Contralateral translocation of progenitor retinal cells observed on bifurcation of the primordial eye field is predicted by the Inversion Hypothesis

Rodger Guy Loosemore

Abstract


Though counter-intuitive, the origins of vertebrate forebrain contralaterality as proposed by the Inversion Hypothesis, are nonetheless eminently predictable. The hypothesis proposes that contralaterality developed to support an evolving single frontal eye in ancestral craniates, predating bilateral vision and development of the optic chiasm. Its most empirically accessible prediction claims that on bifurcation of the embryonic primordial eye field, the majority of progenitor retinal cells (PRCs) must cross the midline to become mature retinal cells in the contralateral eye, in the process creating an incipient optic chiasm. Here we show, by way of a focused review, that, despite a general belief to the contrary, such a translocation has previously been demonstrated in both zebrafish and Xenopus frog embryos.


Keywords


Contralaterality; optic primordium; optic chiasm; Inversion Hypothesis

References


. Adelmann, H. B. 1929a. Experimental studies on the development of the eye. I. The effect of removal of median and lateral areas of the anterior end of the urodelan neural plate on the development of the eyes (Triton teniatus and Amblystoma punctatum). J. Exp. Zool. 54, 249-290.

. Adelmann, H. B. 1929b. Experimental studies on the development of the eye. II. The eye forming potencies of the median portions of the urodelan neural plate on the development of the eyes. (Triton teniatus and Amblystoma punctatum). J. Exp. Zool. 54, 291-317.

. Adelmann, H. B. 1929c. Experimental studies on the development of the eye. III. The effect of the substrate (’Unterlagerung’) on the heterotropic development of median and lateral strips of the anterior end of the neural plate of Amblystoma. J. Exp. Zool. 57, 223-281.

. Adelmann, H. B. 1936a. The problem of cyclopia, Pt. 1. Q. Rev. Biol. 11:161-82.

. Adelmann, H. B. 1936b. The problem of cyclopia, Pt. 11. Q. Rev. Biol. 11:284-304.

. Castro-Gonzalez, C., Luengo-Oroz, M. A., Douloquin, L., Savy, T., Mclani, C., Desnoulez, S., Ledesma-Carbayo, M. J., Bourgine, P., Peyrieras, N., Santos, A. 2010. Towards a digital model of zebrafish embryogenesis. Integration of cell tracking and gene expression quantification. 32nd Annual International Conference of the IEEE EMBS.

. Chow, R. L. and Lang, R. A. 2001. Early eye development in vertebrates. Annu. Rev. Cell Dev. Biol. 17:255-96.

. England, S. J., Blanchard, G. B., Mahadevan, L., Adams, R. J. 2006. A dynamic fate map of the forebrain shows how vertebrate eyes form and explains two causes of cyclopia. Development 133, 4613-4617

. Hatta, K., Kimmel, C. B., Ho, R. K., Walker, C. 1991. The Cyclops mutation blocks specification of the floorplate of the zebrafish central nervous system. Nature 350:339-41.

. Huschke, E. 1832. Uber die Entwicklung des Auges und die damit Zusammenhangende Cyklopie. Meckels Arch. f. Anat. u. Phys. 6, 1-47.

. Jacobson, M. and Hirose, G. 1978. Origin of the retina from both sides of the embryonic brain: a contribution to the problem of crossing at the optic chiasma. Science 202, 637-639.

. Lamb, T., Collin, S., Pugh, E. 2007. Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup. Nature Reviews Neuroscience. 8, 960-976.

. LePlat, G. 1919. Action du milieu sur le developpement des larves d’amphibiens. Localization et differenciation des premieres ebauches oculaires chez les vertebres. Cyclopie et anophtalmie. Arch. De Biol. 30, 231-321.

. Li, H., Tierney, C., Wen, L., Rao, Y. 1997. A single morphogenetic field gives rise to two retina primordia under the influence of the prechordal plate. Development 124: 603-15.

. Loosemore, R. G. 2009. The inversion hypothesis: A novel explanation for the contralaterality of the human brain. Bioscience Hypotheses 2, 375-382.

. Loosemore, R. G. 2011a. The evolution of forebrain contralaterality as a response to eye development: the path of least resistance. Hypotheses in the Life Sciences. Vol 1.

. Meckel, J. F. 1826. Uber Verschmelzungsbildungen. Arch. F. Anat. u. Phys. 1, 1-47.

. Mogi, K., Misawa, K., Utsunomiya, K., Kamada, Y., Yamazaki, T., Takeuchi, S., Toyoizumi, R. 2009. Optic chiasm in the species of order Clupeiformes, family Clupeidae: Optic chiasm of Spratelloides gracilis shows an opposite laterality to that of Etrumeus teres. Laterality, 14(5), 495-514.

. Nilsson, D-E., and Pelger, S. 1994. A pessimistic estimate of the time required for an eye to evolve. Proceedings of the Royal Society of London, B. 256, 53-58.

. Rebagliati, M. R., Toyama, R., Haffter, P., Dawid, I. B. 1998. Cyclops encodes a nodal-related factor in midline

signalling. Proc. Natl. Acad. Sci. USA 95, 9932-9937.

. Rembold, M., Loosli, F., Adams, R. J., Wittbrodt, J.

Individual cell migration serves as the driving force for optic vesicle evagination. Science. 313, 1130-1134.

. Sampath, K., Rubinstein, A. L., Cheng, A. M., Liang, J.O., Fekany, K., et al. 1998. Induction of the zebrafish ventral brain and floorplate requires Cyclops/nodal signalling. Nature 395:185-89.

. Spemann, H. 1904. Uber experimentellerzeugte Doppelbildungen mit cyclopischem Defekt. Zool. Jahr. 7, 429-470.

. Spemann, H. 1912. Uber die Entwicklung umgedrehter Hirnteile bei Amphibienembryonen. Zool. Jahrbuch. 15, 1-48.

. Stockhard, C. R. 1913. Location of the optic anlage in Amblystoma and the interpretation of certain eye defects. Proc. Soc. Exp. Biol. Med. 10, 162-164.

. Varga, Z., Wegner, J., Westerfield, M. 1999. Anterior movement of ventral diencephalic precursors separates the primordial eye field in the neural plate and requires Cyclops. Development 126, 5533-5546.

. Wilson, S. and Houart, C. 2004. Early steps in the development of the forebrain. Developmental Cell, Vol. 6, 167-181.

. Woo, K. and Fraser, S. E. 1995. Order and coherence in the fate map of the zebrafish nervous system. Development 121:2595-609.


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