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Sodium-dependent potassium channels of a Slack-like subtype contribute to the slow afterhyperpolarization in lamprey spinal neurons

  1. Peter Wallén1,2,
  2. Brita Robertson1,2,
  3. Lorenzo Cangiano1,2,
  4. Peter Löw2,
  5. Arin Bhattacharjee3,
  6. Leonard K. Kaczmarek4,
  7. Sten Grillner1,2

Article first published online: 14 NOV 2007

DOI: 10.1113/jphysiol.2007.138156

Issue

The Journal of Physiology

The Journal of Physiology

Volume 585, Issue 1, pages 75–90, November 2007

Additional Information

How to Cite

Wallén, P., Robertson, B., Cangiano, L., Löw, P., Bhattacharjee, A., Kaczmarek, L. K. and Grillner, S. (2007), Sodium-dependent potassium channels of a Slack-like subtype contribute to the slow afterhyperpolarization in lamprey spinal neurons. The Journal of Physiology, 585: 75–90. doi: 10.1113/jphysiol.2007.138156

Author Information

  1. 1

    Nobel Institute for Neurophysiology, Karolinska Institutet, Stockholm, Sweden

  2. 2

    Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden

  3. 3

    Department Pharmacology & Toxicology, SUNY, Buffalo, NY, USA

  4. 4

    Department of Pharmacology, Yale University School of Medicine, New Haven, CT, USA

*Corresponding author P. Wallén: Nobel Institute for Neurophysiology, Department of Neuroscience, Karolinska Institutet, SE-171 77 Stockholm, Sweden. Email: peter.wallen@ki.se

Publication History

  1. Issue published online: 14 NOV 2007
  2. Article first published online: 14 NOV 2007
  3. (Received 8 June 2007; accepted after revision 20 September 2007; first published online 20 September 2007)

