Reduced movement-related beta desynchronisation in juvenile myoclonic epilepsy: A MEG study of task specific cortical modulation

Clinical Neurophysiology

Volumn 122, Issue 11, 2011, Pages 2128-2138

  Hamandi, Khalid ^a   Singh, Krish D ^b   Muthukumaraswamy, Suresh ^b  

^a UNIVERSITY HOSPITAL OF WALES   (United Kingdom)

^b CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

Beamformer; JME; Juvenile myoclonic epilepsy; Magnetoencephalography; MEG

Indexed keywords

ADULT; ANALYSIS; ARTICLE; BETA RHYTHM; BODY MOVEMENT; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; JUVENILE MYOCLONIC EPILEPSY; MAGNETOENCEPHALOGRAPHY; MALE; MYOCLONUS EPILEPSY; NUCLEAR MAGNETIC RESONANCE IMAGING; OCCIPITAL CORTEX; OSCILLATION; PRIORITY JOURNAL; SENSORIMOTOR CORTEX; TIME FREQUENCY ANALYSIS; VISUAL ACUITY;

ADOLESCENT; ADULT; BETA RHYTHM; CEREBRAL CORTEX; CORTICAL SYNCHRONIZATION; FEMALE; HUMANS; MAGNETOENCEPHALOGRAPHY; MALE; MYOCLONIC EPILEPSY, JUVENILE; PSYCHOMOTOR PERFORMANCE; YOUNG ADULT;

EID: 80053192298     PISSN: 13882457     EISSN: 18728952     Source Type: Journal    
DOI: 10.1016/j.clinph.2011.04.017     Document Type: Article

References (87)

