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Retinal ganglion cell axons must make a decision at the embryonic optic chiasm to grow into the appropriate optic tract. To gain insight into the cues that play a role in sorting out the crossed from the uncrossed optic axons, we investigated the sequence of their initial ingrowth in rhesus monkey embryos. Two carbocyanine dyes, 1,1'-dioctadecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate and 4-(4-dihexadecylaminostyryl)-N-methylpyridinium iodide, were placed, respectively, into the left and right retinas to identify the course of uncrossed and crossed retinal axons through the optic chiasm and tract. Our results show that at embryonic day 36 the most advanced retinal projections are uncrossed. At this age the leading crossed axons are just reaching the chiasmatic midline, whereas the uncrossed fibers have already entered the optic tract. This indicates that the pathfinding of these pioneer uncrossed fibers does not require the presence of retinal axons from the opposite eye. At subsequent stages of development (embryonic days 40 and 42) there is a clear partial segregation of the uncrossed and crossed retinal axons within the optic tract: the uncrossed-component course is in the deeper portion of the optic tract, whereas the crossed component lies in a more superficial region. Thus, the spatial organization of retinal axons within the primordial optic tract reflects the sequential addition of the uncrossed and crossed retinal fibers. The orderly and sequential ingrowth of these pioneer retinal axons indicates that specific chiasmatic cues are expressed early in development and that such pioneer fibers may serve as guides for the later-arriving retinal fibers.

Organization of pioneer retinal axons within the optic tract of the rhesus monkey.