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References

  • Bhattacharjee A, Joiner WJ, Wu M, Yang Y, Sigworth FJ & Kaczmarek LK (2003). Slick (Slo2.1), a rapidly-gating sodium-activated potassium channel inhibited by ATP. J Neurosci 23, 11681–11691.
  • Bhattacharjee A & Kaczmarek LK (2005). For K+ channels, Na+ is the new Ca2+. Trends Neurosci 28, 422–428.
  • Bhattacharjee A, Von Hehn CAA, Mei X, Joiner WJ & Kaczmarek LK (2005). Localization of the Na+-activated K+ channel slick in the rat central nervous system. J Comp Neurol 484, 80–92.
    Direct Link:
  • Bischoff U, Vogel W & Safronov BV (1998). Na+-activated K+ channels in small dorsal root ganglion neurones of rat. J Physiol 510, 743–754.
    Direct Link:
  • Buchanan JT (1993). Electrophysiological properties of identified classes of lamprey spinal neurons. J Neurophysiol 70, 2313–2325.
  • Cangiano L, Wallén P & Grillner S (2002). Role of apamin-sensitive KCa channels for reticulospinal synaptic transmission to motoneuron and for the afterhyperpolarization. J Neurophysiol 88, 289–299.
  • Dale N (1993). A large, sustained Na+- and voltage-dependent K+ current in spinal neurons of the frog embryo. J Physiol 462, 349–372.
  • Dryer SE (1994). Na+-activated K+ channels: a new family of large-conductance ion channels. Trends Neurosci 17, 155–160.
  • Dryer SE (2003). Molecular identification of the Na+-activated K+ channel. Neuron 37, 727–728.
  • El Manira A, Tegnér J & Grillner S (1994). Calcium-dependent potassium channels play a critical role for burst termination in the locomotor network in lamprey. J Neurophysiol 72, 1852–1861.
  • Franceschetti S, Lavazza T, Curia G, Aracri P, Panzica F, Sancini G, Avanzini G & Magistretti J (2003). Na+-activated K+ current contributes to postexcitatory hyperpolarization in neocortical intrinsically bursting neurons. J Neurophysiol 89, 2101–2111.
  • Grillner S (2003). The motor infrastructure: From ion channels to neuronal networks. Nat Rev Neurosci 4, 573–586.
  • Grillner S, Wallén P, Hill R, Cangiano L & El Manira A (2001). Ion channels of importance for the locomotor pattern generation in the lamprey brainstem–spinal cord. J Physiol 533, 23–30.
    Direct Link:
  • Gustafsson B (1974). Afterhyperpolarization and the control of repetitive firing in spinal neurones of the cat. Acta Physiol Scand Suppl 416, 1–47.
  • Hess D & El Manira A (2001). Characterization of a high-voltage-activated IA current with a role in spike timing and locomotor pattern generation. Proc Natl Acad Sci U S A 98, 5276–5281.
  • Hess D, Nanou E & El Manira A (2007). Characterization of Na+-activated K+ currents in larval lamprey spinal cord neurons. J Neurophysiol 97, 3484–3493.
  • Hill RH, Århem P & Grillner S (1985). Ionic mechanisms of 3 types of functionally different neurons in the lamprey spinal cord. Brain Res 358, 40–52.
  • Hill R, Matsushima T, Schotland J & Grillner S (1992). Apamin blocks the slow AHP in lamprey and delays termination of locomotor bursts. Neuroreport 3, 943–945.
  • Hill RH, Svensson E, Dewael Y & Grillner S (2003). 5-HT inhibits N-type but not L-type Ca2+ channels via 5-HT1A receptors in lamprey spinal neurons. Eur J Neurosci 18, 2919–2924.
    Direct Link:
  • Hille B (1972). The permeability of the sodium channel to metal cations in myelinated nerve. J Gen Physiol 59, 637–658.
  • Kernell D (1965). The limits of firing frequency in cat lumbosacral motoneurons possessing different time course of afterhyperpolarization. Acta Physiol Scand 65, 87–100.
    Direct Link:
  • Kettunen P, Hess D & El Manira A (2003). mGluR1, but not mGluR5, mediates depolarization of spinal cord neurons by blocking a leak current. J Neurophysiol 90, 2341–2348.
  • Kettunen P, Krieger P, Hess D & El Manira A (2002). Signaling mechanisms of metabotropic glutamate receptor 5 subtype and its endogenous role in a locomotor network. J Neurosci 22, 1868–1873.
  • Kim U & McCormick DA (1998). Functional and ionic properties of a slow afterhyperpolarization in ferret perigeniculate neurons in vitro. J Neurophysiol 80, 1222–1235.
  • Koh DS, Jonas P & Vogel W (1994). Na+-activated K+ channels localized in the nodal region of myelinated axons of Xenopus. J Physiol 479, 183–197.
  • Krieger P, El Manira A & Grillner S (1996). Activation of pharmacologically distinct metabotropic glutamate receptors depresses reticulospinal-evoked monosynaptic EPSPs in the lamprey spinal cord. J Neurophysiol 76, 3834–3841.
