Gamma oscillations in the hyperkinetic state detected with chronic human brain recordings in parkinson’s disease

Journal of Neuroscience

Volumn 36, Issue 24, 2016, Pages 6445-6458

  Swann, Nicole C ^a   De Hemptinne, Coralie ^a   Miocinovic, Svjetlana ^b   Qasim, Salman ^a   Wang, Sarah S ^b   Ziman, Nathan ^b   Ostrem, Jill L ^b   Luciano, Marta San ^b   Galifianakis, Nicholas B ^b   Starr, Philip A ^a,c,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Departments of Neurology   (United States)

^c Departments of Kavli Institute for Fundamental Neuroscience   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Deep brain stimulation; Dyskinesia; Electrocorticography; Local field potentials; Motor cortex; Parkinson s disease

Indexed keywords

ADULT; ARTICLE; BRAIN DEPTH STIMULATION; CASE REPORT; COMPUTER ASSISTED TOMOGRAPHY; DISEASE SEVERITY; FEMALE; GAMMA OSCILLATION; HUMAN; HYPERKINESIA; MALE; MIDDLE AGED; MOTOR CORTEX; NERVOUS SYSTEM PARAMETERS; NUCLEAR MAGNETIC RESONANCE IMAGING; PARKINSON DISEASE; PRIORITY JOURNAL; SIGNAL NOISE RATIO; SOMATOSENSORY EVOKED POTENTIAL; STEREOTACTIC PROCEDURE; VOLUNTARY MOVEMENT; ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; BRAIN; COMPLICATION; ELECTROENCEPHALOGRAPHY; GAMMA RHYTHM; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; RECEIVER OPERATING CHARACTERISTIC; SEVERITY OF ILLNESS INDEX; SUBTHALAMIC NUCLEUS;

ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; BRAIN; DEEP BRAIN STIMULATION; ELECTROENCEPHALOGRAPHY; FEMALE; GAMMA RHYTHM; HUMANS; MALE; PARKINSON DISEASE; ROC CURVE; SEVERITY OF ILLNESS INDEX; SUBTHALAMIC NUCLEUS;

EID: 84974806622     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1128-16.2016     Document Type: Article

References (63)

