Saltatory axonal conduction in the avian retina

Abstract

In contrast to most parts of the vertebrate nervous system, the ganglion cell axons in the retina typically lack any myelination. Ganglion cell axons of most species only become myelinated once they leave the retina to form the optic nerve. The avian retina is a well known exception in that ganglion cell axons are partly myelinated in the retinal nerve fiber layer. However, the functional and structural properties of myelination in the nerve fiber layer remain elusive. Here, we used large-scale multi-electrode array recordings in combination with immunohisto-chemistry and fluorescence microscopy of European quail and pigeon retinas to investigate myelination of retinal ganglion cell axons. Intraretinal myelination was accompanied by the formation of nodes of Ranvier. The internode length was positively correlated with the axon diameter. The variability of internode lengths along each axon was significantly smaller than across axons. Saltatory conduction of action potentials was observed in a large population of recorded cells. On average, myelinated axons had higher conduction velocities than unmyelinated axons. However, both groups showed a significant overlap at low velocities. The number of simultaneously active nodes was positively correlated with the conduction velocity. In contrast, the internode length and the time it took a node to activate were weak predictors for the conduction velocity. However, the conduction velocity was well described by the number of activated nodes, the internode length, and the activation time in concert. Significance StatementMyelination of axons serves saltatory signal conduction, which greatly decreases the time it takes for an action potential to travel along an axon. Retinal ganglion cell (RGC) axons, as part of the central nervous system, are usually devoid of myelin in mammals, whereas avian RGC axons are myelinated well before they enter the optic nerve. Using high resolution multi electrode arrays, we were able to image the saltatory propagation of a spike across an axon. Most axons with saltatory conduction were faster than non-saltatory axons. Surprisingly, a large number of saltatory axons had low conduction velocities. The signal conduction patterns were more diverse than expected. The velocity could be explained by the number of simultaneously activated nodes of Ranvier, the internode length and their activation time.