Close Packing of Cells in Vestibular Epithelia Supports Local Electrical Potentials that Reduce Latency of Action Potential Generation

In the vestibular system, upon transduction of head motion, ionic currents from type I sensory hair cells alter [K ⁺ ] and electrical potentials in an extended synaptic cleft formed by a calyx terminal of the associated afferent neuron. During excitatory stimuli, these changes in turn modulate post-synaptic currents across the calyx inner face to depolarize the afferent and initiate action potentials. Within the tightly packed columnar vestibular sensory epithelium, electrical currents from the hair cell and calyx must also traverse non-synaptic extracellular spaces and generate local extracellular potentials before dispersing into the perilymph beneath the basement membrane. Here we show that such dynamic electrical potentials enhance action potential generation by reducing outward K ⁺ currents on both the inner and outer faces of the calyx. This effect also influences adjacent calyces and may explain the abundance of calyx terminals in amniotes where there is a need for rapid recognition of changes in head orientation and acceleration.