Reciprocal modulation of Ih and ITASK in thalamocortical relay neurons by halothane

Pflugers Archiv European Journal of Physiology

Volumn 456, Issue 6, 2008, Pages 1061-1073

  Budde, Thomas ^a   Coulon, Philippe ^a   Pawlowski, Matthias ^a   Meuth, Patrick ^a   Kanyshkova, Tatyana ^a   Japes, Ansgar ^a   Meuth, Sven G ^b   Pape, Hans Christian ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Anesthetic; Halothane; HCN; TASK; TC neurons

Indexed keywords

HALOTHANE; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL PROTEIN HCN1; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL PROTEIN HCN2; HYPERPOLARIZATION ACTIVATED CYCLIC NUCLEOTIDE GATED CHANNEL PROTEIN HCN4; ION CHANNEL; POTASSIUM CHANNEL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CELL MEMBRANE CONDUCTANCE; CELL MEMBRANE POTENTIAL; CELL POLARITY; COMPUTER MODEL; COMPUTER SIMULATION; CONTROLLED STUDY; DRUG MECHANISM; ELECTROPHYSIOLOGY; HYPERPOLARIZATION; IMMUNOHISTOCHEMISTRY; LATERAL GENICULATE BODY; NONHUMAN; PATCH CLAMP; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; RAT; THALAMOCORTICAL TRACT;

ANESTHETICS, INHALATION; ANIMALS; CEREBRAL CORTEX; COMPUTER SIMULATION; CYCLIC NUCLEOTIDE-GATED CATION CHANNELS; ELECTROPHYSIOLOGY; EXTRACELLULAR SPACE; HALOTHANE; IMMUNOHISTOCHEMISTRY; NEURAL NETWORKS (COMPUTER); NEURAL PATHWAYS; NEURONS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNELS; POTASSIUM CHANNELS, TANDEM PORE DOMAIN; RATS; RATS, LONG-EVANS; THALAMUS;

EID: 50049092351     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-008-0482-9     Document Type: Article

References (58)

