Avian cochlear nucleus neurons exhibit tonotopic specializations across development.

Tonotopy is a hallmark feature of auditory structures that describes the spatial separation of sound frequencies along a gradient from high to low. Identifying biophysical differences along the frequency axis is essential for understanding how tonotopic maps develop in auditory structures and how these maps serve specific functions. In the mammalian cochlear nucleus and the analogous avian nucleus magnocellularis (NM), neurons are arranged along a tonotopic gradient resulting from ordered synaptic connections from the auditory nerve. Although mature NM neurons exhibit some intrinsic (i.e., ion channel) differences along the tonotopic axis, it is unclear whether these intrinsic properties of high- and low-frequency neurons diverge in phenotype across development or if they instead converge by embryonic maturation to resemble each other, suggesting offset developmental timelines. Using whole cell patch-clamp electrophysiology, we recorded from high- and low-frequency NM neurons in the embryonic chicken at early (E12-13), middle (E15-16), and late (E20-21) developmental stages. High- and low-frequency neurons differed in their action potential rise and repolarization rates during development, but these differences disappeared by late development, indicating a tonotopic developmental progression from high- to low-frequency neurons. However, neuronal input resistance, rheobase, and action potential latency were distinct across the tonotopic axis and remained so across development. High-frequency neurons had more low-voltage-activated potassium channels than low-frequency neurons at each developmental stage, thereby mediating differences in action potential properties. Overall, although some intrinsic properties converged in high- and low-frequency neurons by embryonic maturity, other disparities persisted, suggesting distinct phenotypes of high- and low-frequency neurons.NEW & NOTEWORTHY Auditory structures are organized along a tonotopic (i.e., frequency) axis from high- to low-frequencies. In the inner ear and auditory regions within the brainstem, high-frequency neurons develop earlier than low-frequency neurons. Our report challenges the notion that developmental differences along the tonotopic axis are solely attributable to a tonotopic developmental progression. In the avian cochlear nucleus, distinct intrinsic properties contribute to the varied developmental timeline, thereby promoting differential development along the tonotopic axis.