Subthalamic nucleus phase-amplitude coupling correlates with motor impairment in Parkinson's disease

Clinical Neurophysiology

Volumn 127, Issue 4, 2016, Pages 2010-2019

  van Wijk, Bernadette C M ^a   Beudel, Martijn ^a,b,c   Jha, Ashwani ^a   Oswal, Ashwini ^a,b   Foltynie, Tom ^a   Hariz, Marwan I ^a   Limousin, Patricia ^a   Zrinzo, Ludvic ^a   Aziz, Tipu Z ^b,d   Green, Alexander L ^b,d   Brown, Peter ^b,d   Litvak, Vladimir ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Beta oscillations; Cross frequency coupling; Local field potentials; Motor system; Parkinson's disease; Subthalamic nucleus

Indexed keywords

ARTICLE; BETA RHYTHM; BRADYKINESIA; BRAIN DEPTH STIMULATION; CLINICAL ARTICLE; DEPTH ELECTRODE; DISEASE SEVERITY; HIGH FREQUENCY OSCILLATION; HUMAN; IPSILATERAL MOTOR CORTEX; MAGNETOENCEPHALOGRAPHY; MOTOR CORTEX; MOTOR DYSFUNCTION; PARKINSON DISEASE; PRIORITY JOURNAL; SUBTHALAMIC NUCLEUS; COHORT ANALYSIS; FEMALE; MALE; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES;

BETA RHYTHM; COHORT STUDIES; DEEP BRAIN STIMULATION; FEMALE; HUMANS; MAGNETOENCEPHALOGRAPHY; MALE; MOTOR CORTEX; PARKINSON DISEASE; SUBTHALAMIC NUCLEUS;

EID: 84960158823     PISSN: 13882457     EISSN: 18728952     Source Type: Journal    
DOI: 10.1016/j.clinph.2016.01.015     Document Type: Article

References (59)