1. C Altomare B Terragni C Brioschi R Milanesi C Pagliuca C Viscomi A Moroni M Baruscotti D DiFrancesco 2003 Heteromeric HCN1-HCN4 channels: a comparison with native pacemaker channels from the rabbit sinoatrial node J Physiol (Lond) 549 347 359
2. R Basheer RE Strecker MM Thakkar RW McCarley 2004 Adenosine and sleep-wake regulation Prog Neurobiol 73 379 396
3. 2+ of the hyperpolarization-activated cation current in rat thalamic neurons J Physiol (Lond) 503.1 79 85
4. T Budde L Caputi T Kanyshkova R Staak C Abrahamczik T Munsch HC Pape 2005 Impaired regulation of thalamic pacemaker channels through an imbalance of subunit expression in absence epilepsy J Neurosci 25 9871 9882
5. JA Campagna KW Miller SA Forman 2003 Mechanisms of actions of inhaled anesthetics N Engl J Med 348 2110 2124
6. X Chen JE Sirois Q Lei EM Talley C Lynch III DA Bayliss 2005 HCN subunit-specific and cAMP-modulated effects of anesthetics on neuronal pacemaker currents J Neurosci 25 5803 5814
7. M Day DB Carr S Ulrich E Ilijic T Tkatch DJ Surmeier 2005 Dendritic excitability of mouse frontal cortex pyramidal neurons is shaped by the interaction among HCN, Kir2, and Kleak channels J Neurosci 25 8776 8787
8. O Detsch E Kochs M Siemers B Bromm C Vahle-Hinz 2002 Differential effects of isoflurane on excitatory and inhibitory synaptic inputs to thalamic neurones in vivo Br J Anaesth 89 294 300
9. JP Dilger AM Vidal AI Mody Y Liu 1994 Evidence for direct actions of general anesthetics on an ion channel protein. A new look at a unified mechanism of action Anesthesiology 81 431 442
10. EE Fanselow K Sameshima LA Baccala MA Nicolelis 2001 Thalamic bursting in rats during different awake behavioral states Proc Natl Acad Sci U S A 98 15330 15335
11. NP Franks WR Lieb 1994 Molecular and cellular mechanisms of general anaethesia Nature 367 607 614
12. NP Franks WR Lieb 1998 Which molecular targets are most relevant to general anaesthesia? Toxicol Lett 100-101 1 8
13. C Heurteaux N Guy C Laigle N Blondeau F Duprat M Mazzuca L Lang-Lazdunski C Widmann M Zanzouri G Romey M Lazdunski 2004 TREK-1, a K(+) channel involved in neuroprotection and general anesthesia EMBO J 23 2684 2695
14. ML Hines NT Carnevale 2001 NEURON: a tool for neuroscientists Neuroscientist 7 123 135
15. E Honore 2007 The neuronal background K2P channels: focus on TREK1 Nat Rev Neurosci 8 251 261
16. JR Huguenard DA McCormick 1992 Simulation of the currents involved in rhythmic oscillations in thalamic relay neurons J Neurophysiol 68 1373 1383
17. MV Jones NL Harrison 1993 Effects of volatile anesthetics on the kinetics of inhibitory postsynaptic currents in cultured rat hippocampal neurons J Neurophysiol 70 1339 1349
18. A-M Linden MI Aller E Leppa O Vekovischeva T Aitta-aho EL Veale A Mathie P Rosenberg W Wisden ER Korpi 2006 The in vivo contributions of TASK-1-containing channels to the actions of inhalation anesthetics, the {alpha}2 adrenergic sedative dexmedetomidine, and cannabinoid agonists J Pharmacol Exp Ther 317 615 626
19. A-M Linden C Sandu MI Aller OY Vekovischeva PH Rosenberg W Wisden ER Korpi 2007 TASK-3 knockout mice exhibit exaggerated nocturnal activity, impairments in cognitive functions, and reduced sensitivity to inhalation anesthetics J Pharmacol Exp Ther 323 924 934
20. A Ludwig T Budde J Stieber S Moosmang C Wahl K Holthoff A Langebartels C Wotjak T Munsch X Zong S Feil R Feil M Lancel KR Chien A Konnerth HC Pape M Biel F Hofmann 2003 Absence epilepsy and sinus dysrhythmia in mice lacking the pacemaker channel HCN2 EMBO J 22 216 224
21. F Maingret AJ Patel F Lesage M Lazdunski E Honore 1999 Mechano- or acid stimulation, two interactive modes of activation of the TREK-1 potassium channel J Biol Chem 274 26691 26696
22. DA McCormick 1992 Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity Prog Neurobiol 39 337 388
23. DA McCormick JR Huguenard 1992 A model of the electrophysiological properties of thalamocortical relay neurons J Neurophysiol 68 1384 1400
24. DA McCormick H-C Pape 1990 Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones J Physiol (Lond) 431 291 318
25. P Meuth SG Meuth D Jacobi T Broicher HC Pape T Budde 2005 Get the rhythm: modeling of neuronal activity Journal of Undergraduate Neuroscience Education 4 1 A1 A11
26. SG Meuth MI Aller T Munsch T Schuhmacher T Seidenbecher C Kleinschnitz HC Pape H Wiendl W Wisden T Budde 2006 The contribution of TASK-1-containing channels to the function of dorsal lateral geniculate thalamocortical relay neurons Mol Pharmacol 69 1468 1476
