Saltatory axonal conduction in the avian retina

In contrast to most parts of the vertebrate nervous system, ganglion cell axons in the retina typically lack myelination. In the majority of species, ganglion cell axons only become myelinated after leaving the retina to form the optic nerve. The avian retina, however, presents a remarkable exception in that ganglion cell axons are partly myelinated in the retinal nerve fibre layer. It was hypothesized that the optically detrimental properties of retinal myelination are evolutionarily offset by advantages in spike conduction velocity. Using high-resolution multielectrode array recordings, we analysed the spike conduction in the retina of various avian species in comparison to mammalian species. Indeed, mammals showed lower conduction velocities than avian species. Myelinated axons typically achieved higher conduction velocities than unmyelinated axons. Notably, some myelinated axons exhibited conduction velocities lower than those of unmyelinated axons. Anatomical analyses revealed that myelination in the nerve fibre layer was accompanied by the formation of nodes of Ranvier. The internode length was positively correlated with the axon diameter. In physiological recordings, the spatial extent of simultaneously active nodes was positively correlated with the conduction velocity. Conversely, the internode length and the activation kinetics of a node were weak predictors of conduction velocity. Overall, this study illuminates the unique features of the avian retina and offers insights into the functional requirements and evolutionary pressures of myelination affecting conduction velocity in the nervous system. KEY POINTS: Intraretinal saltatory axonal spike conduction was studied across multiple avian species using high-resolution multielectrode arrays. The highest conduction velocities were observed exclusively in saltatory axons, while the lowest were found in non-saltatory axons. However, slow myelinated axons exist, exhibiting a surprisingly large overlap in conduction velocities with unmyelinated axons. The spatial extent of a spike showed a strong positive correlation with conduction velocity. The internodal length exhibited a positive correlation with axon diameter, and the variability in internodal length was smaller within individual axons than across axons. Intraretinal axonal conduction velocities across species appear to align with their ecological niche. The maximal intraretinal spike conduction velocity observed in birds was up to four times faster than in rodents.