1. Alegre M., Alonso-Frech F., Rodriguez-Oroz M.C., Guridi J., Zamarbide I., Valencia M., et al. Movement-related changes in oscillatory activity in the human subthalamic nucleus: ipsilateral vs contralateral movements. Eur J Neurosci 2005, 22:2315-2324.
2. Alonso-Frech F., Zamarbide I., Alegre M., Rodriguez-Oroz M.C., Guridi J., Manrique M., et al. Slow oscillatory activity and levodopa-induced dyskinesias in Parkinson's disease. Brain 2006, 129:1748-1757.
3. Androulidakis A.G., Kühn A.A., Chen C.C., Blomstedt P., Kempf F., Kupsch A., et al. Dopaminergic therapy promotes lateralized motor activity in the subthalamic area in Parkinson's disease. Brain 2007, 130:457-468.
4. Cassidy M., Mazzone P., Oliviero A., Insola A., Tonali P., Di Lazzaro V., et al. Movement-related changes in synchronization in the human basal ganglia. Brain 2002, 125:1235-1246.
5. Connolly A.T., Jensen A.L., Bello E.M., Netoff T.I., Baker K.B., Johnson M.D., et al. Modulations in oscillatory frequency and coupling in globus pallidus with increasing parkinsonian severity. J Neurosci 2015, 35:6231-6240.
6. de Hemptinne C., Ryapolova-Webb E.S., Air E.L., Garcia P.A., Miller K.J., Ojemann J.G., et al. Exaggerated phase-amplitude coupling in the primary motor cortex in Parkinson disease. Proc Natl Acad Sci USA 2013, 110:4780-4785.
7. de Hemptinne C., Swann N.C., Ostrem J.L., Ryapolova-Webb E.S., San L.M., Galifianakis N.B., et al. Therapeutic deep brain stimulation reduces cortical phase-amplitude coupling in Parkinson's disease. Nat Neurosci 2015, 18:779-786.
8. Deuschl G., Schade-Brittinger C., Krack P., Volkmann J., Schafer H., Botzel K., et al. A randomized trial of deep-brain stimulation for Parkinson's disease. N Engl J Med 2006, 355:896-908.
9. Eusebio A., Thevathasan W., Doyle G.L., Pogosyan A., Bye E., Foltynie T., et al. Deep brain stimulation can suppress pathological synchronisation in parkinsonian patients. J Neurol Neurosurg Psychiatry 2011, 82:569-573.
10. Foffani G., Priori A., Egidi M., Rampini P., Tamma F., Caputo E., et al. 300-Hz subthalamic oscillations in Parkinson's disease. Brain 2003, 126:2153-2163.
11. Fogelson N., Pogosyan A., Kühn A.A., Kupsch A., van B.G., Speelman H., et al. Reciprocal interactions between oscillatory activities of different frequencies in the subthalamic region of patients with Parkinson's disease. Eur J Neurosci 2005, 22:257-266.
12. Fogelson N., Williams D., Tijssen M., van B.G., Speelman H., Brown P. Different functional loops between cerebral cortex and the subthalmic area in Parkinson's disease. Eur J Neurosci 2005, 22:257-266.
13. Foltynie T., Zrinzo L., Martinez-Torres I., Tripoliti E., Petersen E., Holl E., et al. MRI-guided STN DBS in Parkinson's disease without microelectrode recording: efficacy and safety. J Neurol Neurosurg Psychiatry 2011, 82:358-363.
14. Gale J.T., Shields D.C., Jain F.A., Amirnouin R., Eskandar E.N. Subthalamic nucleus discharge patterns during movement in the normal monkey and Parkinsonian patient. Brain Res 2009, 1260:15-23.
15. Galvan A., Wichmann T. Pathophysiology of parkinsonism. Clin Neurophysiol 2008, 119:1459-1474.
16. Gatev P., Darbin O., Wichmann T. Oscillations in the basal ganglia under normal conditions and in movement disorders. Mov Disord 2006, 21:1566-1577.
17. Gibb W.R.G., Lees A.J. The relevance of the Lewy body to the pathogenesis of idiopathic parkinsons-disease. J Neurol Neurosurg Psychiatry 1988, 51:745-752.
18. Hammond C., Bergman H., Brown P. Pathological synchronization in Parkinson's disease: networks, models and treatments. Trends Neurosci 2007, 30:357-364.
19. Hariz M.I., Krack P., Melvill R., Jorgensen J.V., Hamel W., Hirabayashi H., et al. A quick and universal method for stereotactic visualization of the subthalamic nucleus before and after implantation of deep brain stimulation electrodes. Stereotact Funct Neurosurg 2003, 80:96-101.
20. Herz D.M., Florin E., Christensen M.S., Reck C., Barbe M.T., Tscheuschler M.K., et al. Dopamine replacement modulates oscillatory coupling between premotor and motor cortical areas in Parkinson's disease. Cereb Cortex 2014, 24:2873-2883.
