Excitability of Type II Cochlear Afferents

Two types of sensory hair cells in the mammalian cochlea signal through anatomically distinct populations of spiral ganglion afferent neurons. The solitary inner hair cell ribbon synapse uses multivesicular release to trigger action potentials that encode acoustic timing, intensity, and frequency in each type I afferent. In contrast, cochlear outer hair cells (OHCs) have a far weaker effect on their postsynaptic targets, the type II spiral ganglion afferents. OHCs typically release single vesicles with low probability so that extensive summation is required to reach the relatively high action potential initiation threshold. These stark differences in synaptic transfer call into question whether type II neurons contribute to the cognitive perception of sound. Given the sparse and weak synaptic inputs from OHCs, the electrical properties of type II afferents are crucial in determining whether synaptic responses can sum to evoke an action potential to convey information to the cochlear nucleus. In the present work, dual-electrode recordings determined that type II afferents of rats have length constants that exceed the length of the distal, spiral process, enabling spatial summation from widespread OHCs. Focal application of tetrodotoxin localized the spike initiation zone to the type II proximal, radial process, near the spiral ganglion, in agreement with the high voltage threshold measured in the spiral process. These measured membrane properties were incorporated into a compartmental model of the type II neuron to demonstrate that neurotransmitter release from at least six OHCs is required to trigger an action potential in a type II neuron.