Expansion, folding, and abnormal lamination of the chick optic tectum after intraventricular injections of FGF2

Abstract

Comparative research has shown that evolutionary increases in brain region volumes often involve delays in neurogenesis. However, little is known about the influence of such changes on subsequent development. To get at this question, we injected FGF2-which delays cell cycle exit in mammalian neocortex-into the cerebral ventricles of chicks at embryonic day (ED) 4. This manipulation alters the development of the optic tectum dramatically. By ED7, the tectum of FGF2-treated birds is abnormally thin and has a reduced postmitotic layer, consistent with a delay in neurogenesis. FGF2 treatment also increases tectal volume and ventricular surface area, disturbs tectal lamination, and creates small discontinuities in the pia mater overlying the tectum. On ED12, the tectum is still larger in FGF2-treated embryos than in controls. However, lateral portions of the FGF2-treated tectum now exhibit volcano-like laminar disturbances that coincide with holes in the pia, and the caudomedial tectum exhibits prominent folds. To explain these observations, we propose that the tangential expansion of the ventricular surface in FGF2-treated tecta outpaces the expansion of the pial surface, creating abnormal mechanical stresses. Two alternative means of alleviating these stresses are tectal foliation and the formation of pial holes. The latter probably alter signaling gradients required for normal cell migration and may generate abnormal patterns of cerebrospinal fluid flow; both abnormalities would generate disturbances in tectal lamination. Overall, our findings suggest that evolutionary expansion of sheet-like, laminated brain regions requires a concomitant expansion of the pia mater.brain evolution | evolutionary developmental biology | proliferation | meninges | cortical folding E volutionary increases in brain region volumes are common (1).For example, the neocortex is disproportionately enlarged in primates relative to other mammals, and the telencephalon is disproportionately enlarged in parrots and songbirds relative to other birds (1-4). Recent work in evolutionary developmental neurobiology has shown that these evolutionary increases in brain region volumes are often caused by delays in cell cycle exit of neuronal precursors (5, 6). Among birds, for example, parrots and songbirds exhibit delayed telencephalic neurogenesis relative to chicken-like birds (7-9). Among mammals, cell cycle exit in the neocortex is similarly delayed in primates, which have a disproportionately enlarged neocortex (5, 10-12).Unfortunately, the downstream effects of delayed cell cycle exit on subsequent developmental processes and adult morphology remain poorly understood. One way to fill this gap in our knowledge is to experimentally recreate the key species differences in the laboratory by means of carefully selected developmental manipulations. A good example of this phenocopy approach was the creation of transgenic mice with a constitutively active form of β-catenin that prolongs proliferation, increases neocortical volume, and generates cortica...

NRP1-mediated Sema3A signals coordinate laminar formation in the developing chick optic tectum

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Systematic, Cross-Cortex Variation in Neuron Numbers in Rodents and Primates

“…This is known to be the case in mammals and in birds (Finlay and Darlington 1995;Finlay et al 1998;Clancy et al 2001;Chenn and Walsh 2002;Striedter 2005;Striedter 2008, 2011;Striedter and Charvet 2008;Dyer et al 2009;McGowan et al 2012;Workman et al 2013). Therefore, although specific data about the length of developmental schedules for most of the species examined here is largely lacking, there is no reason to assume the species described here should depart from the general mammalian pattern established in other primates and rodents.…”

Evolution of connections and cell types: integrating diffusion MR tractography with gene expression data highlights increased cortico-cortical projections in primates

“…The differential growth across the cortex, the migration of neurons along radial glia, and/or the differential expansion of upper versus lower layer neurons are a few proposed mechanisms generating variation in cortical folding between species (Richman et al, 1975;Van Essen, 1997;Toro and Burnod, 2005;Xu et al, 2010;Chen et al, 2013;Striedter et al, 2015;Fernández et al, 2016;Tallinen et al, 2016;Razavi et al, 2017). Modifications to neurogenetic programs are well-documented sources of variation across species, and experimental manipulations of cell proliferation during development impact cortical composition, as well as cortical folding (Dyer et al, 2009;Clowry et al, 2010;Striedter, 2008, 2011;Charvet et al, 2017ab;Lewitus et al, 2013;McGowan et al, 2012McGowan et al, , 2013Nonaka-Kinoshita et al, 2013;Borrell and Götz, 2014;Otani et al, 2016;Tallinen et al, 2016;Toda et al, 2016;Matsumoto et al, 2017;Shinmyo et al, 2017;de Juan Romero and Borrell, 2017). We suggest that the differential composition of neurons across the depth of the cortex may cause major differences in white matter tension between species.…”