HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Full Text Full Text (PDF) All Versions of this Article: 545/3/783    most recent 2002.029249v1 Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Hu, H. Articles by Storm, J. F. Search for Related Content PubMed PubMed Citation Articles by Hu, H. Articles by Storm, J. F.

Two forms of electrical resonance at theta frequencies, generated by M-current, h-current and persistent Na⁺ current in rat hippocampal pyramidal cells

Hua Hu, Koen Vervaeke and Johan F. Storm

Coherent network oscillations in the brain are correlated with different behavioural states. Intrinsic resonance properties of neurons provide a basis for such oscillations. In the hippocampus, CA1 pyramidal neurons show resonance at theta () frequencies (2-7 Hz). To study the mechanisms underlying -resonance, we performed whole-cell recordings from CA1 pyramidal cells (n = 73) in rat hippocampal slices. Oscillating current injections at different frequencies (ZAP protocol), revealed clear resonance with peak impedance at 2-5 Hz at ~33 °C (increasing to ~7 Hz at ~38 °C). The -resonance showed a U-shaped voltage dependence, being strong at subthreshold, depolarized (~-60 mV) and hyperpolarized (~-80 mV) potentials, but weaker near the resting potential (-72 mV). Voltage clamp experiments revealed three non-inactivating currents operating in the subthresold voltage range: (1) M-current (I_M), which activated positive to -65 mV and was blocked by the M/KCNQ channel blocker XE991 (10 µM); (2) h-current (I_h), which activated negative to -65 mV and was blocked by the h/HCN channel blocker ZD7288 (10 µM); and (3) a persistent Na⁺ current (I_NaP), which activated positive to -65 mV and was blocked by tetrodotoxin (TTX, 1 µM). In current clamp, XE991 or TTX suppressed the resonance at depolarized, but not hyperpolarized membrane potentials, whereas ZD7288 abolished the resonance only at hyperpolarized potentials. We conclude that these cells show two forms of -resonance: 'M-resonance' generated by the M-current and persistent Na⁺ current in depolarized cells, and 'H-resonance' generated by the h-current in hyperpolarized cells. Computer simulations supported this interpretation. These results suggest a novel function for M/KCNQ channels in the brain: to facilitate neuronal resonance and network oscillations in cortical neurons, thus providing a basis for an oscillation-based neural code.

This article has been cited by other articles:

				S. A. Prescott and T. J. Sejnowski Spike-Rate Coding and Spike-Time Coding Are Affected Oppositely by Different Adaptation Mechanisms J. Neurosci., December 10, 2008; 28(50): 13649 - 13661. [Abstract] [Full Text] [PDF]

				S. A. Prescott, S. Ratte, Y. De Koninck, and T. J. Sejnowski Pyramidal Neurons Switch From Integrators In Vitro to Resonators Under In Vivo-Like Conditions J Neurophysiol, December 1, 2008; 100(6): 3030 - 3042. [Abstract] [Full Text] [PDF]

				S. D. Glasgow and C. A. Chapman Conductances Mediating Intrinsic Theta-Frequency Membrane Potential Oscillations in Layer II Parasubicular Neurons J Neurophysiol, November 1, 2008; 100(5): 2746 - 2756. [Abstract] [Full Text] [PDF]

				V. Varga, B. Hangya, K. Kranitz, A. Ludanyi, R. Zemankovics, I. Katona, R. Shigemoto, T. F. Freund, and Z. Borhegyi The presence of pacemaker HCN channels identifies theta rhythmic GABAergic neurons in the medial septum J. Physiol., August 15, 2008; 586(16): 3893 - 3915. [Abstract] [Full Text] [PDF]

				B. A. Neubauer, S. Waldegger, J. Heinzinger, A. Hahn, G. Kurlemann, B. Fiedler, F. Eberhard, H. Muhle, U. Stephani, S. Garkisch, et al. KCNQ2 and KCNQ3 mutations contribute to different idiopathic epilepsy syndromes Neurology, July 15, 2008; 71(3): 177 - 183. [Abstract] [Full Text] [PDF]

