Differential effects on fast and slow spindle activity, and the sleep slow oscillation in humans with carbamazepine and flunarizine to antagonize voltage-dependent Na+ and Ca2+ channel activity

Sleep

Volumn 36, Issue 6, 2013, Pages 905-911

  Ayoub, Amr ^a,b   Aumann, Dominic ^a   Hörschelmann, Anne ^a   Kouchekmanesch, Atossa ^a   Paul, Pia ^a   Born, Jan ^a,b   Marshall, Lisa ^a  

^a UNIVERSITY OF LÜBECK   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

EEG; Ion channels; Sleep spindles; Slow oscillations; Theta

Indexed keywords

CARBAMAZEPINE; FLUNARIZINE; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED SODIUM CHANNEL;

ADULT; ARTICLE; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; FEMALE; FRONTAL CORTEX; HUMAN; HUMAN EXPERIMENT; MALE; NONREM SLEEP; NORMAL HUMAN; PARIETAL CORTEX; PRIORITY JOURNAL; SLEEP; SLEEP SLOW OSCILLATION; SLEEP SPINDLE;

EEG; ION CHANNELS; SLEEP SPINDLES; SLOW OSCILLATIONS; THETA;

ADULT; BRAIN; CALCIUM CHANNEL BLOCKERS; CALCIUM CHANNELS; CARBAMAZEPINE; CROSS-OVER STUDIES; DOUBLE-BLIND METHOD; ELECTROENCEPHALOGRAPHY; FEMALE; FLUNARIZINE; HUMANS; MALE; SLEEP STAGES; SODIUM CHANNEL BLOCKERS; SODIUM CHANNELS;

EID: 84878424737     PISSN: 01618105     EISSN: 15509109     Source Type: Journal    
DOI: 10.5665/sleep.2722     Document Type: Article

References (62)

