Cochlear afferent nerve fibers (ANF) are the first neurons in the ascending auditory pathway. We investigated the low-voltage activating K⁺ channels expressed in ANF dendrites using isolated rat cochlear segments. Whole cell patch clamp recordings were made from the dendritic terminals of ANFs. Outward currents activating at membrane potentials as low as -64 mV were observed in all dendrites studied. These currents were inhibited by 4-aminopyridine (4-AP), a blocker known to preferentially inhibit low-voltage activating K⁺ currents (I_KL) in CNS auditory neurons and spiral ganglion neurons. When the dendritic I_KL was blocked by 4-AP, the EPSP decay time was significantly prolonged, suggesting that dendritic I_KL speeds up the decay of EPSPs and likely modulates action potentials of ANFs. To reveal molecular subtype of dendritic I_KL, α-dendrotoxin (α-DTX), a selective inhibitor for K_v1.1, K_v1.2, and K_v1.6 containing channels, was tested. α-DTX inhibited 23±9% of dendritic I_KL. To identify the α-DTXsensitive and α-DTX-insensitive components of I_KL, immunofluorescence labeling was performed. Strong K_v1.1- and K_v1.2-immunoreactivity was found at unmyelinated dendritic segments, nodes of Ranvier, and cell bodies of most ANFs. A small fraction of ANF dendrites showed K_v7.2- immunoreactivity. These data suggest that dendritic I_KL is conducted through K_v1.1and K_v1.2 channels, with a minor contribution from K_v7.2 and other as yet unidentified channels.