  • Krieger P, Hellgren-Kotaleski J, Kettunen P & El Manira A (2000). Interaction between metabotropic and ionotropic glutamate receptors regulates neuronal network activity. J Neurosci 20, 5382–5391.
  • Lamotte d'Incamps B, Hess D & El Manira A (2004). Control of the temporal fidelity of synaptic transmission by a presynaptic high voltage-activated transient K+ current. Eur J Neurosci 19, 3202–3210.
    Direct Link:
  • Madison DV & Nicoll RA (1984). Control of the repetitive discharge of rat CA 1 pyramidal neurones in vitro. J Physiol 354, 319–331.
  • Martin MM (2002). Changes in electrophysiological properties of lamprey spinal motoneurons during fictive swimming. J Neurophysiol 88, 2463–2476.
  • Matsushima T, Tegnér J, Hill RH & Grillner S (1993). GABAB receptor activation causes a depression of low- and high-voltage-activated Ca2+ currents, postinhibitory rebound, and postspike afterhyperpolarization in lamprey neurons. J Neurophysiol 70, 2606–2619.
  • Meer DP & Buchanan JT (1992). Apamin reduces the late afterhyperpolarization of lamprey spinal neurons, with little effect on fictive swimming. Neurosci Lett 143, 1–4.
  • Morita K, David G, Barrett JN & Barrett EF (1993). Posttetanic hyperpolarization produced by electrogenic Na+-K+ pump in lizard axons impaled near their motor terminals. J Neurophysiol 70, 1874–1884.
  • Parker D, Hill R & Grillner S (1996). Electrogenic pump and a Ca2+- dependent K+ conductance contribute to a posttetanic hyperpolarization in lamprey sensory neurons. J Neurophysiol 76, 540–553.
  • Safronov BV & Vogel W (1996). Properties and functions of Na+-activated K+ channels in the soma of rat motoneurones. J Physiol 497, 727–734.
  • Sah P & Davies P (2000). Calcium-activated potassium currents in mammalian neurons. Clin Exp Pharmacol Physiol 27, 657–663.
    Direct Link:
  • Sah P & Faber ES (2002). Channels underlying neuronal calcium-activated potassium currents. Prog Neurobiol 66, 345–353.
  • Schotland J, Shupliakov O, Wikström M, Brodin L, Srinivasan M, You ZB, Herrera-Marschitz M, Zhang W, Hökfelt T & Grillner S (1995). Control of lamprey locomotor neurons by colocalized monoamine transmitters. Nature 374, 266–268.
  • Schwindt PC & Calvin WH (1973). Nature of conductances underlying rhythmic firing in cat spinal motoneurons. J Neurophysiol 36, 955–973.
  • Scuri R, Mozzachiodi R & Brunelli M (2002). Activity-dependent increase of the AHP amplitude in T sensory neurons of the leech. J Neurophysiol 88, 2490–2500.
  • Tegnér J, Matsushima T, El Manira A & Grillner S (1993). The spinal GABA system modulates burst frequency and intersegmental coordination in the lamprey: differential effects of GABAA and GABAB receptors. J Neurophysiol 69, 647–657.
  • Thompson SM & Prince DA (1986). Activation of electrogenic sodium pump in hippocampal CA1 neurons following glutamate-induced depolarization. J Neurophysiol 56, 507–522.
  • Uchino S, Wada H, Honda S, Hirasawa T, Yanai S, Nakamura Y, Ondo Y & Kohsaka S (2003). Slo2 sodium-activated K+ channels bind to the PDZ domain of PSD-95. Biochem Biophys Res Commun 310, 1140–1147.
  • Wallén P, Buchanan JT, Grillner S, Hill RH, Christenson J & Hökfelt T (1989a). Effects of 5-hydroxytryptamine on the afterhyperpolarization, spike frequency regulation, and oscillatory membrane properties in lamprey spinal cord neurons. J Neurophysiol 61, 759–768.
  • Wallén P, Christenson J, Brodin L, Hill R, Lansner A & Grillner S (1989b). Mechanisms underlying the serotonergic modulation of the spinal circuitry for locomotion in lamprey. Prog Brain Res 80, 321–327.
  • Wallén P & Grillner S (2003). One component of the slow afterhyperpolarization in lamprey neurons is mediated by a Na+ activated K+ current. Soc Neurosci Abs 53.52.
  • Wallén P, Hess D, El Manira A & Grillner S (2002). A slow non Ca2+ dependent afterhyperpolarization in lamprey neurons. Soc Neurosci Abs 546.549.
  • Wallén P, Robertson B, Bhattacharjee A, Kaczmarek LK & Grillner S (2005). KNa channels of the Slack subtype underlie the non-Ca component of the slow AHP in lamprey spinal neurons. Soc Neurosci Abs 152.155.
  • Wikström MA & El Manira A (1998). Calcium influx through N- and P/Q-type channels activate apamin-sensitive calcium-dependent potassium channels generating the late afterhyperpolarization in lamprey spinal neurons. Eur J Neurosci 10, 1528–1532.
    Direct Link:
  • Yuan A, Santi CM, Wei A, Wang ZW, Pollak K, Nonet M, Kaczmarek L, Crowder CM & Salkoff L (2003). The sodium-activated potassium channel is encoded by a member of the Slo gene family. Neuron 37, 765–773.
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