The evolution of forebrain contralaterality as a response to eye development: the path of least resistance.

Rodger Guy Loosemore

Abstract


The origins of vertebrate forebrain contralaterality remain to be adequately explained. A new and novel idea outlined previously by this author as the Inversion Hypothesis (2009) proposed that the vertebrate forebrain developed its ‘wrong-sidedness’ as a response to the inversion of visual images in an ancestral vertebrate possessing a single frontal eye. Here we develop further the likely mechanisms such processes would entail. Using the single frontal eye of ancestral protochordates as a theoretical starting point for the evolution of bilateral vision in early vertebrates, a simple evolutionary pathway involving incremental improvements in retinal design shows how forebrain contralaterality could evolve due to the requirements set by geometric optical physics alone. This untested proposition, while challenging in many respects, provides a concise and credible framework based on established biological data, from which testable corollaries can now be drawn.


Keywords


Contralaterality; Inversion Hypothesis; visual evolution; cyclopia

References


. Berrill, N. J. 1987. Early chordate evolution I. Amphioxus, the riddle of the sands. Int. J. Invert. Reprod. Devel. 11, 1-14

. Borowsky, R. 2008. Restoring sight in blind cavefish. Current Biology. Vol 18;1, 23-24

. Cronly-Dillon, J. and Gregory, R. (Eds). 1991. Vision and visual dysfunction, Vol. 3; Evolution of the eye and visual systems. Macmillan Press.

. Dawkins, R. 1996. Climbing Mount Improbable. Viking. Great Britiain.

. De Miguel, E., Rodicio, M., Anadon, R. 1990. Organisation of the visual system in larval lampreys: an HRP study. J. Comp Neurol. 15;302(3):529-42

. Delsuc, F., Brinkmann, H., Chourrout, D. and Philippe, H. 2006. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439, 965-968

. Donoghue, P. C. J., Purnell, M. A. and Aldridge, R. J. 1998. Conodont anatomy, chordate phylogeny and vertebrate classification. Lethaia 31, 211-219

. 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

. Holland, P. W. H. 1996. Molecular biology of lancelets: insights into development and evolution. Isr. J. Zool. 42, S247-S272.

. Holland, P. 2006. My sister is a sea squirt? Heredity, 96, 424-425

. Janvier P. 2008. Early jawless vertebrates and cyclostome origins. Zoological Science 25(10), 1045-1056

. Janvier, P., and Arsenault, M. 2007. The anatomy of Euphanerops longaevus Woodward,1900, an anaspid-like jawless vertebrate from the Upper Devonian of Miguasha, Quebec, Canada. Geodiversitas 29(1), 143-216

. Jeffery, G. 2001. Architecture of the optic chiasm and the mechanisms that sculpt its development. Physiological Reviews, Vol. 81, No. 4

. Jeffery, G. and Erskine, L. 2005. Variations in the architecture and development of the vertebrate optic chiasm. Progress in Rteinal and Eye Research 24; 721-753

. Kosareva, A. 1980. Retinal projections in lamprey (Lampetra fluviatilis). J. Hirnforsch, 21(3):243-56

. Kusunoki, T. and Amemiya, F. 1983. Retinal projections in the hagfish, Eptatretus burgeri. Brain Research, 262; 295-298

. Lacalli, T.C. 1996. Frontal eye circuitry, rostral sensory pathways and brain organisation in amphioxus larvae: evidence from 3D reconstructions. Phil. Trans. R. Soc. Lond. B. 351, 243-263

. Lacalli, T. C. 1998. The developing dorsal ganglion of the salp Thalia democratica, and the nature of the ancestral chordate brain. Phil. Trans. R. Soc. Lond. B 353, 1943-1967

. Lacalli, T. C. 2001. New perspectives on the evolution of protochordate sensory and locomotory systems, and the origin of brains and heads. Phil. Trans. R. Soc. Lond. B 356, 1565-1572

. Lacalli, T.C. 2002. Sensory pathways in amphioxus larvae I. Constituent fibres of the rostral and anterodorsal nerves, their targets and evolutionary significance. Acta Zoologica (Stockholm) 83: 149-166

. Lacalli, T.C., and Holland, L.Z. 1998. The developing dorsal ganglion of the salp Thalia democratica, and the nature of the ancestral chordate brain. Phil. Trans. R. Soc. Lond. B. 353, 1943-1967

. Lacalli, T., Holland, N., and West, J. 1994. Landmarks in the anterior central nervous system of amphioxus larvae. Phil. Trans. R. Soc. Lond. B 344; 165-185

. Llinas, R. 2003. The contribution of Santiago Ramon y Cajal to functional neuroscience. Nature Reviews; Neuroscience, 4, 77-80

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

. Mogi, K., Misawa, K., Utsunomiya, K., Kamada, Y., Yamazaki, T., Takeuchi, S., andToyoizumi, R. 2009. Optic chasm 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

. Northcutt, R. G. and Gans, C. 1983. The genesis of neural crest and epidermal placodes: A reinterpretation of vertebrate origins. Q Rev Biol 58, 1-28

. O’Leary, D., Gerfen, C., Cowan, N. 1983. The development and restriction of the ipsilateral retinofugal projection in the chick. Brain Res. 312, 93-109.

. Ramon y Cajal, S. 1898. Estructura del kiasma optico y teoria general de los entrecruzamientos de las vias nerviosas. Rev Trim Micrografica, 3:15-65

. Rembold, M., Loosli, F., Adams, R.J., Wittbrodt, J. 2006. Individual cell migration serves as the driving force for optic vesicle evagination. Science 313, 1130-1134

. Sarnat, H. and Netsky, M. 1974. Evolution of the nervous system. Oxford University Press.

. Schwab, I., Ho, V., Roth, A., Blankenship, T., and Fitzgerald, P. 2001. Evolutionary attempts at 4 eyes in vertebrates. Tr. Am. Ophth. Soc. Vol. 99, 145-157

. Stokes, M. D. and Holland, N. D. 1995. Ciliary hovering in larval lancelets. Biol. Bull. 188, 231-233

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


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