The Sound of Silence

Science's STKE  06 Nov 2007:
Vol. 2007, Issue 411, pp. tw403
DOI: 10.1126/stke.4112007tw403

The spontaneous firing of auditory neurons triggered by the release of the neurotransmitter glutamate from the inner hair cells (IHCs) of the cochlea is critical for neuronal survival during development of the auditory system. However, how these responses are triggered before the auditory canal has opened (that is, without sound as a stimulus) is unknown. Tritsch et al. removed cochlea from postnatal rats with closed auditory canals, performed whole-cell voltage clamp experiments, and measured low-frequency spontaneous currents and extracellular potentials in the supporting cells of a structure called Kölliker’s organ, which resides close to the IHCs. Antagonists of the P2 purinergic receptors P2Y and P2X inhibited these spontaneous potentials, as did the ATP-hydrolyzing enzyme, apyrase. The supporting cells contain connexin 26 and are connected to each other by gap junctions, and ATP-dependent spontaneous potentials were blocked by gap junction inhibitors. The authors then simultaneously measured light scattering and electrical activity in the Kölliker’s organ and nearby IHCs and demonstrated ATP-dependent spontaneous currents in the IHCs that were coincident with waves of cell-shape changes and currents in the supporting cells of the Kölliker’s organ. Whole-cell recordings of afferent neurons at the base of IHCs showed that both endogenous (from the supporting cells) and exogenous ATP elicited glutamate-dependent synaptic currents. Finally, cell-shape changes, extracellular potentials, and spontaneous IHC currents were almost completely absent in the cochlea of rats whose auditory canals had opened. The lack of spontaneous action potentials in the IHCs of animals that can hear prevents interference with the accurate detection of sound. Forsythe discusses the implications of these findings in accompanying commentary.

N. X. Tritsch, E. Yi, J. E. Gale, E. Glowatzki, D. E. Bergles, The origin of spontaneous activity in the developing auditory system. Nature 450, 50-55 (2007). [PubMed]

I. D. Forsythe, A fantasia on Kölliker’s organ. Nature 450, 43-44 (2007). [PubMed]