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Distribution and function of potassium channels in the electrosensory lateral line lobe of weakly electric apteronotid fish

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Abstract

Potassium channels are one of the fundamental requirements for the generation of action potentials in the nervous system, and their characteristics shape the output of neurons in response to synaptic input. We review here the distribution and function of a high-threshold potassium channel (Kv3.3) in the electrosensory lateral line lobe of the weakly electric fish Apteronotus leptorhynchus, with particular focus on the pyramidal cells in this brain structure. These cells contain both high-threshold Kv3.3 channels, as well as low-threshold potassium channels of unknown molecular identity. Kv3.3 potassium channels regulate burst discharge in pyramidal cells and enable sustained high frequency firing through their ability to reduce an accumulation of low-threshold potassium current.

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Abbreviations

CCb:

Corpus cerebelli

EGp:

Eminentia granularis pars posterior

ELL:

Electrosensory lateral line lobe

EOD:

Electric organ discharge

GC1:

Type-1 granule cells

GC2:

Type-2 granule cells

IKHT :

High-threshold potassium channel

IKLT :

Low-threshold potassium channel

JAR:

Jamming avoidance response

LC:

Caudal lobe of cerebellum

NADPH-d:

Nicotinamide adenine dinucleotide phosphate-diaphorase

TEA:

Tetraethylammonium

V 1/2 :

Half-activation voltage

References

  • Baranauskas G, Tkatch T, Nagata K, Yeh JZ, Surmeier DJ (2003) Kv3.4 subunits enhance the repolarizing efficiency of Kv3.1 channels in fast-spiking neurons. Nat Neurosci 6:258–266

    Article  PubMed  CAS  Google Scholar 

  • Barnes-Davies M, Barker MC, Osmani F and Forsythe ID (2004) Kv1 currents mediate a gradient of principal neuron excitability across the tonotopic axis in the rat lateral superior olive. Eur J Neurosci 19:25–33

    Article  Google Scholar 

  • Bastian J (1986a) Gain control in the electrosensory system mediated by descending inputs to the electrosensory lateral line lobe. J Neurosci 6:553–562

    PubMed  CAS  Google Scholar 

  • Bastian J (1986b) Gain control in the electrosensory system: a role for the descending projections to the electrosensory lateral line lobe. J Comp Physiol A 158:505–515

    Article  PubMed  CAS  Google Scholar 

  • Bastian J, Courtright J (1991) Morphological correlates of pyramidal cell adaptation rate in the electrosensory lateral line lobe of weakly electric fish. J Comp Physiol A 168:393–407

    Article  PubMed  CAS  Google Scholar 

  • Bastian J, Nguyenkim J (2001) Dendritic modulation of burst-like firing in sensory neurons. J Neurophysiol 85:10–22

    PubMed  CAS  Google Scholar 

  • Bastian J, Courtright J, Crawford J (1993) Commissural neurons of the electrosensory lateral line lobe of Apteronotus leptorhynchus: morphological and physiological characteristics. J Comp Physiol A 173:257–274

    Article  PubMed  CAS  Google Scholar 

  • Bastian J, Chacron MJ, Maler L (2004) Plastic and nonplastic pyramidal cells perform unique roles in a network capable of adaptive redundancy reduction. Neuron 41:767–779

    Article  PubMed  CAS  Google Scholar 

  • Berman NJ, Maler L (1998) Interaction of GABAB-mediated inhibition with voltage-gated currents of pyramidal cells: computational mechanism of a sensory searchlight. J Neurophysiol 80:3197–3213

    PubMed  CAS  Google Scholar 

  • Berman NJ, Maler L (1999) Neural architecture of the electrosensory lateral line lobe: adaptations for coincidence detection, a sensory searchlight and frequency-dependent adaptive filtering. J Exp Biol 202:1243–1253

    PubMed  Google Scholar 

  • Brew HM, Forsythe ID (1995) Two voltage-dependent K+ conductances with complementary functions in postsynaptic integration at a central auditory synapse. J Neurosci 15:8011–8022

    PubMed  CAS  Google Scholar 

  • Cai X, Liang CW, Muralidharan S, Kao JP, Tang CM, Thompson SM (2004) Unique roles of SK and Kv4.2 potassium channels in dendritic integration. Neuron 44:351–364

    Article  PubMed  CAS  Google Scholar 

  • Carr CE, Maler L (1986) Electroreception in gymnotiform fish. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 319–373