				S. M. Montgomery, A. Sirota, and G. Buzsaki Theta and Gamma Coordination of Hippocampal Networks during Waking and Rapid Eye Movement Sleep J. Neurosci., June 25, 2008; 28(26): 6731 - 6741. [Abstract] [Full Text] [PDF]

				R. Narayanan and D. Johnston The h Channel Mediates Location Dependence and Plasticity of Intrinsic Phase Response in Rat Hippocampal Neurons J. Neurosci., May 28, 2008; 28(22): 5846 - 5860. [Abstract] [Full Text] [PDF]

				A. Etxeberria, P. Aivar, J. A. Rodriguez-Alfaro, A. Alaimo, P. Villace, J. C. Gomez-Posada, P. Areso, and A. Villarroel Calmodulin regulates the trafficking of KCNQ2 potassium channels FASEB J, April 1, 2008; 22(4): 1135 - 1143. [Abstract] [Full Text] [PDF]

				M. Manuel, C. Meunier, M. Donnet, and D. Zytnicki Resonant or Not, Two Amplification Modes of Proprioceptive Inputs by Persistent Inward Currents in Spinal Motoneurons J. Neurosci., November 21, 2007; 27(47): 12977 - 12988. [Abstract] [Full Text] [PDF]

				M. Yoshida and A. Alonso Cell-Type Specific Modulation of Intrinsic Firing Properties and Subthreshold Membrane Oscillations by the M(Kv7)-Current in Neurons of the Entorhinal Cortex J Neurophysiol, November 1, 2007; 98(5): 2779 - 2794. [Abstract] [Full Text] [PDF]

				S. D. Glasgow and C. A. Chapman Local Generation of Theta-Frequency EEG Activity in the Parasubiculum J Neurophysiol, June 1, 2007; 97(6): 3868 - 3879. [Abstract] [Full Text] [PDF]

				C. Geisler, D. Robbe, M. Zugaro, A. Sirota, and G. Buzsaki Hippocampal place cell assemblies are speed-controlled oscillators PNAS, May 8, 2007; 104(19): 8149 - 8154. [Abstract] [Full Text] [PDF]

				S. Gasparini, A. Losonczy, X. Chen, D. Johnston, and J. C. Magee Associative pairing enhances action potential back-propagation in radial oblique branches of CA1 pyramidal neurons J. Physiol., May 1, 2007; 580(3): 787 - 800. [Abstract] [Full Text] [PDF]

				N. Gu, K. Vervaeke, and J. F. Storm BK potassium channels facilitate high-frequency firing and cause early spike frequency adaptation in rat CA1 hippocampal pyramidal cells J. Physiol., May 1, 2007; 580(3): 859 - 882. [Abstract] [Full Text] [PDF]

				M. Beraneck, S. Pfanzelt, I. Vassias, M. Rohregger, N. Vibert, P.-P. Vidal, L. E. Moore, and H. Straka Differential Intrinsic Response Dynamics Determine Synaptic Signal Processing in Frog Vestibular Neurons J. Neurosci., April 18, 2007; 27(16): 4283 - 4296. [Abstract] [Full Text] [PDF]

				J. R. Huxter, L. E. Zinyuk, E. v. L. Roloff, V. R. J. Clarke, N. P. Dolman, J. C. A. More, D. E. Jane, G. L. Collingridge, and R. U. Muller Inhibition of Kainate Receptors Reduces the Frequency of Hippocampal Theta Oscillations J. Neurosci., February 28, 2007; 27(9): 2212 - 2223. [Abstract] [Full Text] [PDF]

				H. Hu, K. Vervaeke, and J. F. Storm M-Channels (Kv7/KCNQ Channels) That Regulate Synaptic Integration, Excitability, and Spike Pattern of CA1 Pyramidal Cells Are Located in the Perisomatic Region J. Neurosci., February 21, 2007; 27(8): 1853 - 1867. [Abstract] [Full Text] [PDF]

