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Laboratoire de Biologie Cellulaire et Moléculaire de l'Audition, Equipe Mixte Institut National de la Santé et de la Recherche Médicale 99-27, Université de Bordeaux 2, Centre Hospitalier Universitaire Hôpital Pellegrin, 33076 Bordeaux, France
Submitted 23 December 2002; accepted in final form 9 February 2003
Large-conductance calcium-activated potassium (BK) channels are known to
play a prominent role in the hair cell function of lower vertebrates where
these channels determine electrical tuning and regulation of neurotransmitter
release. Very little is known, by contrast, about the role of BK channels in
the mammalian cochlea. In the current study, we perfused specific toxins in
the guinea pig cochlea to characterize the role of BK channels in cochlear
neurotransmission. Intracochlear perfusion of charybdotoxin (ChTX) or
iberiotoxin (IbTX) reversibly reduced the compound action potential (CAP) of
the auditory nerve within minutes. The cochlear microphonics (CM at f1 = 8 kHz
and f2 = 9.68 kHz) and their distortion product (DPCM at 2f1–f2) were
essentially not affected, suggesting that the BK specific toxins do not alter
the active cochlear amplification at the outer hair cells (OHCs). We also
tested the effects of these toxins on the whole cell voltage-dependent
membrane current of isolated guinea pig inner hair cells (IHCs). ChTX and IbTX
reversibly reduced a fast outward current (activating above –40 mV,
peaking at 0 mV with a mean activation time constant 
ranging between 0.5
and 1 ms). A similar block of a fast outward current was also observed with
the extracellular application of barium ions, which we believe permeate
through Ca2+ channels and block BK channels. In situ
hybridization of Slo antisense riboprobes and immunocytochemistry
demonstrated a strong expression of BK channels in IHCs and spiral ganglion
and to a lesser extent in OHCs. Overall, our results clearly revealed the
importance of BK channels in mammalian cochlear neurotransmission and
demonstrated that at the presynaptic level, fast BK channels are a significant
component of the repolarizing current of IHCs.
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