1. Akgun Y., Soysal A., Atakli D., Yuksel B., Dayan C., Arpaci B. Cortical excitability in juvenile myoclonic epileptic patients and their asymptomatic siblings: a transcranial magnetic stimulation study. Seizure 2009, 18(6):387-391.
2. Babiloni C., Carducci F., Cincotti F., Rossini P.M., Neuper C., Pfurtscheller G., et al. Human movement-related potentials vs desynchronization of EEG alpha rhythm: a high-resolution EEG study. NeuroImage 1999, 10(6):658-665.
3. Badawy R.A., Macdonell R.A., Jackson G.D., Berkovic S.F. Can changes in cortical excitability distinguish progressive from juvenile myoclonic epilepsy?. Epilepsia 2010, 51(10):2084-2088.
4. Baker S.N., Olivier E., Lemon R.N. Coherent oscillations in monkey motor cortex and hand muscle EMG show task-dependent modulation. J Physiol 1997, 501(1):225-241.
5. Ball T., Demandt E., Mutschler I., Neitzel E., Mehring C., Vogt K., et al. Movement related activity in the high gamma range of the human EEG. NeuroImage 2008, 41(2):302-310.
6. Barnes G.R., Hillebrand A. Statistical flattening of MEG beamformer images. Hum Brain Mapp 2003, 18(1):1-12.
7. Bergey G.K. Evidence-based treatment of idiopathic generalized epilepsies with new antiepileptic drugs. Epilepsia 2005, 46(Suppl. 9):161-168.
8. Betting L.E., Mory S.B., Li L.M., Lopes-Cendes I., Guerreiro M.M., Guerreiro C.A., et al. Voxel-based morphometry in patients with idiopathic generalized epilepsies. NeuroImage 2006, 32(2):498-502.
9. Bromley R.L., Mawer G., Love J., Kelly J., Purdy L., McEwan L., et al. Early cognitive development in children born to women with epilepsy: a prospective report. Epilepsia 2010, 51(10):2058-2065.
10. Buschman T.J., Miller E.K. Top-down versus bottom-up control of attention in the prefrontal and posterior parietal cortices. Science 2007, 315(5820):1860-1862.
11. Chau W., McIntosh A.R., Robinson S.E., Schulz M., Pantev C. Improving permutation test power for group analysis of spatially filtered MEG data. NeuroImage 2004, 23(3):983-996.
12. Chen R., Hallett M. The time course of changes in motor cortex excitability associated with voluntary movement. Can J Neurol Sci 1999, 26(3):163-169.
13. Cheyne D., Bells S., Ferrari P., Gaetz W., Bostan A.C. Self-paced movements induce high-frequency gamma oscillations in primary motor cortex. NeuroImage 2008, 42(1):332-342.
14. Clemens B. Valproate decreases EEG synchronization in a use-dependent manner in idiopathic generalized epilepsy. Seizure 2008, 17(3):224-233.
15. Cossette P., Liu L., Brisebois K., Dong H., Lortie A., Vanasse M., et al. Mutation of GABRA1 in an autosomal dominant form of juvenile myoclonic epilepsy. Nat Genet 2002, 31(2):184-189.
16. Crone N.E., Miglioretti D.L., Gordon B., Lesser R.P. Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. Brain 1998, 121(Pt 12):2301-2315.
17. Crone N.E., Miglioretti D.L., Gordon B., Sieracki J.M., Wilson M.T., Uematsu S., et al. Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. Brain 1998, 121(Pt 12):2271-2299.
18. Dalal S.S., Guggisberg A.G., Edwards E., Sekihara K., Findlay A.M., Canolty R.T., et al. Five-dimensional neuroimaging: localization of the time-frequency dynamics of cortical activity. NeuroImage 2008, 40(4):1686-1700.
19. Darvas F., Scherer R., Ojemann J.G., Rao R.P., Miller K.J., Sorensen L.B. High gamma mapping using EEG. NeuroImage 2010, 49(1):930-938.
20. Donoghue J.P., Sanes J.N., Hatsopoulos N.G., Gaal G. Neural discharge and local field potential oscillations in primate motor cortex during voluntary movements. J Neurophysiol. 1998, 79(1):159-173.
21. Engel A.K., Fries P. Beta-band oscillations--signalling the status quo?. Curr Opin Neurobiol 2010, 20(2):156-165.
22. Gaetz W., Macdonald M., Cheyne D., Snead O.C. Neuromagnetic imaging of movement-related cortical oscillations in children and adults: age predicts post-movement beta rebound. NeuroImage 2010, 51(2):792-807.