1. Agnesi F, Muralidharan A, Baker KB, Vitek JL, Johnson MD (2015) Fidelity of frequency and phase entrainment of circuit-level spike activity during DBS. J Neurophysiol 114:825–834.
2. Alegre M, López-Azca´rate J, Alonso-Frech F, Rodríguez-Oroz MC, Valencia M, Guridi J, Artieda J, Obeso JA (2012) Subthalamic activity during diphasic dyskinesias in Parkinson’s disease. Mov Disord 27:1178–1181.
3. Alonso-Frech F, Zamarbide I, Alegre M, Rodríguez-Oroz MC, Guridi J, Manrique M, Valencia M, Artieda J, Obeso JA (2006) Slow oscillatory activity and levodopa-induced dyskinesias in Parkinson’s disease. Brain 129: 1748–1757.
4. Bastide MF, Meissner WG, Picconi B, Fasano S, Fernagut PO, Feyder M, Francardo V, Alcacer C, Ding Y, Brambilla R, Fisone G, Jon Stoessl A, Bourdenx M, Engeln M, Navailles S, De Deurwaerdère P, Ko WK, Simola N, Morelli M, Groc L, et al. (2015) Pathophysiology of L-dopa-induced motor and non-motor complications in Parkinson’s disease. Prog Neurobiol 132:96–168.
5. Brown P, Williams D (2005) Basal ganglia local field potential activity: character and functional significance in the human. Clin Neurophysiol 116: 2510–2519.
6. Cagnan H, Kuhn AA, Brown P (2014) Co-modulation of finely tuned highgamma band activity across hemispheres in Parkinson’s disease. Clin Neurophysiol 125:777–785.
7. Carta M, Carlsson T, Kirik D, Björklund A (2007) Dopamine released from 5-HT terminals is the cause of L-DOPA-induced dyskinesia in parkinsonian rats. Brain 130:1819–1833.
8. Cassidy M, Mazzone P, Oliviero A, Insola A, Tonali P, Di Lazzaro V, Brown P (2002) Movement-related changes in synchronization in the human basal ganglia. Brain 125:1235–1246.
9. Crone NE, Miglioretti DL, Gordon B, Lesser RP (1998a) Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. Brain 121: 2301–2315.
10. Crone NE, Miglioretti DL, Gordon B, Sieracki JM, Wilson MT, Uematsu S, Lesser RP (1998b) Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta eventrelated desynchronization. Brain 121:2271–2299.
11. Crowell AL, Ryapolova-Webb ES, Ostrem JL, Galifianakis NB, Shimamoto S, Lim DA, Starr PA (2012) Oscillations in sensorimotor cortex in movement disorders: an electrocorticography study. Brain 135:615–630.
12. de Hemptinne C, Ryapolova-Webb ES, Air EL, Garcia PA, Miller KJ, Ojemann JG, Ostrem JL, Galifianakis NB, Starr PA (2013) Exaggerated phase-amplitude coupling in the primary motor cortex in Parkinson disease. Proc Natl Acad Sci U S A 110:4780–4785.
13. de Hemptinne C, Swann NC, Ostrem JL, Ryapolova-Webb ES, San Luciano M, Galifianakis NB, Starr PA (2015) Therapeutic deep brain stimulation reduces cortical phase-amplitude coupling in Parkinson’s disease. Nat Neurosci 18:779–786.
14. Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134:9–21.
15. Fieblinger T, Cenci MA (2015) Zooming in on the small: the plasticity of striatal dendritic spines in L-DOPA-induced dyskinesia. Mov Disord 30: 484–493.
16. Fries P (2005) A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn Sci 9:474–480.
17. Fries P (2009) Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu Rev Neurosci 32:209–224.
18. Fries P, Reynolds JH, Rorie AE, Desimone R (2001) Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291: 1560–1563.
19. Garcia L, Audin J, D’Alessandro G, Bioulac B, Hammond C (2003) Dual effect of high-frequency stimulation on subthalamic neuron activity. J Neurosci 23:8743–8751.
20. Goetz CG, Nutt JG, Stebbins GT (2008) The Unified Dyskinesia Rating Scale: presentation and clinimetric profile. Mov Disord 23:2398–2403.
21. Graziano MS, Taylor CS, Moore T (2002) Complex movements evoked by microstimulation of precentral cortex. Neuron 34:841–851.
22. Halje P, Tamtè M, Richter U, Mohammed M, Cenci MA, Petersson P (2012) Levodopa-induced dyskinesia is strongly associated with resonant cortical oscillations. J Neurosci 32:16541–16551.
23. Hammond C, Bergman H, Brown P (2007) Pathological synchronization in Parkinson’s disease: networks, models and treatments. Trends Neurosci 30:357–364.
24. Hashimoto T, Elder CM, Okun MS, Patrick SK, Vitek JL (2003) Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons. J Neurosci 23:1916–1923.
