while morphology can vary substantially across cortical regions, subjects, and species, it always does so in accordance with a common scaling law, suggesting that the underlying processes driving cortical gyrification are universal.

SUBMITTER: Wang Y

PROVIDER: S-EPMC6527703 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Human cortical folding across regions within individual brains follows universal scaling law.

Wang Yujiang Y Necus Joe J Rodriguez Luis Peraza LP Taylor Peter Neal PN Mota Bruno B

Communications biology 20190520

Different cortical regions vary systematically in their morphology. Here we investigate if the scaling law of cortical morphology, which was previously demonstrated across both human subjects and mammalian species, still holds within a single cortex across different brain regions. By topologically correcting for regional curvature, we could analyse how different morphological parameters co-vary within single cortices. We show in over 1500 healthy individuals that, despite their morphological div ...[more]

PMID: 31123715

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Project description:Various types of neural-based signals, such as EEG, local field potentials and intracellular synaptic potentials, integrate multiple sources of activity distributed across large assemblies. They have in common a power-law frequency-scaling structure at high frequencies, but it is still unclear whether this scaling property is dominated by intrinsic neuronal properties or by network activity. The latter case is particularly interesting because if frequency-scaling reflects the network state it could be used to characterize the functional impact of the connectivity. In intracellularly recorded neurons of cat primary visual cortex in vivo, the power spectral density of V(m) activity displays a power-law structure at high frequencies with a fractional scaling exponent. We show that this exponent is not constant, but depends on the visual statistics used to drive the network. To investigate the determinants of this frequency-scaling, we considered a generic recurrent model of cortex receiving a retinotopically organized external input. Similarly to the in vivo case, our in computo simulations show that the scaling exponent reflects the correlation level imposed in the input. This systematic dependence was also replicated at the single cell level, by controlling independently, in a parametric way, the strength and the temporal decay of the pairwise correlation between presynaptic inputs. This last model was implemented in vitro by imposing the correlation control in artificial presynaptic spike trains through dynamic-clamp techniques. These in vitro manipulations induced a modulation of the scaling exponent, similar to that observed in vivo and predicted in computo. We conclude that the frequency-scaling exponent of the V(m) reflects stimulus-driven correlations in the cortical network activity. Therefore, we propose that the scaling exponent could be used to read-out the "effective" connectivity responsible for the dynamical signature of the population signals measured at different integration levels, from Vm to LFP, EEG and fMRI.

Project description:A universal allometric scaling law has been proposed to describe cortical folding of the mammalian brain as a function of the product of cortical surface area and the square root of cortical thickness across different mammalian species, including humans. Since these cortical properties are vulnerable to developmental disturbances caused by preterm birth in humans and since these alterations are related to cognitive impairments, we tested (i) whether cortical folding in preterm-born adults follows this cortical scaling law and (ii) the functional relevance of potential scaling aberrances. We analysed the cortical scaling relationship in a large and prospectively collected cohort of 91 very premature-born adults (<32 weeks of gestation and/or birthweight <1500 g, very preterm and/or very low birth weight) and 105 full-term controls at 26 years of age based on the total surface area, exposed surface area and average cortical thickness measured with structural magnetic resonance imaging and surface-based morphometry. We found that the slope of the log-transformed cortical scaling relationship was significantly altered in adults (very preterm and/or very low birth weight: 1.24, full-term: 1.14, P = 0.018). More specifically, the slope was significantly altered in male adults (very preterm and/or very low birth weight: 1.24, full-term: 1.00, P = 0.031), while there was no significant difference in the slope of female adults (very preterm and/or very low birth weight: 1.27, full-term: 1.12, P = 0.225). Furthermore, offset was significantly lower compared with full-term controls in both male (very preterm and/or very low birth weight: -0.546, full-term: -0.538, P = 0.001) and female adults (very preterm and/or very low birth weight: -0.545, full-term: -0.538, P = 0.023), indicating a systematic shift of the regression line after preterm birth. Gestational age had a significant effect on the slope in very preterm and/or very low birth weight adults and more specifically in male very preterm and/or very low birth weight adults, indicating that the difference in slope is specifically related to preterm birth. The shape or tension term of the scaling law had no significant effect on cognitive performance, while the size of the cortex did. Results demonstrate altered scaling of cortical surface and cortical thickness in very premature-born adults. Data suggest altered mechanical forces acting on the cortex after preterm birth.

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Human cortical folding across regions within individual brains follows universal scaling law.

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Human cortical folding across regions within individual brains follows universal scaling law.

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