23. Gloor P. Generalized epilepsy with spike-and-wave discharge: a reinterpretation of its electrographic and clinical manifestations. The 1977 William G. Lennox Lecture, American Epilepsy Society. Epilepsia 1979, 20(5):571-588.
24. Groppa S., Siebner H.R., Kurth C., Stephani U., Siniatchkin M. Abnormal response of motor cortex to photic stimulation in idiopathic generalized epilepsy. Epilepsia 2008, 49(12):2022-2029.
25. Guerrini R., Parmeggiani L. Topiramate and its clinical applications in epilepsy. Expert Opin Pharmacother 2006, 7(6):811-823.
26. Hall S.D., Barnes G.R., Furlong P.L., Seri S., Hillebrand A. Neuronal network pharmacodynamics of GABAergic modulation in the human cortex determined using pharmaco-magnetoencephalography. Hum Brain Mapp 2010, 31(4):581-594.
27. Hall S.D., Stanford I.M., Yamawaki N., McAllister C.J., Ronnqvist K.C., Woodhall G.L., et al. The role of GABAergic modulation in motor function related neuronal network activity. NeuroImage 2011, 10.1016/j.neuroimage.2011.02.02.
28. Haug K., Warnstedt M., Alekov A.K., Sander T., Ramirez A., Poser B., et al. Mutations in CLCN2 encoding a voltage-gated chloride channel are associated with idiopathic generalized epilepsies. Nat Genet 2003, 33(4):527-532.
29. Hillebrand A., Singh K.D., Holliday I.E., Furlong P.L., Barnes G.R. A new approach to neuroimaging with magnetoencephalography. Hum Brain Mapp 2005, 25(2):199-211.
30. Holmes M.D., Quiring J., Tucker D.M. Evidence that juvenile myoclonic epilepsy is a disorder of frontotemporal corticothalamic networks. NeuroImage 2010, 49(1):80-93.
31. Huang M.X., Mosher J.C., Leahy R.M. A sensor-weighted overlapping-sphere head model and exhaustive head model comparison for MEG. Phys Med Biol 1999, 44(2):423-440.
32. Jenkinson M., Smith S. A global optimisation method for robust affine registration of brain images. Med Image Anal 2001, 5(2):143-156.
33. Jensen O., Goel P., Kopell N., Pohja M., Hari R., Ermentrout B. On the human sensorimotor-cortex beta rhythm: sources and modeling. NeuroImage 2005, 26(2):347-355.
34. Jentink J., Loane M.A., Dolk H., Barisic I., Garne E., Morris J.K., et al. Valproic acid monotherapy in pregnancy and major congenital malformations. N Engl J Med 2010, 362(23):2185-2193.
35. Jurkiewicz M.T., Gaetz W.C., Bostan A.C., Cheyne D. Post-movement beta rebound is generated in motor cortex: evidence from neuromagnetic recordings. NeuroImage 2006, 32(3):1281-1289.
36. Kaiser J., Birbaumer N., Lutzenberger W. Event-related beta desynchronization indicates timing of response selection in a delayed-response paradigm in humans. Neurosci Lett 2001, 312(3):149-152.
37. Kilner J.M., Baker S.N., Salenius S., Jousmaki V., Hari R., Lemon R.N. Task-dependent modulation of 15-30Hz coherence between rectified EMGs from human hand and forearm muscles. J Physiol 1999, 516(Pt 2):559-570.
38. Kim J.H., Lee J.K., Koh S.B., Lee S.A., Lee J.M., Kim S.I., et al. Regional grey matter abnormalities in juvenile myoclonic epilepsy: a voxel-based morphometry study. NeuroImage 2007, 37(4):1132-1137.
39. Kim S.Y., Hwang Y.H., Lee H.W., Suh C.K., Kwon S.H., Park S.P. Cognitive impairment in juvenile myoclonic epilepsy. J Clin Neurol 2007, 3(2):86-92.
40. Koelewijn L., Dumont J.R., Muthukumaraswamy S.D., Rich A.N., Singh K.D. Induced and evoked neural correlates of orientation selectivity in human visual cortex. NeuroImage 2011, 54(4):2983-2993.
41. Konishi T., Naganuma Y., Hongou K., Murakami M., Yamatani M., Okada T. Effects of antiepileptic drugs on EEG background activity in children with epilepsy: initial phase of therapy. Clin Electroencephalogr 1995, 26(2):113-119.
42. Krampfl K., Maljevic S., Cossette P., Ziegler E., Rouleau G.A., Lerche H., et al. Molecular analysis of the A322D mutation in the GABA receptor alpha-subunit causing juvenile myoclonic epilepsy. Eur J Neurosci 2005, 22(1):10-20.
