Optic tectum morphogenesis: A step‐by‐step model based on the temporal–spatial organization of the cell proliferation. Significance of deterministic and stochastic components subsumed in the spatial organization

Abstract

Background: Cell proliferation plays an important morphogenetic role. This work analyzes the temporalspatial organization of cell proliferation as an attempt to understand its contribution to the chick optic tectum (OT) morphogenesis. Results: A morphogenetic model based on space-dependent differences in cell proliferation is presented. Step1: a medial zone of high mitotic density (mZHMD) appears at the caudal zone. Step2: the mZHMD expands cephalically forming the dorsal curvature and then duplicates into two bilateral ZHMDs (bZHMD). Step3: the bZHMDs move toward the central region of each hemitectum. Step4: the planar expansion of both bZHMD and a relative decrement in the dorsal midline growth produces a dorsal medial groove separating the tectal hemispheres. Step5: a relative caudal displacement of the bZHMDs produces the OT caudal curvature. Numerical sequences derived from records of mitotic cells spatial coordinates, analyzed as stochastic point processes, show that they correspond to 1/f (b) processes. The spatial organization subsumes deterministic and stochastic components. Conclusions: The deterministic component describes the presence of a long-range influence that installs an asymmetric distribution of cell proliferation, i.e., an asymmetrically located ZHMD that print space-dependent differences onto the tectal corticogenesis. The stochastic component reveals short-range anti-correlations reflecting spatial clusterization and synchronization between neighboring cells. Developmental Dynamics 241:1043-1061, 2012. V C 2012 Wiley Periodicals, Inc.Key words: developing CNS; mitotic cell organization; nonlinear analyses; morphogenesis Key findings:The signals representing the mitotic cell spatial organization display 1/f type spectrum. The signals subsume deterministic components that reveal the existence of long-range influences. The signals subsume stochastic fluctuations revealing short-range anti-correlations between adjacent cells. The differential displacements of zones of high mitotic density regulate planar expansion. The asymmetric proliferation prints space-dependent histogenetic changes to the tectal corticogenesis.

Sonic hedgehog (Shh)/Gli modulates the spatial organization of neuroepithelial cell proliferation in the developing chick optic tectum

“…GliA and Shh electroporation alter the intertectal sulcus formation. It is considered that the medial-dorsal furrow, i.e., the longitudinal groove preceding the intertectal fissure (intertectal sulcus) formation, involves a relative shortening of the dorsal midline -with respect to the lateral region of each hemitectum- due to a relative decrease in the NEc proliferation along the dorsal-medial region [10]. The dorsal-medial groove formation is a relevant morphogenetic feature of the DMB since it is required for intectectal sulcus formation and subsequent segregation of the right and left tectal hemispheres.…”

“…Thus, most of the additional mNEc produced by GliA or Shh electroporation appeared adjacent to another mNEc. Considering that the increase in the mNEc density and the intercalation of additional mNEcs occurs preferentially between or within the smaller clusters [10], it is likely that the proliferative effect of the Shh pathway preferentially takes places at zones where mNEc are involved in symmetrical divisions and neuroepithelial tangential expansion.…”

“…It is known that the midbrain DV axis is established at a time when the vast majority of midbrain cells corresponds to NEcs (between stages 12–18; embryonic day (ED) 2–3); afterwards (ED3-4) a change in their adhesive properties lead to a reduction in cell mixing and to a clear structural regionalization into dorsal (alar) and ventral (basal) regions [9]. These processes are followed by an intensive proliferative activity in the alar plate [10,11] leading to a massive expansion of the tectal hemispheres between ED4-6.…”

The developing optic tectum: An asymmetrically organized system and the need for a redefinition of the notion of sensitive period

“…In fact, frequency analyses of numerical sequences representing the mNScs distributions correspond to 1/f (β) ‐like spectra that include low frequency components with high amplitude. These oscillations are considered to represent long‐range ordering influences (Goldberger et al, 1986; Eke et al, 2002) and were interpreted as a manifestation of the polarity installed by the IsO (Wurst and Bally‐Cuif, 2001; Alexandre and Wassef, 2003; Rapacioli et al, 2012b). An emergent feature of this asymmetry is the presence of a zone of high mitotic density (Zhmd) in the caudal region of the OT (Fig.…”

“…The developing OT displays a cph‐cd asymmetric proliferative activity. This is manifested by the presence of the Zhmd that appears around the IsO node and that, after a defined set of displacements, remains at a constant position respect to the caudal midline (Rapacioli et al, 2012b). Submitting the chick embryo to a controlled aerogenic hypoxia (between ED4‐ED6) produces a 20% global decrease in the density of proliferating NSc.…”