Quantification of the initial phases of rapid brain enlargement in the chick embryo

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Abstract
Rapid brain enlargement requires a hydraulic mechanism in the chick embryo. Such a mechanism involves a closed, fluid-filled system that generates positive pressure. For the chick embryo this study (1) determined when rapid brain enlargement begins, (2) assessed the relative contributions of cavity expansion and tissue growth to overall brain enlargement, and (3) evaluated mathematical models of overall brain enlargement and expansion and growth of the component parts. Three to five embryos were collected at each Hamburger and Hamilton stage (11, 12, 14, 16, and 18) and processed for paraffin serial sectioning. Brain growth was determined over a 24-hr period (stages 11–18) by calculating volumes from area measurements of sections of brains from individual embryos by using a computerized image-analysis system. Statistical analysis indicated that a linear model adequately described cavity expansion, and a linear model was rejected for the description of tissue growth and total brain enlargement. At the onset of brain enlargement, the cavity expands faster than the tissue grows; but after 12 hr the reverse is true. Initially (i.e., at stage 11), the cavity accounts for 60% of the total brain volume and tissue for 40%. At stages 12–16, cavity and tissue contribute 50% each. Finally at stage 18, cavity accounts for 55% and tissue for 45%. In order to better distinguish changes in cavity expansion and tissue growth over the 24-hr period studied, this period was divided into four intervals (I-IV). The rates of both cavity expansion and tissue growth increase between intervals I and II, decrease between intervals II and III, and increase between intervals III and IV. Overall, the brain enlarges 8.5 times, the cavity expands 9.8 times, and the tissue grows 7.6 times. Change in cavity expansion for fixed time intervals is constant; for tissue growth it increases continually. Our results describe the cavity and tissue kinetics that occur during rapid brain enlargement. Such information is important for understanding normal development of the brain and may provide insight into the mechanisms of genesis of certain congenital malformations such as microcephaly and hydrocephaly.