    Google Scholar 

  • Carr CE, Heiligenberg W, Rose GJ (1986) A time-comparison circuit in the electric fish midbrain. I. Behavior and physiology. J Neurosci 6:107–119

    PubMed  CAS  Google Scholar 

  • Chandy KG, Gutman GA (1993) Nomenclature for mammalian potassium channel genes. Trends Pharmacol Sci 14:434

    Article  PubMed  CAS  Google Scholar 

  • Coetzee WA, Amarillo Y, Chiu J, Chow A, Lau D, McCormack T, Moreno H, Nadal MS, Ozaita A, Pountney D, Saganich M, Vega-Saenz de Miera E, Rudy B (1999) Molecular diversity of K+ channels. Ann N Y Acad Sci 868:233–285

    Article  PubMed  CAS  Google Scholar 

  • Critz SD, Wible BA, Lopez HS, Brown AM (1993) Stable expression and regulation of a rat brain K+ channel. J Neurochem 60:1175–1178

    Article  PubMed  CAS  Google Scholar 

  • Dodson PD, Barker MC, Forsythe ID (2002) Two heteromeric Kv1 potassium channels differentially regulate action potential firing. J Neurosci 22:6953–6961

    PubMed  CAS  Google Scholar 

  • Dodson PD, Billups B, Rusznak Z, Szucs G, Barker MC, Forsythe ID (2003) Presynaptic rat Kv1.2 channels suppress synaptic terminal hyperexcitability following action potential invasion. J Physiol 550:27–33

    Article  PubMed  CAS  Google Scholar 

  • Doiron B, Longtin A, Turner RW, Maler L (2001) Model of gamma frequency burst discharge generated by conditional backpropagation. J Neurophysiol 86:1523–1545

    PubMed  CAS  Google Scholar 

  • Doiron B, Noonan L, Lemon N, Turner RW (2003) Persistent Na+ current modifies burst discharge by regulating conditional backpropagation of dendritic spikes. J Neurophysiol 89:324–337

    Article  PubMed  Google Scholar 

  • Dunlap KD (2002) Hormonal and body size correlates of electrocommunication behavior during dyadic interactions in a weakly electric fish, Apteronotus leptorhynchus. Horm Behav 41:187–194

    Article  PubMed  CAS  Google Scholar 

  • Dunlap KD, Larkins-Ford J (2003) Diversity in the structure of electrocommunication signals within a genus of electric fish, Apteronotus. J Comp Physiol A 189:153–161

    CAS  Google Scholar 

  • Dunlap KD, Oliveri LM (2002) Retreat site selection and social organization in captive electric fish, Apteronotus leptorhynchus. J Comp Physiol A 188:469–477

    Article  CAS  Google Scholar 

  • Erisir A, Lau D, Rudy B, Leonard CS (1999) Function of specific K+ channels in sustained high-frequency firing of fast-spiking neocortical interneurons. J Neurophysiol 82:2476–2489

    PubMed  CAS  Google Scholar 

  • Fernandez FR, Morales E, Rashid AJ, Dunn RJ, Turner RW (2003) Inactivation of Kv3.3 potassium channels in heterologous expression systems. J Biol Chem 278:40890–40898

    Article  PubMed  CAS  Google Scholar 

  • Fernandez FR, Mehaffey WH, Molineux ML, Turner RW (2005) High-threshold K+ current increases gain by offsetting a frequency-dependent increase in low-threshold K+ current. J Neurosci 25:363–371

    Article  PubMed  CAS  Google Scholar 

  • Ferragamo MJ, Oertel D (2002) Octopus cells of the mammalian ventral cochlear nucleus sense the rate of depolarization. J Neurophysiol 87:2262–2270

    PubMed  Google Scholar 

  • Gabbiani F, Metzner W, Wessel R, Koch C (1996) From stimulus encoding to feature extraction in weakly electric fish. Nature 384:564–567

    Article  PubMed  CAS  Google Scholar 

  • Gan L, Kaczmarek LK (1998) When, where, and how much? Expression of the Kv3.1 potassium channel in high-frequency firing neurons. J Neurobiol 37:69–79

    Article  PubMed  CAS  Google Scholar 

  • Han VZ, Bell CC (2003) Physiology of cells in the central lobes of the mormyrid cerebellum. J Neurosci 23:11147–11157

    PubMed  CAS  Google Scholar 

  • Heiligenberg W (1986) Jamming avoidance responses: model systems for neuroethology. In: Bullock TH, Heiligenberg W (eds) Electroreception. Wiley, New York, pp 613–649

