The Activity of Spontaneous Action Potentials in Developing Hair Cells Is Regulated by Ca2+-Dependence of a Transient K+ Current

Spontaneous action potentials have been described in developing sensory systems. These rhythmic activities may have instructional roles for the functional development of synaptic connections. The importance of spontaneous action potentials in the developing auditory system is underpinned by the stark correlation between the time of auditory system functional maturity, and the cessation of spontaneous action potentials. A prominent K+ current that regulates patterning of action potentials is IA. This current undergoes marked changes in expression during chicken hair cell development. Although the properties of IA are not normally classified as Ca2+-dependent, we demonstrate that throughout the development of chicken hair cells, IA is greatly reduced by acute alterations of intracellular Ca2+. As determinants of spike timing and firing frequency, intracellular Ca2+ buffers shift the activation and inactivation properties of the current to more positive potentials. Our findings provide evidence to demonstrate that the kinetics and functional expression of IA are tightly regulated by intracellular Ca2+. Such feedback mechanism between the functional expression of IA and intracellular Ca2+ may shape the activity of spontaneous action potentials, thus potentially sculpting synaptic connections in an activity-dependent manner in the developing cochlea.