Distribution of Kv1‐like potassium channels in the electromotor and electrosensory systems of the weakly electric fish Apteronotus leptorhynchus

Abstract

The electromotor and electrosensory systems of the weakly electric fish Apteronotus leptorhynchus are model systems for studying mechanisms of high-frequency motor pattern generation and sensory processing. Voltage-dependent ionic currents, including low-threshold potassium currents, influence excitability of neurons in these circuits and thereby regulate motor output and sensory filtering. Although Kv1-like potassium channels are likely to carry low-threshold potassium currents in electromotor and electrosensory neurons, the distribution of Kv1 alpha subunits in A. leptorhynchus is unknown. In this study, we used immunohistochemistry with six different antibodies raised against specific mammalian Kv1 alpha subunits (Kv1.1-Kv1.6) to characterize the distribution of Kv1-like channels in electromotor and electrosensory structures. Each Kv1 antibody labeled a distinct subset of neurons, fibers, and/or dendrites in electromotor and electrosensory nuclei. Kv1-like immunoreactivity in the electrosensory lateral line lobe (ELL) and pacemaker nucleus are particularly relevant in light of previous studies suggesting that potassium currents carried by Kv1 channels regulate neuronal excitability in these regions. Immunoreactivity of pyramidal cells in the ELL with several Kv1 antibodies is consistent with Kv1 channels carrying low-threshold outward currents that regulate spike waveform in these cells (Fernandez et al., J Neurosci 2005;25:363-371). Similarly, Kv1-like immunoreactivity in the pacemaker nucleus is consistent with a role of Kv1 channels in spontaneous high-frequency firing in pacemaker neurons. Robust Kv1-like immunoreactivity in several other structures, including the dorsal torus semicircularis, tuberous electroreceptors, and the electric organ, indicates that Kv1 channels are broadly expressed and are likely to contribute significantly to generating the electric organ discharge and processing electrosensory inputs.

Genes linked to species diversity in a sexually dimorphic communication signal in electric fish

“…In A. leptorhynchus , the female Pn expressed more mRNA for the K + channel β2 subunit (Kvβ2, KCNAB2) than the male Pn. Kvβ2 increases the amplitude of Kv1-mediated K + currents, and Kv1 channels are likely candidates for influencing Pn firing (Smith and Zakon 2000; Smith et al 2006). It is possible that increased expression of the Kvβ2 gene in females may lower their EODf by strengthening outward currents during pacemaking ramp potentials, thereby increasing interspike intervals and reducing Pn firing rates.…”

Ionic and neuromodulatory regulation of burst discharge controls frequency tuning

“…This burst mechanism has been shown to be controlled by a variety of intrinsic membrane conductances including persistent sodium currents and high-threshold potassium channels (Ellis et al, 2007b;Fernandez et al, 2005a;Mehaffey et al, 2006;Noonan et al, 2003;Rashid et al, 2001a,b). As channel densities have been shown to vary across the different tuberous maps (Deng et al, 2005;Smith et al, 2006), they may contribute to map-specific computations including frequency selectivity (Metzner and Juranek, 1997;Shumway, 1989a). Furthermore, synaptic input from feedback pathways can have a significant impact on burst firing (Bastian and Nguyenkim, 2001;Chacron and Bastian, 2008;Chacron et al, 2005a;Mehaffey et al, 2007Mehaffey et al, , 2008a.…”

“…One mechanism used to encode specific aspects of the signal involves multiple neuronal representations ('maps') that differentially encode the same stimulus, as found in the auditory and olfactory systems. This often involves gradients of expression of specific ion channels as observed in the ELL (Deng et al, 2005;Ellis et al, 2007b;Mehaffey et al, 2006;Smith et al, 2006) and in mammalian auditory processing, in particular in the auditory brainstem (Li et al, 2001;Perney and Kaczmarek, 1997;von Hehn et al, 2004).…”

Ion channels as molecular targets of glioblastoma electrotherapy

“…Likewise, the orthologs of mammalian K v 1.x-like voltage-gated K + channels are reportedly expressed by tuberous organs that are used for active electrolocation of, e.g., elephantfish (Smith et al, 2006). These tuberous electroreceptors are electrically isolated from the environmental fresh water.…”