21. Herz D.M., Siebner H.R., Hulme O.J., Florin E., Christensen M.S., Timmermann L. Levodopa reinstates connectivity from prefrontal to premotor cortex during externally paced movement in Parkinson's disease. Neuroimage 2014, 90:15-23.
22. Jensen O., Colgin L.L. Cross-frequency coupling between neuronal oscillations. Trends Cogn Sci 2007, 11:267-269.
23. Krack P., Batir A., Van Blercom N., Chabardes S., Fraix V., Ardouin C., et al. Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med 2003, 349:1925-1934.
24. Kühn A.A., Kupsch A., Schneider G.H., Brown P. Reduction in subthalamic 8-35 Hz oscillatory activity correlates with clinical improvement in Parkinson's disease. Eur J Neurosci 2006, 23:1956-1960.
25. Kühn A.A., Kempf F., Brucke C., Gaynor D.L., Martinez-Torres I., Pogosyan A., et al. High-frequency stimulation of the subthalamic nucleus suppresses oscillatory beta activity in patients with Parkinson's disease in parallel with improvement in motor performance. J Neurosci 2008, 28:6165-6173.
26. Kühn A.A., Tsui A., Aziz T., Ray N., Brucke C., Kupsch A., et al. Pathological synchronisation in the subthalamic nucleus of patients with Parkinson's disease relates to both bradykinesia and rigidity. Exp Neurol 2009, 215:380-387.
27. Lalo E., Thobois S., Sharott A., Polo G., Mertens P., Pogosyan A., et al. Patterns of bidirectional communication between cortex and basal ganglia during movement in patients with Parkinson disease. J Neurosci 2008, 28:3008-3016.
28. Little S., Pogosyan A., Neal S., Zavala B., Zrinzo L., Hariz M., et al. Adaptive deep brain stimulation in advanced Parkinson disease. Ann Neurol 2013, 74:449-457.
29. Little S., Tan H., Anzak A., Pogosyan A., Kühn A., Brown P. Bilateral functional connectivity of the basal ganglia in patients with Parkinson's disease and its modulation by dopaminergic treatment. PLoS One 2013, 8:e82762.
30. Litvak V., Eusebio A., Jha A., Oostenveld R., Barnes G.R., Penny W.D., et al. Optimized beamforming for simultaneous MEG and intracranial local field potential recordings in deep brain stimulation patients. Neuroimage 2010, 50:1578-1588.
31. Litvak V., Jha A., Eusebio A., Oostenveld R., Foltynie T., Limousin P., et al. Resting oscillatory cortico-subthalamic connectivity in patients with Parkinson's disease. Brain 2011, 134:359-374.
32. Litvak V., Mattout J., Kiebel S., Phillips C., Henson R., Kilner J., et al. EEG and MEG data analysis in SPM8. Comput Intell Neurosci 2011, 2011:852961.
33. Litvak V., Eusebio A., Jha A., Oostenveld R., Barnes G., Foltynie T., et al. Movement-related changes in local and long-range synchronization in Parkinson's disease revealed by simultaneous magnetoencephalography and intracranial recordings. J Neurosci 2012, 32:10541-10553.
34. Lobb C. Abnormal bursting as a pathophysiological mechanism in Parkinson's disease. Basal Ganglia 2014, 3:187-195.
35. López-Azcárate J., Tainta M., Rodríguez-Oroz M.C., Valencia M., González R., Guridi J., et al. Coupling between beta and high-frequency activity in the human subthalamic nucleus may be a pathophysiological mechanism in Parkinson's disease. J Neurosci 2010, 30:6667-6677.
36. Nolte G. The magnetic lead field theorem in the quasi-static approximation and its use for magnetoencephalography forward calculation in realistic volume conductors. Phys Med Biol 2003, 48:3637-3652.
37. Oswal A., Brown P., Litvak V. Movement related dynamics of subthalmo-cortical alpha connectivity in Parkinson's disease. Neuroimage 2013, 70:132-142.
38. Oswal A., Brown P., Litvak V. Synchronized neural oscillations and the pathophysiology of Parkinson's disease. Cur Opin Neurol 2013, 26:662-670.
39. Oswal A., Jha A., Neal S., Reid A., Bradbury D., Aston P., et al. Analysis of simultaneous MEG and intracranial LFP recordings during deep brain stimulation: a protocol and experimental validation. J Neurosci Methods 2015, 261:29-46.
