An unexpected role for TASK-3 potassium channels in network oscillations with implications for sleep mechanisms and anesthetic action

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 41, 2009, Pages 17546-17551

  Pang, Daniel S J ^a   Robledo, Christian J ^a   Carr, David R ^a   Gent, Thomas C ^a   Vyssotski, Alexei L ^b   Caley, Alex ^a,c   Zecharia, Anna Y ^a   Wisden, William ^a   Brickley, Stephen G ^a   Franks, Nicholas P ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

EEG; Knockout; REM; Theta; Wavelet

Indexed keywords

CYCLOPROPANE; HALOTHANE; POTASSIUM CHANNEL; TASK 3 POTASSIUM CHANNEL; UNCLASSIFIED DRUG;

ANESTHESIA; ANESTHESIA MECHANISM; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EXPLORATORY BEHAVIOR; KNOCKOUT MOUSE; MOTOR ACTIVITY; MOUSE; NEUROBIOLOGY; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; REM SLEEP; RIGHTING REFLEX; SENSORY STIMULATION; SLEEP; SLEEP PATTERN; THETA RHYTHM; WALKING;

ANIMALS; CIRCADIAN RHYTHM; ELECTROENCEPHALOGRAPHY; ELECTROMYOGRAPHY; GENOTYPE; MICE; MICE, KNOCKOUT; OSCILLOMETRY; POTASSIUM CHANNELS, TANDEM PORE DOMAIN; SLEEP; WAKEFULNESS;

ANIMALIA; MUS;

EID: 70350443586     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0907228106     Document Type: Article

References (51)

