Development of the retinofugal pathway in birds and mammals: evidence for a common 'timetable'

We have compared changes in axon numbers in the developing optic nerves of eight homeotherms (seven mammals and one bird) using data from the available literature and our own material. The proportion of axons lost during development is smaller in the chick (35%) than in mammals (54-74%). The relative magnitude of this loss does not correlate with the extent of the binocular visual field or the size of the retinofugal ipsilateral projection. The timing of developmental events in the retinofugal pathway was compared as a proportion of the period between conception and eye opening (percentage of the 'caecal period', CP). In eutherian mammals, retinal ganglion cells and their target neurons are generated between 30 and 49% of CP (a duration of 19% of CP). In homeotherms, a phase of rapid axon generation begins around 38% of CP and the peak number of axons is reached at about 56% of CP (a duration of 18% of CP). A phase of rapid axon loss begins thereafter, and in most species it ends at about 74% of CP (a duration of 18% of CP), the rate of rapid axons loss being about half the rate of rapid axon generation. The similarity in relative timing (homochrony), like the similarity in the relative magnitude of the axon loss, suggests that cell generation and loss in the retinofugal pathway are influenced by a mechanism common to all homeotherms. We propose that in homeotherms each cohort of retinal ganglion cells is numerically matched with a group of target cells that is at an appropriate stage of maturation ('temporal matching' hypothesis). About twice as many ganglion cells are produced in each cohort than are needed, and their survival is determined by natural selection.