27. + channel 1 (TASK1) and TASK3 channels to the control of activity modes in thalamocortical neurons J Neurosci 23 6460 6469
28. SG Meuth T Kanyshkova P Meuth P Landgraf T Munsch A Ludwig F Hofmann HC Pape T Budde 2006 The membrane resting potential of thalamocortical relay neurons is shaped by the interaction among TASK3 and HCN2 channels J Neurophysiol 96 1517 1529
29. SJ Mihic Q Ye MJ Wick VV Koltchine MD Krasowski SE Finn MP Mascia CF Valenzuela KK Hanson EP Greenblatt RA Harris NL Harrison 1997 Sites of alcohol and volatile anaesthetic action on GABAA and glycine receptors Nature 389 385 389
30. AA Mikulec S Pittson SM Amagasu FA Monroe MB MacIver 1998 Halothane depresses action potential conduction in hippocampal axons Brain Res 796 231 238
31. LM Monteggia AJ Eisch MD Tang LK Kaczmarek EJ Nestler 2000 Cloning and localization of the hyperpolarization-activated cyclic nucleotide-gated channel family in rat brain Brain Res Mol Brain Res 81 129 139
32. B Much C Wahl-Schott X Zong A Schneider L Baumann S Moosmang A Ludwig M Biel 2003 Role of subunit heteromerization and N-linked glycosylation in the formation of functional hyperpolarization-activated cyclic nucleotide-gated channels J Biol Chem 278 43781 43786
33. LE Nelson TZ Guo J Lu CB Saper NP Franks M Maze 2002 The sedative component of anesthesia is mediated by GABAA receptors in an endogenous sleep pathway Nat Neurosci 5 979 984
34. H-C Pape 1992 Adenosine promotes burst activity in guinea-pig geniculocortical neurones through two different ionic mechanisms J Physiol (Lond) 447 729 753
35. H-C Pape 1996 Queer current and pacemaker: the hyperpolarization- activated cation current in neurons Annu Rev Physiol 58 299 327
36. h, in absence epilepsy. Thalamus & Related Systems DOI 10.1017/S1472928807000180
37. + channels: role in apoptosis and tumorigenesis Pflugers Arch 448 261 273
38. + channels Nat Neurosci 2 422 426
39. RA Pearce 1996 Volatile anaesthetic enhancement of paired-pulse depression investigated in the rat hippocampus in vitro J Physiol (Lond) 492 823 840
40. T Porkka-Heiskanen L Alanko A Kalinchuk D Stenberg 2002 Adenosine and sleep Sleep Med Rev 6 321 332
41. + channels J Biol Chem 276 7302 7311
42. CR Ries E Puil 1999 Mechanism of anesthesia revealed by shunting actions of isoflurane on thalamocortical neurons J Neurophysiol 81 1795 1801
43. CR Ries E Puil 1999 Ionic mechanism of isoflurane's actions on thalamocortical neurons J Neurophysiol 81 1802 1809
44. R Seifert A Scholten R Gauss A Mincheva P Lichter UB Kaupp 1999 Molecular characterization of a slowly gating human hyperpolarization-activated channel predominantly expressed in thalamus, heart, and testis Proc Natl Acad Sci U S A 96 9391 9396
45. SM Sherman RW Guillery 1996 Functional organization of thalamocortical relays J Neurophysiol 76 1367 1395
46. Sherman SM, Guillery RW (2001) Exploring the thalamus. Academic Press, San Diego
47. + channel is a molecular substrate for neuronal effects of inhalation anesthetics J Neurosci 20 6347 6354
48. h by an inhalational anaesthetic and neurotransmitters in rat brainstem motoneurones J Physiol (Lond) 541 717 729
49. M Steriade 1997 Synchronized activities of coupled oscillators in the cerebral cortex and thalamus at different levels of vigilance Cereb Cortex 7 583 604
50. Steriade M, Jones EG, McCormick DA (1997) Thalamus. Elsevier, Amsterdam
51. K Sugiyama T Muteki K Shimoji 1992 Halothane-induced hyperpolarization and depression of postsynaptic potentials of guinea pig thalamic neurons in vitro Brain Res 576 97 103
52. EM Talley DA Bayliss 2002 Modulation of TASK-1 (Kcnk3) and TASK-3 (Kcnk9) potassium channels. Volatile anesthetics and neurotransmitters share a molecular site of action J Biol Chem 277 17733 17742
53. EM Talley G Solorzano Q Lei D Kim DA Bayliss 2001 CNS distribution of members of the two-pore-domain (KCNK) potassium channel family J Neurosci 21 7491 7505
54. L Triner Y Vulliemoz S-Y Woo M Verosky 1980 Halothane effect on cAMP generation and hydrolysis in rat brain Eur J Pharmacol 66 73 80
55. JR Trudell E Bertaccini 2002 Molecular modelling of specific and non-specific anaesthetic interactions Br J Anaesth 89 32 40
56. A Tung WB Mendelson 2004 Anesthesia and sleep Sleep Med Rev 8 213 225
57. C Vahle-Hinz O Detsch M Siemers E Kochs 2007 Contributions of GABAergic and glutamatergic mechanisms to isoflurane-induced suppression of thalamic somatosensory information transfer Exp Brain Res 176 159 172
58. TG Weyand M Boudreaux W Guido 2001 Burst and tonic response modes in thalamic neurons during sleep and wakefulness J Neurophysiol 85 1107 1118