Morphology and morphometry of the human embryonic brain: A three-dimensional analysis

Abstract

The three-dimensional dynamics and morphology of the human embryonic brain have not been previously analyzed using modern imaging techniques. The morphogenesis of the cerebral vesicles and ventricles was analyzed using images derived from human embryo specimens from the Kyoto Collection, which were acquired with a magnetic resonance microscope equipped with a 2.35-T superconducting magnet. A total of 101 embryos between Carnegie stages (CS) 13 and 23, without apparent morphological damage or torsion in the brain ventricles and axes, were studied. To estimate the uneven development of the cerebral vesicles, the volumes of the whole embryo and brain, prosencephalon, mesencephalon, and rhombencephalon with their respective ventricles were measured using image analyzing Amira™ software. The brain volume, excluding the ventricles (brain tissue), was 1.15 ± 0.43 mm(3) (mean ± SD) at CS13 and increased exponentially to 189.10 ± 36.91 mm(3) at CS23, a 164.4-fold increase, which is consistent with the observed morphological changes. The mean volume of the prosencephalon was 0.26 ± 0.15 mm(3) at CS13. The volume increased exponentially until CS23, when it reached 110.99 ± 27.58 mm(3). The mean volumes of the mesencephalon and rhombencephalon were 0.20 ± 0.07 mm(3) and 0.69 ± 0.23 mm(3) at CS13, respectively; the volumes reached 21.86 ± 3.30 mm(3) and 56.45 ± 7.64 mm(3) at CS23, respectively. The ratio of the cerebellum to the rhombencephalon was approximately 7.2% at CS20, and increased to 12.8% at CS23. The ratio of the volume of the cerebral vesicles to that of the whole embryo remained nearly constant between CS15 and CS23 (11.6-15.5%). The non-uniform thickness of the brain tissue during development, which may indicate the differentiation of the brain, was visualized with surface color mapping by thickness. At CS23, the basal regions of the prosencephalon and rhombencephalon were thicker than the corresponding dorsal regions. The brain was further studied by the serial digital subtraction of layers of tissue from both the external and internal surfaces to visualize the core region (COR) of the thickening brain tissue. The COR, associated with the development of nuclei, became apparent after CS16; this was particularly visible in the prosencephalon. The anatomical positions of the COR were mostly consistent with the formation of the basal ganglia, thalamus, and pyramidal tract. This was confirmed through comparisons with serial histological sections of the human embryonic brain. The approach used in this study may be suitable as a convenient alternative method for estimating the development and differentiation of the neural ganglia and tracts. These findings contribute to a better understanding of brain and cerebral ventricle development.

Morphometric human embryonic brain features according to developmental stage

“…The human brain develops in a very complicated manner during the embryonic period . For example, three brain vesicles that develop at the cranial end of the neural tube differentiate to form the prosencephalon, mesencephalon, and rhombencephalon at CS13 .…”

Craniofacial skeletal response to encephalization: How do we know what we think we know?

“…Magnetic resonance microscopy of 3D dynamics and morphology of the human embryonic brain have revealed eccentric (without thickening of brain tissue) and concentric (resulting in brain tissue thickening) growth dynamics (Shiraishi et al, 2015). Each part of the brain grows at different rates during the embryonic and fetal periods (Nolte, 2009).…”

“…Each part of the brain grows at different rates during the embryonic and fetal periods (Nolte, 2009). The arrangement of these regions and their disproportionate growth result in the brain taking on an increasingly flexed morphology by week 8 (Carnegie stage 23) (Nolte, 2009; Shiraishi et al, 2015). Surface mapping by tissue thickness enabled simultaneous visualization of surface morphology and internal thickness and demonstrated a correlation between the flexion and extension of the forming brain and tissue thickness (Shiraishi et al, 2015).…”

“…The arrangement of these regions and their disproportionate growth result in the brain taking on an increasingly flexed morphology by week 8 (Carnegie stage 23) (Nolte, 2009; Shiraishi et al, 2015). Surface mapping by tissue thickness enabled simultaneous visualization of surface morphology and internal thickness and demonstrated a correlation between the flexion and extension of the forming brain and tissue thickness (Shiraishi et al, 2015). Tissue became thicker in the regions of brain flexion, while it remained thin in the regions of extension, suggesting that intrinsic growth dynamics contribute to the formation of various brain flexures (Shiraishi et al, 2015).…”

“…(a) Early development of neural tube from neuroectoderm (adapted from Richtsmeier & Flaherty, 2013). (b) Morphogenesis of brain from neural tube and formation of major brain regions (adapted from Shiraishi et al, 2015). CS = Carnegie stage…”