1. Buzsaki G (2002) Theta oscillations in the hippocampus. Neuron 33:325-340.
2. Oddie SD, Kirk IJ, Whishaw IQ, Bland BH (1997) Hippocampal formation is involved in movement selection: Evidence from medial septal cholinergic modulation and concurrent slow-wave (theta rhythm) recording. Behav Brain Res 88:169-180.
3. Vanderwolf CH (1969) Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26:407-418.
4. Kramis R, Vanderwolf CH, Bland BH (1975) Two types of hippocampal rhythmical slow activity in both the rabbit and the rat: Relations to behavior and effects of atropine, diethyl ether, urethane, and pentobarbital. Exp Neurol 49:58-85.
5. Oddie SD, Bland BH (1998) Hippocampal formation theta activity and movement selection. Neurosci Biobehav Rev 22:221-231.
6. Colom LV, et al. (1991) In vivo intrahippocampal microinfusion of carbachol and bicuculline induces theta-like oscillations in the septally deafferented hippocampus. Hippocampus 1:381-390.
7. Kirk IJ (1998) Frequency modulation of hippocampal theta by the supramammillary nucleus, and other hypothalamo-hippocampal interactions: Mechanisms and functional implications. Neurosci Biobehav Rev 22:291-302.
8. Kirk IJ, McNaughton N (1993) Mapping the differential effects of procaine on frequency and amplitude of reticularly elicited hippocampal rhythmical slow activity. Hippocampus 3:517-525.
9. Vertes RP, Kocsis B (1997) Brainstem-diencephalo-septohippocampal systems controlling the theta rhythm of the hippocampus. Neuroscience 81:893-926. (Pubitemid 27421757)
10. Acker CD, Kopell N, White JA (2003) Synchronization of strongly coupled excitatory neurons: Relating network behavior to biophysics. J Comput Neurosci 15:71-90. (Pubitemid 36992478)
11. Rotstein HG, et al. (2005) Slow and fast inhibition and an H-current interact to create a theta rhythm in amodel of CA1 interneuron network. J Neurophysiol 94:1509-1518.
12. Traub RD, et al. (2004) Cellular mechanisms of neuronal population oscillations in the hippocampus in vitro. Annu Rev Neurosci 27:247-278.
13. Goldstein SA, Bockenhauer D, O'Kelly I, Zilberberg N (2001) Potassium leak channels and the KCNK family of two-P-domain subunits. Nat Rev Neurosci 2:175-184. (Pubitemid 33673370)
14. + channels. Nat Neurosci 2:422-426.
15. Talley EM, Bayliss DA (2002) Modulation of TASK-1 (Kcnk3) and TASK-3 (Kcnk9) potassium channels: Volatile anesthetics and neurotransmitters share amolecular site of action. J Biol Chem 277:17733-17742.
16. Franks NP (2008) General anaesthesia: From molecular targets to neuronal pathways of sleep and arousal. Nat Rev Neurosci 9:370-386.
17. Andres-Enguix I, et al. (2007) Determinants of the anesthetic sensitivity of two-pore domain acid-sensitive potassium channels: Molecular cloning of an anestheticactivated potassium channel from Lymnaea stagnalis. J Biol Chem 282:20977-20990. (Pubitemid 47099953)
18. + current. Nature 333:662-664.
19. + currents activated by volatile anaesthetics and FMRF-amide in molluscan neurones. Br J Pharmacol 125:309-318.
20. + channels are a novel target for the anesthetic gases xenon, nitrous oxide, and cyclopropane. Mol Pharmacol 65:443-452. (Pubitemid 38134273)
21. Mizumori SJ, Barnes CA, McNaughton BL (1989) Reversible inactivation of the medial septum: Selective effectsonthe spontaneous unit activity of different hippocampal cell types. Brain Res 500:99-106.
22. Oddie SD, Stefanek W, Kirk IJ, Bland BH (1996) Intraseptal procaine abolishes hypothalamic stimulation-induced wheel-running and hippocampal theta field activity in rats. J Neurosci 16:1948-1956. (Pubitemid 26145970)
23. Leung LS, Vanderwolf CH (1980) Behavior-dependent evoked potentials in the hippocampal CA1 region of the rat. II. Effect of eserine, atropine, ether and pentobarbital. Brain Res 198:119-133. (Pubitemid 10002678)
24. Bland BH, Colom LV (1988) Responses of phasic and tonic hippocampal theta-on cells to cholinergics: Differential effects of muscarinic and nicotinic activation. Brain Res 440:167-171.
25. Tebano MT, et al. (1999) Effects of cholinergic drugs on neocortical EEG and flash-visual evoked potentials in the mouse. Neuropsychobiology 40:47-56.
26. O'Keefe J (1993) Hippocampus, theta, and spatial memory. Curr Opin Neurobiol 3:917-924.
27. Jeewajee A, Barry C, O'Keefe J, Burgess N (2008) Grid cells and theta as oscillatory interference: Electrophysiological data from freely moving rats. Hippocampus 18:1175-1185.
28. Rivas J, Gaztelu JM, Garcia-Austt E (1996) Changes in hippocampal cell discharge patterns and theta rhythm spectral properties as a function of walking velocity in the guinea pig. Exp Brain Res 108:113-118. (Pubitemid 26076025)
29. Slawinska U, Kasicki S (1998) The frequency of rat's hippocampal theta rhythm is related to the speed of locomotion. Brain Res 796:327-331. (Pubitemid 28343268)
30. Gordon JA, Lacefield CO, Kentros CG, Hen R (2005) State-dependent alterations in hippocampal oscillations in serotonin 1A receptor-deficient mice. J Neurosci 25:6509-6519.
31. Daubechies I (1990) The wavelet transform, time-frequency localization and signal analysis. IEEE Trans Inf Theory 36:961-1005.
32. Linden AM, et al. (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.
33. + channel involved in neuroprotection and general anesthesia. EMBO J 23:2684-2695. (Pubitemid 38988239)
34. Nicoll RA, Madison DV (1982) General anesthetics hyperpolarize neurons in the vertebrate central nervous system. Science 217:1055-1057. (Pubitemid 12059106)
35. Hemmings HC, Jr, et al. (2005) Emerging molecular mechanisms of general anesthetic action. Trends Pharmacol Sci 26:503-510. (Pubitemid 41338560)
36. Rudolph U, Antkowiak B (2004) Molecular and neuronal substrates for general anaesthetics. Nat Rev Neurosci 5:709-720. (Pubitemid 39150142)
37. Bland BH, et al. (2003) Effect of halothane on type 2 immobility-related hippocampal theta field activity and theta-on/theta-off cell discharges. Hippocampus 13:38-47.
38. Aller MI, Wisden W (2008) Changes in expression of some two-pore domain potassium channel genes (KCNK) in selected brain regions of developing mice. Neuroscience 151:1154-1172.
39. Aller MI, et al. (2005) Modifying the subunit composition of TASK channels alters the modulation of a leak conductance in cerebellar granule neurons. J Neurosci 25:11455-11467.
40. Torborg CL, et al. (2006) TASK-like conductances are present within hippocampal CA1 stratum oriens interneuron subpopulations. J Neurosci 26:7362-7367.
41. Klausberger T, Somogyi P (2008) Neuronal diversity and temporal dynamics: The unity of hippocampal circuit operations. Science 321:53-57. (Pubitemid 351956237)
42. Wulff P, et al. (2009) Hippocampal theta rhythm and its coupling with gamma oscillations require fast inhibition onto parvalbumin-positive interneurons. Proc Natl Acad Sci USA 106:3561-3566.
43. Brickley SG, et al. (2007) TASK-3 two-pore domain potassium channels enable sustained high-frequency firing in cerebellar granule neurons. J Neurosci 27:9329-9340.
44. + channel 1 (TASK1) and TASK3 channels to the control of activity modes in thalamocortical neurons. J Neurosci 23:6460-6469.
45. Drucker-Colin R, et al. (1983) Dissociation of rapid eye movement (REM) sleep features: Possible implications for REM triggering mechanisms. J Neurosci Res 9:425-435.
46. Mavanji V, Datta S (2002) Sleep-wake effects of yohimbine and atropine in rats with a clomipramine-based model of depression. Neuroreport 13:1603-1606.
47. Waud DR (1972) On biological assays involving quantal responses. J Pharmacol Exp Ther 183:577-607.
48. Vyssotski A, et al. (2009) EEG responses to visual landmarks in flying pigeons. Curr Biol 19:1159-1166.
49. Torrence C, Compo G (1998) A practical guide to wavelet analysis. Bull Amer Meteor Soc 79:61-78.
50. Farge M (1992) Wavelet transforms and their applications to turbulence. Annu Rev Fluid Mech 24:395-457.
51. Costa-Miserachs D, Portell-Cortes I, Torras-Garcia M, Morgado-Bernal I (2003) Automated sleep staging in rat with a standard spreadsheet. J Neurosci Methods 130:93-101. (Pubitemid 37315933)