43. Le Van Quyen M., Foucher J., Lachaux J., Rodriguez E., Lutz A., Martinerie J., et al. Comparison of Hilbert transform and wavelet methods for the analysis of neuronal synchrony. J Neurosci Methods 2001, 111(2):83-98.
44. Lefaucheur J.P. Myoclonus and transcranial magnetic stimulation. Neurophysiol Clin 2006, 36(5-6):293-297.
45. Lin K., Carrete H., Lin J., Peruchi M.M., de Araujo Filho G.M., Guaranha M.S., et al. Magnetic resonance spectroscopy reveals an epileptic network in juvenile myoclonic epilepsy. Epilepsia 2009, 50(5):1191-1200.
46. Llinas R., Ribary U. Consciousness and the brain. The thalamocortical dialogue in health and disease. Ann N Y Acad Sci 2001, 929:166-175.
47. Llinas R.R., Grace A.A., Yarom Y. In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50-Hz frequency range. Proc Natl Acad Sci USA 1991, 88(3):897-901.
48. Llinas R.R., Pare D. Of dreaming and wakefulness. Neuroscience 1991, 44(3):521-535.
49. Lynch B.A., Lambeng N., Nocka K., Kensel-Hammes P., Bajjalieh S.M., Matagne A., et al. The synaptic vesicle protein SV2A is the binding site for the antiepileptic drug levetiracetam. Proc Natl Acad Sci USA 2004, 101(26):9861-9866.
50. Ma S., Blair M.A., Abou-Khalil B., Lagrange A.H., Gurnett C.A., Hedera P. Mutations in the GABRA1 and EFHC1 genes are rare in familial juvenile myoclonic epilepsy. Epilepsy Res 2006, 71(2-3):129-134.
51. Macdonald R.L., Kang J.Q., Gallagher M.J. Mutations in GABAA receptor subunits associated with genetic epilepsies. J Physiol 2010, 588(Pt 11):1861-1869.
52. Macdonald R.L., Kelly K.M. Mechanisms of action of currently prescribed and newly developed antiepileptic drugs. Epilepsia 1994, 35(Suppl. 4):S41-S50.
53. Mecarelli O., Vicenzini E., Pulitano P., Vanacore N., Romolo F.S., Di Piero V., et al. Clinical, cognitive, and neurophysiologic correlates of short-term treatment with carbamazepine, oxcarbazepine, and levetiracetam in healthy volunteers. Ann Pharmacother 2004, 38(11):1816-1822.
54. Medina M.T., Suzuki T., Alonso M.E., Duron R.M., Martinez-Juarez I.E., Bailey J.N., et al. Novel mutations in Myoclonin1/EFHC1 in sporadic and familial juvenile myoclonic epilepsy. Neurology 2008, 70(22 Pt 2):2137-2144.
55. Miller K.J., Zanos S., Fetz E.E., den Nijs M., Ojemann J.G. Decoupling the cortical power spectrum reveals real-time representation of individual finger movements in humans. J Neurosci 2009, 29(10):3132-3137.
56. Murthy V.N., Fetz E.E. Coherent 25- to 35-Hz oscillations in the sensorimotor cortex of awake behaving monkeys. Proc Natl Acad Sci USA 1992, 89(12):5670-5674.
57. Muthukumaraswamy S.D. Functional properties of human primary motor cortex gamma oscillations. J Neurophysiol 2010, 104(5):2873-2885.
58. Muthukumaraswamy S.D., Edden R.A., Jones D.K., Swettenham J.B., Singh K.D. Resting GABA concentration predicts peak gamma frequency and fMRI amplitude in response to visual stimulation in humans. Proc Natl Acad Sci USA 2009, 106(20):8356-8361.
59. Muthukumaraswamy S.D., Johnson B.W. Changes in rolandic mu rhythm during observation of a precision grip. Psychophysiology 2004, 41(1):152-156.
60. Muthukumaraswamy S.D., Johnson B.W., Gaetz W.C., Cheyne D.O. Neural processing of observed oro-facial movements reflects multiple action encoding strategies in the human brain. Brain Res 2006, 1071(1):105-112.
61. Muthukumaraswamy S.D., Singh K.D., Swettenham J.B., Jones D.K. Visual gamma oscillations and evoked responses: Variability, repeatability and structural MRI correlates. Neuroimage 2009.
62. Neufeld M.Y., Kogan E., Chistik V., Korczyn A.D. Comparison of the effects of vigabatrin, lamotrigine, and topiramate on quantitative EEGs in patients with epilepsy. Clin Neuropharmacol 1999, 22(2):80-86.
63. Neuper C., Pfurtscheller G. Event-related dynamics of cortical rhythms: frequency-specific features and functional correlates. Int J Psychophysiol 2001, 43(1):41-58.
64. Nichols T.E., Holmes A.P. Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum Brain Mapp 2002, 15(1):1-25.
