Properties and Functional Role of Voltage-Dependent Potassium Channels in Dendrites of Rat Cerebellar Purkinje Neurons

Abstract

We characterized the properties and functional roles of voltage-dependent potassium channels in the dendrites of Purkinje neurons studied in rat cerebellar slices. Using outside-out patches formed <or=250 microm away from the soma, we found that depolarization-activated potassium channels were present at high density throughout the dendritic tree. Currents required relatively large depolarizations for activation (midpoint, approximately -10 mV), had rapid activation and deactivation kinetics, and inactivated partially (20-70% over 200 msec) with both fast (time constant, 15-20 msec) and slow (300-400 msec) components. Inactivating and noninactivating components were both blocked potently by external tetraethylammonium (half-block by 150 microm) and 4-aminopyridine (half-block by 110 microm). The voltage dependence, kinetics, and pharmacology suggest a predominant contribution by Kv3 family subunits, and immunocytochemical experiments showed staining for both Kv3.3 and Kv3.4 subunits in the dendritic tree. In the proximal dendrite, potassium channels were activated by passively spread sodium spikes recorded at the same position, and experiments using dual recordings showed that the channels serve to actively dampen back-propagation of somatic sodium spikes. In more distal dendrites, potassium currents were activated by voltage waveforms taken from climbing fiber responses, suggesting that they help shape these responses as well. The requirement for large depolarizations allows dendritic Kv3 channels to shape large depolarizing events while not disrupting spatial and temporal summation of smaller excitatory postsynaptic potentials.

Properties and expression of Kv3 channels in cerebellar Purkinje cells

“…FSNs, including PCs, require channels with special functional features, such as Kv3 voltage-dependent K + channels (Rudy and McBain, 2001;Akemann and Knopfel, 2006). In agreement with previous studies (Sacco and Tempia, 2002;Martina et al, 2003;McKay and Turner, 2004), we show that PCs express very large voltagedependent and Ca 2+ independent K + currents sensitive to submillimolar doses of TEA. In our study, in order to isolate such currents, we used two independent experimental protocols, which were both effective, as shown by the superimposable results obtained for the voltage dependence of activation.…”

“…Our single-cell RT-PCR analysis adds new data to the discussion of a subject where contrasting results have been reported. Regarding Kv3.1, a low but detectable expression was shown by Perney et al (1992) and Weiser et al (1994), while a lack of expression was reported by Weiser et al (1995), Martina et al (2003) and McMahon et al (2004). Regarding Kv3.4, Weiser et al (1994) reported a weak expression by in-situ hybridization, while by immunohistochemistry the results depended on the type of antibody used (Veh et al, 1995;Laube et al, 1996;Martina et al, 2003).…”

“…Cerebellar Purkinje cells (PCs) are FSNs, which express both a resurgent Na + current (Raman et al, 1997) and Kv3 K + channels (Martina et al, 2003;McKay and Turner, 2004). Kv3 currents have been studied in outside-out somatic and dendritic patches pulled from PCs from rats in a late phase of development, when they express the Kv3.3 and Kv3.4 subunits (Martina et al, 2003;McKay and Turner, 2004).…”

“…Kv3 currents have been studied in outside-out somatic and dendritic patches pulled from PCs from rats in a late phase of development, when they express the Kv3.3 and Kv3.4 subunits (Martina et al, 2003;McKay and Turner, 2004). Under these conditions, Kv3 currents were found to inactivate either with a double exponential time course (rapid time constant 10-20 ms; slow time constant 0.2-0.5 s) with no significant difference between soma and dendrites (Martina et al, 2003) or with a single, slow time constant (0.5-1 s; McKay and Turner, 2004). The latter study also described a significant voltage dependence of slow inactivation with a V 1/2 (− 51.7 mV) very close to the threshold for action potentials.…”

Stress-induced corneal epithelial apoptosis mediated by K+ channel activation

“…These channels exhibit relatively fast inactivation as do the Kv1.4, Kv4.1, Kv4.2, and Kv4.3 channels. Kv3.4 expression has been found in the hippocampus, cerebellum, brain stem, spinal cord, skeletal muscle, arterial smooth muscle cells and pancreatic acinar cells (Weiser et al, 1994;Vullhorst et al, 1998;Rudy et al, 1999;Gopel et al, 2000;Abbott et al, 2001;Han et al, 2002;Martina et al, 2003). It performs an important role in modulating electrical excitability of neurons and muscle fibers.…”