An enigmatic translocation of the vertebrate primordial eye field
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(2020) 20:129
REVIEW
Open Access
An enigmatic translocation of the vertebrate primordial eye field R. G. Loosemore1* , S. D. Matthaei2 and T. C. Stanger2
Abstract The primordial eye field of the vertebrate embryo is a single entity of retinal progenitor cells spanning the anterior neural plate before bifurcating to form bilateral optic vesicles. Here we review fate mapping data from zebrafish suggesting that prior to evagination of the optic vesicles the eye field may undergo a Maypole-plait migration of progenitor cells through the midline influenced by the anteriorly subducting diencephalon. Such an enigmatic translocation of scaffolding progenitors could have evolutionary significance if pointing, by way of homology, to an ancient mechanism for transition of the single eye field in chordates to contralateral eye fields in vertebrates. Keywords: Contralaterality, Optic primordium, Primordial eye field, Optic chiasm, Inversation, Chiasmation, Cyclopean, Translocation, Retinal progenitor cells
Background The vertebrate forebrain (prosencephalon), with its rostral telencephalon and caudal diencephalon, exhibits a cluster of four neuroanatomic anomalies in all species. The evolutionary origins of hemisphericity, contralaterality, optic chiasm, and retinal inversion, continue to defy plausible explanation. If the eye as a neural budding of the lightsensitive diencephalon is central to the development of all, exposure of the enigmatic processes that transitioned the single eye spot of chordates to the paired eyes of vertebrates might explain these anomalies. If cogent, this explanation would clarify embryological homologies, enhancing potential developmental and medical implications. Early in vertebrate gastrulation the neural plate is elongated by convergent extension [65] where laterally placed progenitor cells move toward the midline, intercalating into the midline [36, 37, 69]. This process of neurulation, which characterises the tubular folding of most of the neural plate to form the neural tube [9, 24] is a defining developmental process in vertebrates. The distinctive anterior of the neural plate (ANP) where the eye and * Correspondence: [email protected] 1 Maclean District Hospital, Union St, Maclean, NSW 2463, Australia Full list of author information is available at the end of the article
forebrain develop, does not undergo this same neurulation as once thought [3, 23]. Its development begins earlier than neurulation, largely as a single coherent field of retinal progenitor cells (RPCs) that contracts from an early broad field to then bifurcate and evaginate to form bilateral optic vesicles [1, 2, 4, 15, 23, 31, 33, 46, 53, 64, 76, 80]. Contraction of the eye field (EF) follows an initial period of expansion characterised by proliferation of RPCs as gastrulation proceeds, with RPCs and their progeny migrating individually [71]. This contraction involves a ‘roll over’ migration of lateral RPCs over medial RPCs toward the midline [15, 64]. However, at the midline where RPCs are then observed to dive ven
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