65. Noebels J.L. A gene for JME at last: the alpha1 GABA receptor subunit. Epilepsy Curr 2002, 2(4):131-132.
66. Nunez A., Amzica F., Steriade M. Voltage-dependent fast (20-40Hz) oscillations in long-axoned neocortical neurons. Neuroscience 1992, 51(1):7-10.
67. Panayiotopoulos C.P. A clinical guide to epileptic syndromes and their treatment 2007, Springer.
68. Paradiso G., Cunic D., Saint-Cyr J.A., Hoque T., Lozano A.M., Lang A.E., et al. Involvement of human thalamus in the preparation of self-paced movement. Brain 2004, 127(Pt 12):2717-2731.
69. Park S.P., Kwon O.Y. Increased EEG current-source density in the high beta frequency band induced by levetiracetam adjunctive therapy in refractory partial epilepsy. J Clin Neurol 2009, 5(4):178-185.
70. Pfurtscheller G., Neuper C. Simultaneous EEG 10Hz desynchronization and 40Hz synchronization during finger movements. Neuroreport 1992, 3(12):1057-1060.
71. Pfurtscheller G., Neuper C. Motor imagery activates primary sensorimotor area in humans. Neurosci Lett 1997, 239:65-68.
72. Pfurtscheller G., Neuper C., Brunner C., da Silva F.L. Beta rebound after different types of motor imagery in man. Neurosci Lett 2005, 378(3):156-159.
73. Placidi F., Tombini M., Romigi A., Bianchi L., Izzi F., Sperli F., et al. Topiramate: effect on EEG interictal abnormalities and background activity in patients affected by focal epilepsy. Epilepsy Res 2004, 58(1):43-52.
74. Porter R.J. Mechanisms of action of new antiepileptic drugs. Epilepsia 1989, 30(Suppl. 1):S29-S34. [discussion S64-8].
75. Rainesalo S., Saransaari P., Peltola J., Keranen T. Uptake of GABA and activity of GABA-transaminase in platelets from epileptic patients. Epilepsy Res 2003, 53(3):233-239.
76. Roopun A.K., Middleton S.J., Cunningham M.O., LeBeau F.E., Bibbig A., Whittington M.A., et al. A beta2-frequency (20-30Hz) oscillation in nonsynaptic networks of somatosensory cortex. Proc Natl Acad Sci USA 2006, 103(42):15646-15650.
77. Salinsky M., Storzbach D., Oken B., Spencer D. Topiramate effects on the EEG and alertness in healthy volunteers: a different profile of antiepileptic drug neurotoxicity. Epilepsy Behav 2007, 10(3):463-469.
78. Singh K.D., Barnes G.R., Hillebrand A. Group imaging of task-related changes in cortical synchronisation using nonparametric permutation testing. NeuroImage 2003, 19(4):1589-1601.
79. Singh K.D., Barnes G.R., Hillebrand A., Forde E.M., Williams A.L. Task-related changes in cortical synchronization are spatially coincident with the hemodynamic response. NeuroImage 2002, 16(1):103-114.
80. Smith S.M. Fast robust automated brain extraction. Hum Brain Mapp 2002, 17(3):143-155.
81. Tae W.S., Hong S.B., Joo E.Y., Han S.J., Cho J.W., Seo D.W., et al. Structural brain abnormalities in juvenile myoclonic epilepsy patients: volumetry and voxel-based morphometry. Korean J Radiol 2006, 7(3):162-172.
82. Tae W.S., Kim S.H., Joo E.Y., Han S.J., Kim I.Y., Kim S.I., et al. Cortical thickness abnormality in juvenile myoclonic epilepsy. J Neurol 2008, 255(4):561-566.
83. Veauthier J., Haettig H., Meencke H.J. Impact of levetiracetam add-on therapy on different EEG occipital frequencies in epileptic patients. Seizure 2009, 18(6):392-395.
84. Vrba J., Robinson S. Signal processing in magnetoencephalography. Methods 2001, 25.
85. Wilson T.W., Slason E., Asherin R., Kronberg E., Reite M.L., Teale P.D., et al. An extended motor network generates beta and gamma oscillatory perturbations during development. Brain Cogn 2010, 73(2):75-84.
86. Woermann F.G., Free S.L., Koepp M.J., Sisodiya S.M., Duncan J.S. Abnormal cerebral structure in juvenile myoclonic epilepsy demonstrated with voxel-based analysis of MRI. Brain 1999, 122(Pt 11):2101-2108.
87. Yamawaki N., Stanford I.M., Hall S.D., Woodhall G.L. Pharmacologically induced and stimulus evoked rhythmic neuronal oscillatory activity in the primary motor cortex in vitro. Neuroscience 2008, 151(2):386-395.