Abstract
Sound intensity is encoded by auditory neuron subgroups that differ in thresholds and spontaneous rates. Whether variations in neuronal biophysics contributes to this functional diversity is unknown. Because intensity thresholds correlate with synaptic position on sensory hair cells, we combined patch clamping with fiber labeling in semi-intact cochlear preparations in neonatal rats from both sexes. The biophysical properties of auditory neurons vary in a striking spatial gradient with synaptic position. Neurons with high thresholds to injected currents contact hair cells at synaptic positions where neurons with high thresholds to sound-intensity are found in vivo. Alignment between in vitro and in vivo thresholds suggests that biophysical variability contributes to intensity coding. Biophysical gradients were evident at all ages examined, indicating that cell diversity emerges in early post-natal development and persists even after continued maturation. This stability enabled a remarkably successful model for predicting synaptic position based solely on biophysical properties.
Highlights
The bipolar afferent neurons of the auditory system are the principle conduits for information transfer from the sensory periphery to the brainstem
Developing spiral ganglion neurons can be classified based on their pattern of connectivity with hair cells
We characterized the morphology and electrophysiology of spiral ganglion neurons (SGN) using whole cell patch-clamp recordings combined with single-cell labeling from the middle turn of rat cochleae ranging in age from post-natal day (P) 1 through P16
Summary
The bipolar afferent neurons of the auditory system are the principle conduits for information transfer from the sensory periphery to the brainstem. Decades of research focusing on this question have led to multiple classification schemes based on in vivo physiology and active zone morphology (Kawase and Liberman, 1992; Liberman and Dodds, 1984; Merchan-Perez and Liberman, 1996). These studies report an association between synaptic position on inner hair cells and intensity thresholds; wherein high-threshold, low-SR SGN preferentially synapse on the modiolar face of an inner hair cell, and low-threshold high-SR SGN synapse on the pillar face
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