Amphioxus, motion detection, and the evolutionary origin of the vertebrate retinotectal map

Thurston Lacalli

doi:10.1186/s13227-018-0093-2

Abstract

The axonal projection from the retina to the optic tectum maps visual information isomorphically from one to the other and serves as a model for the development of sensory maps more generally in the vertebrate brain. How or why this connection evolved is not known, nor why the midbrain is so important to the processing of visual information. Amphioxus is potentially informative here because its eye homolog, the frontal eye, also has a neural connection to a region of the brain now known to be homologous with the caudal diencephalon and midbrain. The frontal eye has only a one-dimensional receptor array, but simple alterations to the pattern and plane of cell division would have been sufficient to generate a structure more like the vertebrate retina. Accounting for the retinotectal map poses more of a problem. The hypothesis developed here is that this is best explained as a consequence of a prior association between the roof of the anterior nerve cord and an array of rhabdomeric photoreceptors, homologous with the Joseph cells of amphioxus, that were used by the common ancestor of amphioxus and vertebrates for detecting moving shadows. Hence, a rudimentary tectal map could have been present before the evolution of image-forming eyes and been coopted by them secondarily. Assuming the orientation of this map was fixed from the start relative to the external world, its retinal counterpart would have had to adjust to this to accommodate the image reversal that accompanies the conversion of a flat receptor array to a camera-type eye. Exploring this hypothesis further will require more information than is currently available on the Joseph cells, especially as to where and how their neural output is processed.

Highlights

The vertebrate retina maps to the optic tectum in an isomorphic fashion, so the visual field as registered by the former is essentially reproduced on the surface of the latter
The situation in amphioxus is complicated by the presence of multiple photoreceptor systems ([10], see Fig. 1), among which is a set of rhabdomeric receptors, known as Joseph cells, that form a contiguous layer along the dorsal surface of the nerve cord in the head region of latestage larvae and the adult
Gene expression patterns in the developing neural tube show that the location of the anterior-most members of the Joseph cell series corresponds to the roof of the amphioxus homolog of the caudal diencephalon plus the midbrain, so they occupy a region that, in vertebrates, gives rise to both the optic tectum and pretectum, as well as the thalamic nuclei involved in visual processing

Summary

Introduction

The vertebrate retina maps to the optic tectum (the superior colliculus in mammals) in an isomorphic fashion, so the visual field as registered by the former is essentially reproduced on the surface of the latter. Amphioxus is currently considered the best available model for ancestral chordates [3], but features only peripherally in most accounts of eye evolution (for an exception, see Fig. 5.5 in [4]).

Results

Conclusion