    Google Scholar 

  • Heiligenberg W (1991) Neural nets in electric fish. MIT Press, Cambridge

    Google Scholar 

  • von Hehn CA, Bhattacharjee A, Kaczmarek LK (2004) Loss of Kv3.1 tonotopicity and alterations in cAMP response element-binding protein signaling in central auditory neurons of hearing impaired mice. J Neurosci 24:1936–1940

    Article  CAS  Google Scholar 

  • Hodgkin AL, Huxley AF (1952) Movement of sodium and potassium ions during nervous activity. Cold Spring Harb Symp Quant Biol 17:43–52

    PubMed  CAS  Google Scholar 

  • Hoffman DA, Magee JC, Colbert CM, Johnston D (1997) K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387:869–875

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa T, Nakamura Y, Saitoh N, Li WB, Iwasaki S, Takahashi T (2003) Distinct roles of Kv1 and Kv3 potassium channels at the calyx of held presynaptic terminal. J Neurosci 23:10445–10453

    PubMed  CAS  Google Scholar 

  • Kanemasa T, Gan L, Perney TM, Wang LY, Kaczmarek LK (1995) Electrophysiological and pharmacological characterization of a mammalian Shaw channel expressed in NIH 3T3 fibroblasts. J Neurophysiol 74:207–217

    PubMed  CAS  Google Scholar 

  • Krahe R, Gabbiani F (2004) Burst firing in sensory systems. Nat Rev Neurosci 5:13–23

    Article  PubMed  CAS  Google Scholar 

  • Lannoo MJ, Maler L, Tinner B (1989) Ganglion cell arrangement and axonal trajectories in the anterior lateral line nerve of the weakly electric fish Apteronotus leptorhynchus (Gymnotiformes). J Comp Neurol 280:331–342

    Article  PubMed  CAS  Google Scholar 

  • Lee TE, Philipson LH, Nelson DJ (1996) N-type inactivation in the mammalian Shaker K+ channel Kv1.4. J Membr Biol 151:225–235

    Article  PubMed  CAS  Google Scholar 

  • Lemon N, Turner RW (2000) Conditional spike backpropagation generates burst discharge in a sensory neuron. J Neurophysiol 84:1519–1530

    PubMed  CAS  Google Scholar 

  • Lewis A, McCrossan ZA, Abbott GW (2004) MinK, MiRP1, and MiRP2 diversify Kv3.1 and Kv3.2 potassium channel gating. J Biol Chem 279:7884–7892

    Article  PubMed  CAS  Google Scholar 

  • Lien CC, Jonas P (2003) Kv3 potassium conductance is necessary and kinetically optimized for high-frequency action potential generation in hippocampal interneurons. J Neurosci 23:2058–2068

    PubMed  CAS  Google Scholar 

  • Macica CM, Kaczmarek LK (2001) Casein kinase 2 determines the voltage dependence of the Kv3.1 channel in auditory neurons and transfected cells. J Neurosci 21:1160–1168

    PubMed  CAS  Google Scholar 

  • MacIver MA, Sharabash NM, Nelson ME (2001) Prey-capture behavior in gymnotid electric fish: motion analysis and effects of water conductivity. J Exp Biol 204:543–557

    PubMed  CAS  Google Scholar 

  • Maler L (1979) The posterior lateral line lobe of certain gymnotoid fish: quantitative light microscopy. J Comp Neurol 183:323–363

    Article  PubMed  CAS  Google Scholar 

  • Maler L, Mugnaini E (1994) Correlating gamma-aminobutyricacidergic circuits and sensory function in the electrosensory lateral line lobe of a gymnotiform fish. J Comp Neurol 345:224–252

    Article  PubMed  CAS  Google Scholar 

  • Maler L, Sas EK, Rogers J (1981) The cytology of the posterior lateral line lobe of high-frequency weakly electric fish (Gymnotidae): dendritic differentiation and synaptic specificity in a simple cortex. J Comp Neurol 195:87–139

    Article  PubMed  CAS  Google Scholar 

  • Maler L, Sas E, Carr CE, Matsubara J (1982) Efferent projections of the posterior lateral line lobe in gymnotiform fish. J Comp Neurol 211:154–164

    Article  PubMed  CAS  Google Scholar 

  • Martina M, Schultz JH, Ehmke H, Monyer H, Jonas P (1998) Functional and molecular differences between voltage-gated K+ channels of fast-spiking interneurons and pyramidal neurons of rat hippocampus. J Neurosci 18:8111–8125

