Distinct Roles of Kv1 and Kv3 Potassium Channels at the Calyx of Held Presynaptic Terminal

Abstract

Despite identification of >100 potassium channel subunits, relatively little is known about their roles in synaptic transmission. To address this issue we recorded presynaptic potassium currents (IPK) directly from the calyx of Held terminal in brainstem slices of rats. IPK was composed of a 4-aminopyridine (4-AP)-sensitive component and a smaller 4-AP-insensitive component composed of an iberiotoxin-sensitive current and an unidentified slowly activating potassium current. IPK could also be separated into a tetraethylammonium (TEA; 1 mm)-sensitive high-voltage-activated component and a margatoxin (10 nm)-sensitive low-voltage-activated component, which was also blocked by dendrotoxin-I (200 nm) and tityustoxin-Kalpha (100 nm). In outside-out patches excised from calyceal terminals, TEA (1 mm) consistently and to a large extent attenuated IPK, whereas margatoxin attenuated IPK only in a subset of patches (three of seven). Immunocytochemical examination using Kv subtype-specific antibodies indicated that multiple Kv1 and Kv3 subtypes were present at the calyceal terminal. In paired presynaptic and postsynaptic whole-cell recordings, TEA (1 mm) increased both the duration and peak amplitude of presynaptic action potentials and simultaneously potentiated EPSCs. Margatoxin alone had no such effect but reduced the amount of depolarization required for action potential generation, thereby inducing a burst of spikes when the nerve terminal was depolarized for a prolonged period. Thus, at the calyx of Held terminal, Kv3 channels directly regulate evoked transmitter release, whereas Kv1 channels reduce nerve terminal excitability, thereby preventing aberrant transmitter release. We conclude that both Kv3 and Kv1 channels contribute differentially to maintaining the fidelity of synaptic transmission at the calyx of Held.

Loss of Kv3.1 Tonotopicity and Alterations in cAMP Response Element-Binding Protein Signaling in Central Auditory Neurons of Hearing Impaired Mice

“…If this defect is confined to hair cells, our work strongly suggests that a normal ongoing pattern of auditory stimulation in the auditory brainstem is required for maintenance of expression of the transcription factor CREB, its state of phosphorylation, and the tonotopic gradient of the potassium channel Kv3.1. Other ion channels (e.g., Kv1 and Kv3) are also expressed in the auditory brainstem (Ishikawa et al, 2003). Inspection of the upstream regions for these channel genes, however, indicates that there are no CRE consensus sites in the promoter regions.…”

Information processing in the axon

“…Several subtypes of voltage-gated potassium channels have been identified in myelinated and unmyelinated axons. K v 1.1, K v 1.2, K v 1.4, K v 3.1 and K v 3.4 have been identified in mammalian axons [6][7][8][9][10][11][12][13][14] . In addition, large-conductance calcium-dependent potassium channels (BK, also called Maxi-K or Slo1 channels) are present in axons and presynaptic terminals [15][16][17][18][19] .…”

Cortical Interneuron Subtypes Vary in Their Axonal Action Potential Properties

“…and Aghajanian, 2001;Monaghan et al, 2001;Ishikawa et al, 2003;Devaux et al, 2004;Guan et al, 2006;Inda et al, 2006;Kole et al, 2007;Shu et al, 2007b;Lorincz and Nusser, 2008;Rasband, 2010;Debanne et al, 2011;Bender and Trussell, 2012), and is similar to the dependence of layer 5 pyramidal cells on Kv1 channels for spike repolarization in their axons, but not somata (Kole et al, 2007;Shu et al, 2007b;. Our studies also suggest a dependence of SOM-expressing (RS), but not FS, somata and axons on BK Ca 2ϩ -activated K ϩ channels for spike repolarization because the application of IBTX, a relatively specific blocker of BK channels, resulted in a significant broadening of SOM somatic and axonal action potentials (Fig.…”