				M. L. Bourdeau, F. Morin, C. E. Laurent, M. Azzi, and J.-C. Lacaille Kv4.3-Mediated A-Type K+ Currents Underlie Rhythmic Activity in Hippocampal Interneurons J. Neurosci., February 21, 2007; 27(8): 1942 - 1953. [Abstract] [Full Text] [PDF]

				M. A. Castro-Alamancos, P. Rigas, and Y. Tawara-Hirata Resonance (~10 Hz) of excitatory networks in motor cortex: effects of voltage-dependent ion channel blockers J. Physiol., January 1, 2007; 578(1): 173 - 191. [Abstract] [Full Text] [PDF]

				G. Orban, T. Kiss, and P. Erdi Intrinsic and Synaptic Mechanisms Determining the Timing of Neuron Population Activity During Hippocampal Theta Oscillation J Neurophysiol, December 1, 2006; 96(6): 2889 - 2904. [Abstract] [Full Text] [PDF]

				J. J. Lawrence, F. Saraga, J. F. Churchill, J. M. Statland, K. E. Travis, F. K. Skinner, and C. J. McBain Somatodendritic Kv7/KCNQ/M Channels Control Interspike Interval in Hippocampal Interneurons. J. Neurosci., November 22, 2006; 26(47): 12325 - 12338. [Abstract] [Full Text] [PDF]

				K. Vervaeke, N. Gu, C. Agdestein, H. Hu, and J. F. Storm Kv7/KCNQ/M-channels in rat glutamatergic hippocampal axons and their role in regulation of excitability and transmitter release J. Physiol., October 1, 2006; 576(1): 235 - 256. [Abstract] [Full Text] [PDF]

				I. Oren, E. O. Mann, O. Paulsen, and N. Hajos Synaptic Currents in Anatomically Identified CA3 Neurons during Hippocampal Gamma Oscillations In Vitro J. Neurosci., September 27, 2006; 26(39): 9923 - 9934. [Abstract] [Full Text] [PDF]

				Y. Aponte, C.-C. Lien, E. Reisinger, and P. Jonas Hyperpolarization-activated cation channels in fast-spiking interneurons of rat hippocampus J. Physiol., July 1, 2006; 574(1): 229 - 243. [Abstract] [Full Text] [PDF]

				H. J. Chung, Y. N. Jan, and L. Y. Jan Polarized axonal surface expression of neuronal KCNQ channels is mediated by multiple signals in the KCNQ2 and KCNQ3 C-terminal domains PNAS, June 6, 2006; 103(23): 8870 - 8875. [Abstract] [Full Text] [PDF]

				P. Aracri, E. Colombo, M. Mantegazza, P. Scalmani, G. Curia, G. Avanzini, and S. Franceschetti Layer-Specific Properties of the Persistent Sodium Current in Sensorimotor Cortex J Neurophysiol, June 1, 2006; 95(6): 3460 - 3468. [Abstract] [Full Text] [PDF]

				C. Yue and Y. Yaari Axo-Somatic and Apical Dendritic Kv7/M Channels Differentially Regulate the Intrinsic Excitability of Adult Rat CA1 Pyramidal Cells J Neurophysiol, June 1, 2006; 95(6): 3480 - 3495. [Abstract] [Full Text] [PDF]

				S. Piccinin, A. D. Randall, and J. T. Brown KCNQ/Kv7 Channel Regulation of Hippocampal Gamma-Frequency Firing in the Absence of Synaptic Transmission J Neurophysiol, May 1, 2006; 95(5): 3105 - 3112. [Abstract] [Full Text] [PDF]

				J. A. Rosenkranz and D. Johnston Dopaminergic regulation of neuronal excitability through modulation of Ih in layer V entorhinal cortex. J. Neurosci., March 22, 2006; 26(12): 3229 - 3244. [Abstract] [Full Text] [PDF]

				N. S. Desai and E. C. Walcott Synaptic bombardment modulates muscarinic effects in forelimb motor cortex. J. Neurosci., February 22, 2006; 26(8): 2215 - 2226. [Abstract] [Full Text] [PDF]