1. Timofeev I, Grenier F, Bazhenov M, Houweling AR, Sejnowski TJ, Steriade M. Short- and medium-term plasticity associated with augmenting responses in cortical slabs and spindles in intact cortex of cats in vivo. J Physiol 2002;542:583-98. (Pubitemid 35190317)
2. Schabus M, Gruber G, Parapatics S, et al. Sleep spindles and their significance for declarative memory consolidation. Sleep 2004;27:1479-85. (Pubitemid 40041615)
3. Fogel SM, Smith CT. Learning-dependent changes in sleep spindles and Stage 2 sleep. J Sleep Res 2006;15:250-5. (Pubitemid 44215541)
4. Diekelmann S, Born J. The memory function of sleep. Nat Rev Neurosci 2010;11:114-26.
5. Gibbs FA, Gibbs EL. Atlas of Electroencephalography. Cambridge: Addison-Wesley Press, 1950.
6. Caderas M, Niedermeyer E, Uematsu S, Long DM, Nastalski J. Sleep spindles recorded from deep cerebral structures in man. Clin Electroencephalogr 1982;13:216-25. (Pubitemid 13255104)
7. Werth E, Achermann P, Dijk DJ, Borbely AA. Spindle frequency activity in the sleep EEG: individual differences and topographic distribution. Electroencephalogr Clin Neurophysiol 1997;103:535-42. (Pubitemid 27505346)
8. Knoblauch V, Krauchi K, Renz C, Wirz-Justice A, Cajochen C. Homeostatic control of slow-wave and spindle frequency activity during human sleep: effect of differential sleep pressure and brain topography. Cereb Cortex 2002;12:1092-100.
9. Mölle M, Marshall L, Gais S, Born J. Learning increases human electroencephalographic coherence during subsequent slow sleep oscillations. Proc Natl Acad Sci U S A 2004;101:13963-8. (Pubitemid 39298515)
10. Mölle M, Bergmann TO, Marshall L, Born J. Fast and slow spindles during the sleep slow oscillation: disparate coalescence and engagement in memory processing. Sleep 2011;34:1411-21.
11. Terrier G, Gottesmann CL. Study of cortical spindles during sleep in the rat. Brain Res Bull 1978;3:701-6. (Pubitemid 9065465)
12. Gandolfo G, Glin L, Gottesmann C. Study of sleep spindles in the rat: a new improvement. Acta Neurobiol Exp (Wars) 1985;45:151-62. (Pubitemid 16176226)
13. De Gennaro L, Ferrara M. Sleep spindles: an overview. Sleep Med Rev 2003;7:423-40. (Pubitemid 37221986)
14. Contreras D, Destexhe A, Sejnowski TJ, Steriade M. Control of spatio-temporal coherence of a thalamic oscillation by corticothalamic feedback. Science 1996;274:771-4. (Pubitemid 26398254)
15. Steriade M. Grouping of brain rhythms in corticothalamic systems. Neuroscience 2006;137:1087-106. (Pubitemid 43133136)
16. Anderer P, Klosch G, Gruber G, et al. Low-resolution brain electromagnetic tomography revealed simultaneously active frontal and parietal sleep spindle sources in the human cortex. Neuroscience 2001;103:581-92. (Pubitemid 32239328)
17. Doran MS. The dynamic topography of individual sleep spindles. Sleep Research Online 2003;5:133-9.
18. Schabus M, ng-Vu TT, Albouy G, et al. Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proc Natl Acad Sci U S A 2007;104:13164-9.
19. Bonjean M, Baker T, Lemieux M, Timofeev I, Sejnowski T, Bazhenov M. Corticothalamic feedback controls sleep spindle duration in vivo. J Neurosci 2011;31:9124-34.
20. Dehghani N, Cash SS, Halgren E. Topographical frequency dynamics within EEG and MEG sleep spindles. Clin Neurophysiol 2011;122:229-35.
21. Marshall L, Born J. The contribution of sleep to hippocampus-dependent memory consolidation. Trends Cogn Sci 2007;11:442-50. (Pubitemid 47588990)
22. Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ. Model of thalamocortical slow-wave sleep oscillations and transitions to activated States. J Neurosci 2002;22:8691-704. (Pubitemid 35387610)
23. Steriade M, Timofeev I. Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron 2003;37:563-76. (Pubitemid 36262979)
24. Destexhe A, Hughes SW, Rudolph M, Crunelli V. Are corticothalamic 'up' states fragments of wakefulness? Trends Neurosci 2007;30:334-42. (Pubitemid 46991116)
25. Crunelli V, Hughes SW. The slow (< 1 Hz) rhythm of non-REM sleep: a dialogue between three cardinal oscillators. Nat Neurosci 2010;13:9-17.
26. Kuo CC, Chen RS, Lu L, Chen RC. Carbamazepine inhibition of neuronal Na+ currents: quantitative distinction from phenytoin and possible therapeutic implications. Mol Pharmacol 1997;51:1077-83. (Pubitemid 27249142)
27. Landmark CJ. Targets for antiepileptic drugs in the synapse. Med Sci Monit 2007;13:RA1-7. (Pubitemid 46045538)
28. Sun GC, Werkman TR, Battefeld A, Clare JJ, Wadman WJ. Carbamazepine and topiramate modulation of transient and persistent sodium currents studied in HEK293 cells expressing the Na(v)1.3 alpha-subunit. Epilepsia 2007;48:774-82. (Pubitemid 46587602)
29. Porter RJ, Dhir A, Macdonald RL, Rogawski MA. Mechanisms of action of antiseizure drugs. In: Stefan H, Theodore W H, eds. Handbook of clinical neurology, 108. Epilepsy Part II: Treatment. Elsevier Science and Technology, 2012; in press.
30. Peters T, Wilffert B, Vanhoutte PM, van Zwieten PA. Calcium channels in the brain as targets for the calcium-channel modulators used in the treatment of neurological disorders. J Cardiovasc Pharmacol 1991;18:S1-5.
31. Golumbek PT, Rho JM, Spain WJ, van Brederode JF. Effects of flunarizine on spontaneous synaptic currents in rat neocortex. Naunyn Schmiedebergs Arch Pharmacol 2004;370:176-82. (Pubitemid 39361853)
