Local Tissue Growth Patterns Underlying Normal Fetal Human Brain Gyrification QuantifiedIn Utero

Abstract

Existing knowledge of growth patterns in the living fetal human brain is based upon in utero imaging studies by magnetic resonance imaging (MRI) and ultrasound, which describe overall growth and provide mainly qualitative findings. However, formation of the complex folded cortical structure of the adult brain requires, in part, differential rates of regional tissue growth. To better understand these local tissue growth patterns, we applied recent advances in fetal MRI motion correction and computational image analysis techniques to 40 normal fetal human brains covering a period of primary sulcal formation (20 -28 gestational weeks). Growth patterns were mapped by quantifying tissue locations that were expanding more or less quickly than the overall cerebral growth rate, which reveal increasing structural complexity. We detected increased local relative growth rates in the formation of the precentral and postcentral gyri, right superior temporal gyrus, and opercula, which differentiated between the constant growth rate in underlying cerebral mantle and the accelerating rate in the cortical plate undergoing folding. Analysis focused on the cortical plate revealed greater volume increases in parietal and occipital regions compared to the frontal lobe. Cortical plate growth patterns constrained to narrower age ranges showed that gyrification, reflected by greater growth rates, was more pronounced after 24 gestational weeks. Local hemispheric volume asymmetry was located in the posterior peri-Sylvian area associated with structural lateralization in the mature brain. These maps of fetal brain growth patterns construct a spatially specific baseline of developmental biomarkers with which to correlate abnormal development in the human.

Prenatal growth in humans and postnatal brain maturation into late adolescence

“…These findings provide empirical support to neurodevelopmental theories that emphasize the potential for prenatally instilled differences to have temporally delayed postnatal "echoes," of relevance for the emergence of psychopathology (25). From a mechanistic perspective, regional specificity of our findings could potentially reflect regional differences in the timing of prenatal cortical development (23,32) or the fact that frontal and temporal Fig. 2.…”

Morphological brain changes associated with negative symptoms in patients with 22q11.2 Deletion Syndrome

“…The fact that we observed changes in gyrification but not in cortical thickness in our group of patients with 22q11DS may be explained by the varying neurodevelopmental spatiotemporal dynamics, such as differing initiation periods and growth rates, between these two measures (Boardman et al, 2006;Rajagopalan et al, 2011). In particular, postnatal cortical thickness growth rates considerably exceed those of gyrification during the first year of life (Li et al, 2015(Li et al, , 2014, while the gyrification process is typically completed in-utero and shortly after birth (Armstrong et al, 1995;Garel et al, 2003).…”

Aberrant cortical gyrification in schizophrenia: a surface-based morphometry study

“…Insofar as the degree of folding across the different regions in the cortex varies with the rate of maturation of those regions, 7,20,39,40 the gyrification metrics provide crucial information about neurodevelopmental aberrations.…”

“…In particular, the insula is a region of specific interest while investigating cortical folding in patients with schizophrenia, not only owing to its relevance to the illness, 16 but also because it has been shown to be one of the earliest brain regions where gyrification occurs, [17][18][19] with an accelerated growth rate compared to the surrounding cortical plate during fetal development. 20 The search for the brain region with the most prominent gyrification defect in patients with schizophrenia is hampered by several methodological issues. 21 Zilles and colleagues' gyrification index (the ratio between the inner folded contour and the outer curvature), 22 though commonly used, 10 does not capture the regional changes associated with subtle deviations in cortical connectivity.…”