40. Özkurt T.E., Butz M., Homburger M., Elben S., Vesper J., Wojtecki L., et al. High frequency oscillations in the subthalamic nucleus: a neurophysiological marker of the motor state in Parkinson's disease. Exp Neurol 2011, 229:324-331.
41. Penny W.D., Duzel E., Miller K.J., Ojemann J.G. Testing for nested oscillation. J Neurosci Methods 2008, 174:50-61.
42. Ray N.J., Jenkinson N., Wang S., Holland P., Brittain J.S., Joint C., et al. Local field potential beta activity in the subthalamic nucleus of patients with Parkinson's disease is associated with improvements in bradykinesia after dopamine and deep brain stimulation. Exp Neurol 2008, 213:108-113.
43. Rodriguez-Oroz M.C., Obeso J.A., Lang A.E., Houeto J.L., Pollak P., Rehncrona S., et al. Bilateral deep brain stimulation in Parkinson's disease: a multicentre study with 4 years follow-up. Brain 2005, 128:2240-2249.
44. Sanders T.H., Clements M.A., Wichmann T. Parkinsonism-related features of neuronal discharge in primates. J Neurophysiol 2013, 110:720-731.
45. Sharott A., Gulberti A., Zittel S., Jones A.A.T., Fickel U., Munchau A., et al. Activity parameters of subthalamic nucleus neurons selectively predict motor symptom severity in Parkinson's disease. J Neurosci 2014, 34:6273-6285.
46. Shimamoto S.A., Ryapolova-Webb E.S., Ostrem J.L., Galifianakis N.B., Miller K.J., Starr P.A. Subthalamic nucleus neurons are synchronized to primary motor cortex local field potentials in Parkinson's disease. J Neurosci 2013, 33:7220-7233.
47. Stoffers D., Bosboom J.L., Deijen J.B., Wolters E.C., Stam C.J., Berendse H.W. Increased cortico-cortical functional connectivity in early-stage Parkinson's disease: an MEG study. Neuroimage 2008, 41:212-222.
48. Tan H.L., Pogosyan A., Anzak A., Ashkan K., Bogdanovic M., Green A.L., et al. Complementary roles of different oscillatory activities in the subthalamic nucleus in coding motor effort in Parkinsonism. Exp Neurol 2013, 248:187-195.
49. Tsiokos C., Hu X., Pouratian N. 200-300 Hz movement modulated oscillations in the internal globus pallidus of patients with Parkinson's disease. Neurobiol Dis 2013, 54:464-474.
50. Tykocki T., Nauman P., Koziara H., Mandat T. Microlesion effect as a predictor of the effectiveness of subthalamic deep brain stimulation for Parkinson's disease. Stereotact Funct Neurosurg 2013, 91:12-17.
51. van Wijk B.C.M., Jha A., Penny W., Litvak V. Parametric estimation of cross-frequency coupling. J Neurosci Methods 2015, 243:94-102.
52. Wager T.D., Keller M.C., Lacey S.C., Jonides J. Increased sensitivity in neuroimaging analyses using robust regression. Neuroimage 2005, 26:99-113.
53. Wang J., Hirschmann J., Elben S., Hartmann C.J., Vesper J., Wojtecki L., et al. High-frequency oscillations in Parkinson's disease: spatial distribution and clinical relevance. Mov Disord 2014, 29:1265-1272.
54. Weaver F.M., Follett K., Stern M., Hur K., Harris C., Marks W.J., et al. Bilateral deep brain stimulation vs best medical therapy for patients with advanced Parkinson disease: a randomized controlled trial. JAMA 2009, 301:63-73.
55. Weinberger M., Mahant N., Hutchison W.D., Lozano A.M., Moro E., Hodaie M., et al. Beta oscillatory activity in the subthalamic nucleus and its relation to dopaminergic response in Parkinson's disease. J Neurophysiol 2006, 96:3248-3256.
56. Wichmann T., Soares J. Neuronal firing before and after burst discharges in the monkey basal ganglia is predictably patterned in the normal state and altered in parkinsonism. J Neurophysiol 2006, 95:2120-2133.
57. Williams D., Tijssen M., van Bruggen G., Bosch A., Insola A., Di Lazzaro V., et al. Dopamine-dependent changes in the functional connectivity between basal ganglia and cerebral cortex in humans. Brain 2002, 125:1558-1569.
58. Yanagisawa T., Yamashita O., Hirata M., Kishima H., Saitoh Y., Goto T., et al. Regulation of motor representation by phase-amplitude coupling in the sensorimotor cortex. J Neurosci 2012, 32:15467-15475.
59. Yang A.I., Vanegas N., Lungu C., Zaghloul K.A. Beta-coupled high-frequency activity and beta-locked neuronal spiking in the subthalamic nucleus of Parkinson's disease. J Neurosci 2014, 34:12816-12827.