    PubMed  CAS  Google Scholar 

  • Martina M, Yao GL, Bean BP (2003) Properties and functional role of voltage-dependent potassium channels in dendrites of rat cerebellar Purkinje neurons. J Neurosci 23:5698–5707

    PubMed  CAS  Google Scholar 

  • McAnelly ML, Zakon HH (2000) Coregulation of voltage-dependent kinetics of Na+ and K+ currents in electric organ. J Neurosci 20:3408–3414

    PubMed  CAS  Google Scholar 

  • McKay BE, Turner RW (2004) Kv3 K+ channels enable burst output in rat cerebellar Purkinje cells. Eur J Neurosci 20:729–739

    Article  PubMed  CAS  Google Scholar 

  • McKay BE, Molineux ML, Mehaffey WH, Turner RW (2005) Kv1 K+ channels control Purkinje cell output to facilitate postsynaptic rebound discharge in deep cerebellar neurons. J Neurosci 25:1481–1492

    Article  PubMed  CAS  Google Scholar 

  • Mehaffey WH, Doiron B, Maler L, Turner RW (2005) Deterministic multiplicative gain control with active dendrites. J Neurosci 25:9968–9977

    Article  PubMed  CAS  Google Scholar 

  • Nelson ME, MacIver MA, Coombs S (2002) Modeling electrosensory and mechanosensory images during the predatory behavior of weakly electric fish. Brain Behav Evol 59:199–210

    Article  PubMed  Google Scholar 

  • Noonan L, Doiron B, Laing C, Longtin A, Turner RW (2003) A dynamic dendritic refractory period regulates burst discharge in the electrosensory lobe of weakly electric fish. J Neurosci 23:1524–1534

    PubMed  CAS  Google Scholar 

  • Oswald AM, Chacron MJ, Doiron B, Bastian J, Maler L (2004) Parallel processing of sensory input by bursts and isolated spikes. J Neurosci 24:4351–4362

    Article  PubMed  CAS  Google Scholar 

  • Parameshwaran S, Carr CE, Perney TM (2001) Expression of the Kv3.1 potassium channel in the avian auditory brainstem. J Neurosci 21:485–494

    PubMed  CAS  Google Scholar 

  • Perney TM, Marshall J, Martin KA, Hockfield S, Kaczmarek LK (1992) Expression of the mRNAs for the Kv3.1 potassium channel gene in the adult and developing rat brain. J Neurophysiol 68:756–766

    PubMed  CAS  Google Scholar 

  • Phan M, Maler L (1983) Distribution of muscarinic receptors in the caudal cerebellum and electrosensory lateral line lobe of gymnotiform fish. Neurosci Lett 42:137–143

    Article  PubMed  CAS  Google Scholar 

  • Rashid AJ, Dunn RJ (1998) Sequence diversity of voltage-gated potassium channels in an electric fish. Mol Brain Res 54:101–107

    Article  PubMed  CAS  Google Scholar 

  • Rashid AJ, Dunn RJ, Turner RW (2001a) A prominent soma–dendritic distribution of Kv3.3 K+ channels in electrosensory and cerebellar neurons. J Comp Neurol 441:234–247

    Article  PubMed  CAS  Google Scholar 

  • Rashid AJ, Morales E, Turner RW, Dunn RJ (2001b) The contribution of dendritic Kv3 K+ channels to burst threshold in a sensory neuron. J Neurosci 21:125–135

    PubMed  CAS  Google Scholar 

  • Rudy B, McBain CJ (2001) Kv3 channels: voltage-gated K+ channels designed for high-frequency repetitive firing. Trends Neurosci 24:517–526

    Article  PubMed  CAS  Google Scholar 

  • Shibata R, Wakazono Y, Nakahira K, Trimmer JS, Ikenaka K (1999) Expression of Kv3.1 and Kv4.2 genes in developing cerebellar granule cells. Dev Neurosci 21:87–93

    Article  PubMed  CAS  Google Scholar 

  • Smith GT, Zakon HH (2000) Pharmacological characterization of ionic currents that regulate the pacemaker rhythm in a weakly electric fish. J Neurobiol 42:270–286

    Article  PubMed  CAS  Google Scholar 

  • Svirskis G, Kotak V, Sanes DH, Rinzel J (2002) Enhancement of signal-to-noise ratio and phase locking for small inputs by a low-threshold outward current in auditory neurons. J Neurosci 22:11019–11025

