Action-potential propagation gated by an axonal I_A-like K⁺ conductance in hippocampus

Abstract

Integration of membrane-potential changes is traditionally reserved for neuronal somatodendritic compartments. Axons are typically considered to transmit reliably the result of this integration, the action potential¹, to nerve terminals^2,3. By recording from pairs of pyramidal cells in hippocampal slice cultures^4,5,6, we show here that the propagation of action potentials to nerve terminals is impaired if presynaptic action potentials are preceded by brief or tonic hyperpolarization. Action-potential propagation fails only when the presynaptic action potential is triggered within the first 15–20 ms of a depolarizing step from hyperpolarized potentials; action-potential propagation failures are blocked when presynaptic cells are impaled with electrodes containing 4-aminopyridine, indicating that a fast-inactivating, A-type K⁺ conductance is involved. Propagation failed between some, but not all, of the postsynaptic cells contacted by a single presynaptic cell, suggesting that the presynaptic action potentials failed at axonal branch points. We conclude that the physiological activation of an I_A-like potassium conductance can locally block propagation of presynaptic action potentials in axons of the central nervous system. Thus axons do not always behave as simple electrical cables: their capacity to transmit action potentials is determined by a time-dependent integration of recent membrane-potential changes.