Origins of avian ocular and periocular tissues

Abstract

The mesenchyme which surrounds the avian embryonic eye and forms all periocular skeletal and connective tissues, including the orbit and part of the cornea, is derived from two sources, the ectodermal neural crest and the mesoderm. Due to difficulties in distinguishing cells of these separate origins, the precise contributions of each to periocular tissues has not been defined. By transplanting labeled neural creast or mesoderm cells into unlabeled host embryos we have been able to catalogue first the migratory patterns of these populations and then their precise derivatives. Some donor tissues were labeled with [ 3H]thymidine; in other cases embryonic quail cells, which contain a replicating heterochromatin marker, were grafted into chick hosts. As the optic vesicle forms, its caudal (future temporal) surface is contacted by a sparse population of mesodermal mesenchyme; the rest of the eye is closely surrounded by superficial ectoderm. Shortly thereafter neural crest cells migrate over the caudal and rostral surfaces of the eye, forming the maxillary and frontonasal processes as well as presumptive scleral and choroidal cells. Neural crest cells form all of the skeletal and connective tissues adjacent to the medial, fnasal, ienrior, and lateral parts of the eye, including the endothelial and stromal cells of the cornea and much of the orbit. Most of the tissues behind the eye are derived from mesoderm, with the exception of the squamosal (temporal) bone. The myofibers of extrinsic ocular muscles are mesodermal, but connective tissues associated with these muscles are of neural crest origin. The ciliary muscles are formed from neural crest cells. Periocular vascular endothelial cells are all mesodermal, but peri-vascular connective tissues, including associated smooth muscles cells, are of neural crest origin. By performing heterotopic transplantations, for example replacing the chick prosencephalic neural crest with quail metencephalic crest, we have proved that neural crest cells from other regions of the head can mimic the development of periocular crest cells. This proves that the environment through which these cells migrate plays an essential role in establishing the timing and spatial patterns of their movement. Included in the environment are the basement membranes associated with epithelial tissues, such as the optic vesicle and superficial ectoderm. We have described several instances in which basement membranes underlying these epithelia become tightly apposed and appear to act as barriers to cell migration. The patterns of basement membrane apposition and subsequent separation are described and correlated with patterns of mesenchymal cell migrations.