Regional heterogeneities of oligodendrocytes underlie biased Ranvier node spacing along single axons in sound localization circuit

Spacing of Ranvier nodes along myelinated axons is a critical determinant of conduction velocity, influencing spike arrival timing and hence neural circuit function. In the chick brainstem auditory circuit, the pattern of nodal spacing varies regionally along single axons, enabling precise binaural integration for sound localization. Using this model, we investigated the potential factors underlying the biased nodal spacing pattern. 3D morphometry revealed that these axons were almost fully myelinated by oligodendrocytes exhibiting distinct morphologies and cell densities across regions after hearing onset. The structure of axons did not affect internodal length. Inhibiting vesicular release from the axons did not affect internodal length or oligodendrocyte morphology, but caused unmyelinated segments on the axons by suppressing oligodendrogenesis near the presynaptic terminals. These results suggest that the regional heterogeneity in the intrinsic properties of oligodendrocytes is a prominent determinant of the biased nodal spacing pattern in the sound localization circuit, while activity-dependent signaling supports the pattern by ensuring adequate oligodendrocyte density. Our findings highlight the importance of oligodendrocyte heterogeneity in fine-tuning neural circuit function.