Mapping longitudinal development of local cortical gyrification in infants from birth to 2 years of age

Abstract

Human cortical folding is believed to correlate with cognitive functions. This likely correlation may have something to do with why abnormalities of cortical folding have been found in many neurodevelopmental disorders. However, little is known about how cortical gyrification, the cortical folding process, develops in the first 2 years of life, a period of dynamic and regionally heterogeneous cortex growth. In this article, we show how we developed a novel infant-specific method for mapping longitudinal development of local cortical gyrification in infants. By using this method, via 219 longitudinal 3T magnetic resonance imaging scans from 73 healthy infants, we systemically and quantitatively characterized for the first time the longitudinal cortical global gyrification index (GI) and local GI (LGI) development in the first 2 years of life. We found that the cortical GI had age-related and marked development, with 16.1% increase in the first year and 6.6% increase in the second year. We also found marked and regionally heterogeneous cortical LGI development in the first 2 years of life, with the high-growth regions located in the association cortex, whereas the low-growth regions located in sensorimotor, auditory, and visual cortices. Meanwhile, we also showed that LGI growth in most cortical regions was positively correlated with the brain volume growth, which is particularly significant in the prefrontal cortex in the first year. In addition, we observed gender differences in both cortical GIs and LGIs in the first 2 years, with the males having larger GIs than females at 2 years of age. This study provides valuable information on normal cortical folding development in infancy and early childhood.

Keywords: cortical folding; cortical surface; infant; local gyrification; longitudinal development.

Figure 1.

A 2D illustration of establishing correspondences between the outer cortical surface and the cerebral hull surface based on Laplace's equation, with the orange curves indicating the streamlines.

Figure 2.

Illustrations of computing local GIs on a representative subject at 0, 1, and 2 years of age. a, N-ring neighborhood (red) on the resampled outer cortical surfaces of the yellow vertex. b, Corresponding regions (red) on the cerebral hull surfaces, established by Laplace's equation. c, Spatial distributions of the local GI on the lateral views of both cortical surfaces and their inflated surfaces at 0, 1, and 2 years of age. d, Spatial distributions of the local GI on the medial views of both cortical surfaces and their inflated surfaces at 0, 1, and 2 years of age. The insula cortex has the highest LGI because of its extremely folded and deeply buried structure.

Figure 3.

Average local GI on the left hemispheres of all 73 subjects by the proposed method with different N-ring neighborhoods (from N = 50 to N = 70) and by the conventional method with the radius 20 mm at 0, 1, and 2 years of age. The highest LGI is consistently found in the insula cortex due to its extremely folded and deeply buried structure.

Figure 4.

The distribution of longitudinal cortical GIs of 73 subjects at 0, 1, and 2 years of age. A, Left hemisphere; B, right hemisphere.

Figure 5.

Longitudinal cortical LGI development in the first 2 years of life for 73 subjects by the proposed method with N = 60. The left column shows the average growth percentage of the cortical LGI. The right column shows the significant high-growth and low-growth regions of LGIs by TFCE method (p < 0.01). Blue clusters are the low-growth regions of LGIs. Red clusters are the high-growth regions of LGIs. a–c, Results for 0–1 year, 1–2 years, and 0–2 years.

Figure 6.

Significant clusters of high-growth (red) and low-growth (blue) regions of LGIs in the first 2 years of life found from 73 subjects by TFCE method (p < 0.01) with N = 50 and N = 70. a–c, Results for 0–1 year (a), 1–2 years (b), and 0–2 years (c).

Figure 7.

Longitudinal cortical LGI development in the first 2 years of life for 73 subjects, computed by the conventional method with the radius 20 mm. The left column shows the average growth percentage of the cortical LGIs. The right column shows the significant high-growth and low-growth regions of LGIs by TFCE method (p < 0.01). Blue and red clusters are the low-growth and high-growth regions of LGIs, respectively. a–c, Results for 0–1 year (a), 1–2 years (b), and 0–2 years (c).

Figure 8.

Significant clusters of gender differences on LGIs (p < 0.05, multiple-comparisons corrected), at 0, 1, and 2 years of age, by including TBV as a confounding factor. Red clusters indicate that males have larger LGIs than females. No significant cluster of gender difference on LGIs is found in other cortical regions.

Figure 9.

Significant clusters (nonwhite colors) of positive correlations between LGI growth and TBV growth (p < 0.05, multiple-comparisons corrected) in the first 2 years of life. Significant clusters are color-coded by t values. a–c, Results for 0–1 year (a), 1–2 years (b), and 0–2 years (c).