				J. J. Lawrence, J. M. Statland, Z. M. Grinspan, and C. J. McBain Cell type-specific dependence of muscarinic signalling in mouse hippocampal stratum oriens interneurones J. Physiol., February 1, 2006; 570(3): 595 - 610. [Abstract] [Full Text] [PDF]

				E. W Newell and L. C Schlichter Integration of K+ and Cl- currents regulate steady-state and dynamic membrane potentials in cultured rat microglia J. Physiol., September 15, 2005; 567(3): 869 - 890. [Abstract] [Full Text] [PDF]

				W. Shen, S. E. Hamilton, N. M. Nathanson, and D. J. Surmeier Cholinergic Suppression of KCNQ Channel Currents Enhances Excitability of Striatal Medium Spiny Neurons J. Neurosci., August 10, 2005; 25(32): 7449 - 7458. [Abstract] [Full Text] [PDF]

				N. Gu, K. Vervaeke, H. Hu, and J. F Storm Kv7/KCNQ/M and HCN/h, but not KCa2/SK channels, contribute to the somatic medium after-hyperpolarization and excitability control in CA1 hippocampal pyramidal cells J. Physiol., August 1, 2005; 566(3): 689 - 715. [Abstract] [Full Text] [PDF]

				N. Wu, A. Enomoto, S. Tanaka, C.-F. Hsiao, D. Q. Nykamp, E. Izhikevich, and S. H. Chandler Persistent Sodium Currents in Mesencephalic V Neurons Participate in Burst Generation and Control of Membrane Excitability J Neurophysiol, May 1, 2005; 93(5): 2710 - 2722. [Abstract] [Full Text] [PDF]

				C. Chen and N. G. Bazan Endogenous PGE2 Regulates Membrane Excitability and Synaptic Transmission in Hippocampal CA1 Pyramidal Neurons J Neurophysiol, February 1, 2005; 93(2): 929 - 941. [Abstract] [Full Text] [PDF]

				D. V Vasilyev and M. E Barish Regulation of the hyperpolarization-activated cationic current Ih in mouse hippocampal pyramidal neurones by vitronectin, a component of extracellular matrix J. Physiol., November 1, 2004; 560(3): 659 - 675. [Abstract] [Full Text] [PDF]

				I Erchova, G Kreck, U Heinemann, and A. V. M Herz Dynamics of rat entorhinal cortex layer II and III cells: characteristics of membrane potential resonance at rest predict oscillation properties near threshold J. Physiol., October 1, 2004; 560(1): 89 - 110. [Abstract] [Full Text] [PDF]

				S. Schreiber, I. Erchova, U. Heinemann, and A. V. M. Herz Subthreshold Resonance Explains the Frequency-Dependent Integration of Periodic as Well as Random Stimuli in the Entorhinal Cortex J Neurophysiol, July 1, 2004; 92(1): 408 - 415. [Abstract] [Full Text] [PDF]

				C. Yue and Y. Yaari KCNQ/M Channels Control Spike Afterdepolarization and Burst Generation in Hippocampal Neurons J. Neurosci., May 12, 2004; 24(19): 4614 - 4624. [Abstract] [Full Text] [PDF]

				Q.-T. Nguyen, R. Wessel, and D. Kleinfeld Developmental regulation of active and passive membrane properties in rat vibrissa motoneurones J. Physiol., April 1, 2004; 556(1): 203 - 219. [Abstract] [Full Text] [PDF]

				P. Schweitzer, S. G. Madamba, and G. R. Siggins The Sleep-Modulating Peptide Cortistatin Augments the h-Current in Hippocampal Neurons J. Neurosci., November 26, 2003; 23(34): 10884 - 10891. [Abstract] [Full Text] [PDF]

				D. L. Prole, P. A. Lima, and N. V. Marrion Mechanisms Underlying Modulation of Neuronal KCNQ2/KCNQ3 Potassium Channels by Extracellular Protons J. Gen. Physiol., November 24, 2003; 122(6): 775 - 793. [Abstract] [Full Text] [PDF]