    PubMed  CAS  Google Scholar 

  • Tharani Y, Thurlow GA, Turner RW (1996) Distribution of 4-conotoxin GVIA binding sites in teleost cerebellar and electrosensory neurons. J Comp Neurol 364:456–472

    Article  PubMed  CAS  Google Scholar 

  • Toledo-Rodriguez M, Blumenfeld B, Wu C, Luo J, Attali B, Goodman P, Markram H (2004) Correlation maps allow neuronal electrical properties to be predicted from single-cell gene expression profiles in rat neocortex. Cereb Cortex 14:1310–1327

    Article  PubMed  Google Scholar 

  • Trussell LO (1997) Cellular mechanisms for preservation of timing in central auditory pathways. Curr Opin Neurobiol 7:487–492

    Article  PubMed  CAS  Google Scholar 

  • Turner RW, Moroz LL (1995) Localization of nicotinamide adenine dinucleotide phosphate-diaphorase activity in electrosensory and electromotor systems of a gymnotiform teleost, Apteronotus leptorhynchus. J Comp Neurol 356:261–274

    Article  PubMed  CAS  Google Scholar 

  • Turner RW, Maler L, Deerinck T, Levinson SR, Ellisman MH (1994) TTX-sensitive dendritic sodium channels underlie oscillatory discharge in a vertebrate sensory neuron. J Neurosci 14:6453–6471

    PubMed  CAS  Google Scholar 

  • Turner RW, Lemon N, Doiron B, Rashid AJ, Morales E, Longtin A, Maler L, Dunn RJ (2002) Oscillatory burst discharge generated through conditional backpropagation of dendritic spikes. J Physiol (Paris) 96:517–530

    Article  Google Scholar 

  • Wang D, Maler L (1994) The immunocytochemical localization of glutamate in the electrosensory system of the gymnotiform fish, Apteronotus leptorhynchus. Brain Res 653:215–222

    Article  PubMed  CAS  Google Scholar 

  • Wang LY, Gan L, Forsythe ID, Kaczmarek LK (1998) Contribution of the Kv3.1 potassium channel to high-frequency firing in mouse auditory neurones. J Physiol (Lond) 509:183–194

    Article  CAS  Google Scholar 

  • Weiser M, Vega-Saenz de Miera E, Kentros C, Moreno H, Franzen L, Hillman D, Baker H, Rudy B (1994) Differential expression of Shaw-related K+ channels in the rat central nervous system. J Neurosci 14:949–972

    PubMed  CAS  Google Scholar 

  • Weiser M, Bueno E, Sekirnjak C, Martone ME, Baker H, Hillman D, Chen S, Thornhill W, Ellisman M, Rudy B (1995) The potassium channel subunit KV3.1b is localized to somatic and axonal membranes of specific populations of CNS neurons. J Neurosci 15:4298–4314

    PubMed  CAS  Google Scholar 

  • Zakon H, Oestreich J, Tallarovic S, Triefenbach F (2002) EOD modulations of brown ghost electric fish: JARs, chirps, rises, and dips. J Physiol (Paris) 96:451–458

    Article  CAS  Google Scholar 

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Acknowledgements

We gratefully acknowledge E. Morales and L. Noonan for earlier work on Kv3 channels and the expert technical assistance of M. Kruskic and M. LaChance. The work reviewed here was supported by a CIHR grant and CIHR Group Grant (RWT, RD), a CIHR Doctoral Studentship (FRF), Alberta Provincial Graduate Scholarships (FRF, WHM), and an AHFMR Scientist Award (RWT).

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Authors and Affiliations

  1. Hotchkiss Brain Institute, University of Calgary, 3330 Hospital Dr. N.W., , T2N 4N1, Calgary, AB, Canada

    W. H. Mehaffey, F. R. Fernandez & R. W. Turner

  2. University of Toronto, M5S 1A8, Toronto, ON, Canada

    A. J. Rashid

  3. McGill University, H3G 1A4, Montreal, QC, Canada

    R. J. Dunn

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  1. W. H. Mehaffey
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  2. F. R. Fernandez
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  3. A. J. Rashid
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  4. R. J. Dunn
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  5. R. W. Turner
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Correspondence to R. W. Turner.

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W. H. Mehaffey and F. R. Fernandez contributed equally to this work.

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Mehaffey, W.H., Fernandez, F.R., Rashid, A.J. et al. Distribution and function of potassium channels in the electrosensory lateral line lobe of weakly electric apteronotid fish. J Comp Physiol A 192, 637–648 (2006). https://doi.org/10.1007/s00359-006-0103-z

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