Abstract
Timing between action potentials is crucial for information processing in real neural networks. However, the physical axonal lengths largely determine the time necessary for action potentials to reach postsynaptic neurons. Retinal ganglion cell (RGC) axons form the retinal nerve fiber layer (RNFL). The human RNFL shows a highly stereotypical organization characterized by the presence of the fovea, a specialized region enabling high-resolution vision tasks, such as reading. To reach the papilla (i.e., the optic nerve head), the axons of the RNFL do not cross the fovea, but rather some axons detour around it following significantly longer trajectories. We investigated whether different axonal lengths in the human RNFL entail distinct conduction velocities, allowing visual signals to reach the brain synchronously. We used human retinal explants to precisely measure paths and propagation speeds of action potentials of foveal and peripheral RGCs by using high-density microelectrode-array recordings at subcellular resolution. Axonal conduction speeds were spatially heterogeneous and depended on the location of the RGC somas. Around the fovea centralis, action potentials of temporal RGCs traveled up to 50% faster than action potentials of nasal RGCs. In both foveal and peripheral retina, we observed a bimodal distribution of propagation speeds of the two most abundant cell types in primate retina: midget and parasol cells. Peripheral RGC axons exhibited up to three times higher conduction velocities than foveal RGC axons. We modelled the entire human RNFL to predict trajectories (and thus lengths) of RGC axons. The model recapitulated well the organization of the human RNFL and estimates of axonal lengths strongly correlated with observed axonal lengths and action potential propagation speeds. Our measurements suggest that a compensatory mechanism in the human retina contributes to synchronizing the arrival times of visual signals in the brain.