32. Ye Q, Yan LY, Xue LJ, et al. Flunarizine blocks voltage-gated Na(+) and Ca(2+) currents in cultured rat cortical neurons: A possible locus of action in the prevention of migraine. Neurosci Lett 2011;487:394-9.
33. Géradin AP, Abadie FV, Campestrini JA, Theobald W. Pharmacokinetics of carbamazepine in normal humans after single and repeated oral doses. J Pharmacokinet Biopharm 1976;4:521-35. (Pubitemid 8132216)
34. Pynnönen S. Pharmacokinetics of carbamazepine in man: a review. Ther Drug Monit 1979;1:409-31. (Pubitemid 10097086)
35. Holmes B, Brogden RN, Heel RC, Speight TM, Avery GS. Flunarizine. A review of its pharmacodynamic and pharmacokinetic properties and therapeutic use. Drugs 1984;27:6-44. (Pubitemid 14209392)
36. Ziemann U, Lonnecker S, Steinhoff BJ, Paulus W. Effects of antiepileptic drugs on motor cortex excitability in humans: a transcranial magnetic stimulation study. Ann Neurol 1996;40:367-78. (Pubitemid 26304794)
37. Nitsche MA, Fricke K, Henschke U, et al. Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J Physiol 2003;553:293-301. (Pubitemid 37483935)
38. Rechtschaffen A, Kales A. A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects. Washington: NIH Publ. 204, US Government Printing Office, 1968.
39. Mölle M, Marshall L, Gais S, Born J. Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep. J Neurosci 2002;22:10941-7. (Pubitemid 36005170)
40. Timofeev I, Grenier F, Steriade M. Impact of intrinsic properties and synaptic factors on the activity of neocortical networks in vivo. J Physiol Paris 2000;94:343-55. (Pubitemid 32110919)
41. Macdonald RL, Kelly KM. Antiepileptic drug mechanisms of action. Epilepsia 1993;34:S1-8. (Pubitemid 23249438)
42. Dreixler JC, Bian J, Cao Y, Roberts MT, Roizen JD, Houamed KM. Block of rat brain recombinant SK channels by tricyclic antidepressants and related compounds. Eur J Pharmacol 2000;401:1-7. (Pubitemid 30479805)
43. Ambrosio AF, Soares-Da-Silva P, Carvalho CM, Carvalho AP. Mechanisms of action of carbamazepine and its derivatives, oxcarbazepine, BIA 2-093, and BIA 2-024. Neurochem Res 2002;27:121-30. (Pubitemid 34242438)
44. Compte A, Sanchez-Vives MV, McCormick DA, Wang XJ. Cellular and network mechanisms of slow oscillatory activity (< 1 Hz) and wave propagations in a cortical network model. J Neurophysiol 2003;89:2707-25. (Pubitemid 36570233)
45. Sanchez-Vives MV, Mattia M, Compte A, et al. Inhibitory modulation of cortical up states. J Neurophysiol 2010;104:1314-24.
46. Jokeit H, Okujava M, Woermann FG. Carbamazepine reduces memory induced activation of mesial temporal lobe structures: a pharmacological fMRI-study. BMC Neurol 2001;1:6.
47. Bernardi RB, Barros HM. Carbamazepine enhances discriminative memory in a rat model of epilepsy. Epilepsia 2004;45:1443-7. (Pubitemid 39470048)
48. Li Q, Jin CL, Xu LS, et al. Histidine enhances carbamazepine action against seizures and improves spatial memory deficits induced by chronic transauricular kindling in rats. Acta Pharmacol Sin 2005;26:1297-302. (Pubitemid 41607000)
49. Esser SK, Hill SL, Tononi G. Sleep homeostasis and cortical synchronization: I. Modeling the effects of synaptic strength on sleep slow waves. Sleep 2007;30:1617-30. (Pubitemid 350234741)
50. Steriade M, McCormick DA, Sejnowski TJ. Thalamocortical oscillations in the sleeping and aroused brain. Science 1993;262:679-85. (Pubitemid 23350685)
51. McCormick DA, Bal T. Sleep and arousal: thalamocortical mechanisms. Annu Rev Neurosci 1997;20:185-215. (Pubitemid 27106380)
52. Steriade M, McCarley RW. Brain control of wakefulness and sleep. New York: Plenum Publishers, 2005.
53. Contreras D, Destexhe A, Sejnowski TJ, Steriade M. Spatiotemporal patterns of spindle oscillations in cortex and thalamus. J Neurosci 1997;17:1179-96. (Pubitemid 27043974)
54. Destexhe A, Contreras D, Steriade M. Mechanisms underlying the synchronizing action of corticothalamic feedback through inhibition of thalamic relay cells. J Neurophysiol 1998;79:999-1016. (Pubitemid 28095914)
55. Huguenard JR, McCormick DA. Thalamic synchrony and dynamic regulation of global forebrain oscillations. Trends Neurosci 2007;30:350-6. (Pubitemid 46991122)
56. Crunelli V, Cope DW, Hughes SW. Thalamic T-type Ca2+ channels and NREM sleep. Cell Calcium 2006;40:175-90. (Pubitemid 43942299)
57. Blethyn KL, Hughes SW, Toth TI, Cope DW, Crunelli V. Neuronal basis of the slow (< 1 Hz) oscillation in neurons of the nucleus reticularis thalami in vitro. J Neurosci 2006;26:2474-86. (Pubitemid 44699008)
58. Lee J, Kim D, Shin HS. Lack of delta waves and sleep disturbances during non-rapid eye movement sleep in mice lacking alpha1G-subunit of T-type calcium channels. Proc Natl Acad Sci U S A 2004;101:18195-9. (Pubitemid 40054096)
59. Astori S, Wimmer RD, Prosser HM, et al. The CaV3.3 calcium channel is the major sleep spindle pacemaker in thalamus. Proc Natl Acad Sci U S A 2011;108:13823-8.
60. Hughes SW, Lorincz M, Cope DW, et al. Synchronized oscillations at alpha and theta frequencies in the lateral geniculate nucleus. Neuron 2004;42:253-68. (Pubitemid 38501648)
61. Zakir Hossain SM, Shinohara H, Kitano H. Drug assessment based on detection of L-glutamate released from C6 glioma cells using an enzyme-luminescence method. Anal Chem 2008;80:3762-8. (Pubitemid 351705879)
62. Ferrari A, Spaccapelo L, Pinetti D, Tacchi R, Bertolini A. Effective prophylactic treatments of migraine lower plasma glutamate levels. Cephalalgia 2009;29:423-9.