25. Hatsopoulos NG, Xu Q, Amit Y (2007) Encoding of movement fragments in the motor cortex. J Neurosci 27:5105–5114.
26. Kempf F, Brücke C, Salih F, Trottenberg T, Kupsch A, Schneider GH, Doyle Gaynor LM, Hoffmann KT, Vesper J, Wöhrle J, Altenmuller DM, Krauss JK, Mazzone P, Di Lazzaro V, Yelnik J, Kühn AA, Brown P (2009) Gamma activity and reactivity in human thalamic local field potentials. Eur J Neurosci 29:943–953.
27. Kühn AA, Kupsch A, Schneider GH, Brown P (2006) Reduction in subthalamic 8–35 Hz oscillatory activity correlates with clinical improvement in Parkinson’s disease. Eur J Neurosci 23:1956–1960.
28. Kühn AA, Kempf F, Brücke C, Gaynor Doyle L, Martinez-Torres I, Pogosyan A, Trottenberg T, Kupsch A, Schneider GH, Hariz MI, Vandenberghe W, Nuttin B, Brown P (2008) 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 28:6165–6173.
29. Li Q, Ke Y, Chan DC, Qian ZM, Yung KK, Ko H, Arbuthnott GW, Yung WH (2012) Therapeutic deep brain stimulation in Parkinsonian rats directly influences motor cortex. Neuron 76:1030–1041.
30. Little S, Pogosyan A, Neal S, Zavala B, Zrinzo L, Hariz M, Foltynie T, Limousin P, Ashkan K, FitzGerald J, Green AL, Aziz TZ, Brown P (2013) Adaptive deep brain stimulation in advanced Parkinson disease. Ann Neurol 74:449–457.
31. Litvak V, Eusebio A, Jha A, Oostenveld R, Barnes G, Foltynie T, Limousin P, Zrinzo L, Hariz MI, Friston K, Brown P (2012) Movement-related changes in local and long-range synchronization in Parkinson’s disease revealed by simultaneous magnetoencephalography and intracranial recordings. J Neurosci 32:10541–10553.
32. Mallet L, Polosan M, Jaafari N, Baup N, Welter ML, Fontaine D, du Montcel ST, Yelnik J, Chéreau I, Arbus C, Raoul S, Aouizerate B, Damier P, Chabardè s S, Czernecki V, Ardouin C, Krebs MO, Bardinet E, Chaynes P, Burbaud P, et al. (2008) Subthalamic nucleus stimulation in severe obsessive-compulsive disorder. N Engl J Med 359:2121–2134.
33. Manning JR, Jacobs J, Fried I, Kahana MJ (2009) Broadband shifts in local field potential power spectra are correlated with single-neuron spiking in humans. J Neurosci 29:13613–13620.
34. Miller KJ, Leuthardt EC, Schalk G, Rao RP, Anderson NR, Moran DW, Miller JW, Ojemann JG (2007) Spectral Changes in Cortical Surface Potentials during Motor Movement. J Neurosci 27:2424–2432.
35. Moran A, Bergman H, Israel Z, Bar-Gad I (2008) Subthalamic nucleus functional organization revealed by parkinsonian neuronal oscillations and synchrony. Brain 131:3395–3409.
36. Mouton S, Xie-Brustolin J, Mertens P, Polo G, Damier P, Broussolle E, Thobois S (2006) Chorea induced by globus pallidus externus stimulation in a dystonic patient. Mov Disord 21:1771–1773.
37. Ostrem JL, Racine CA, Glass GA, Grace JK, Volz MM, Heath SL, Starr PA (2011) Subthalamic nucleus deep brain stimulation in primary cervical dystonia. Neurology 76:870–878.
38. Oyama G, Foote KD, Jacobson CE 4th, Velez-Lago F, Go C, Limotai N, Zeilman PR, Romrell J, Wu SS, Neal D, Okun MS (2012) GPi and STN deep brain stimulation can suppress dyskinesia in Parkinson’s disease. Parkinsonism Relat Disord 18:814–818.
39. Priori A, Foffani G, Pesenti A, Tamma F, Bianchi AM, Pellegrini M, Locatelli M, Moxon KA, Villani RM (2004) Rhythm-specific pharmacological modulation of subthalamic activity in Parkinson’s disease. Exp Neurol 189:369–379.
40. Pritchard WS (1992) The brain in fractal time: 1/f-like power spectrum scaling of the human electroencephalogram. Int J Neurosci 66:119–129.
41. Puig MV, Watakabe A, Ushimaru M, Yamamori T, Kawaguchi Y (2010) Serotonin modulates fast-spiking interneuron and synchronous activity in the rat prefrontal cortex through 5-HT1A and 5-HT2A receptors. J Neurosci 30:2211–2222.
42. Ray S, Crone NE, Niebur E, Franaszczuk PJ, Hsiao SS (2008) Neural correlates of high-gamma oscillations (60–200 Hz) in macaque local field potentials and their potential implications in electrocorticography. J Neurosci 28:11526–11536.
43. Rosin B, Slovik M, Mitelman R, Rivlin-Etzion M, Haber SN, Israel Z, Vaadia E, Bergman H (2011) Closed-loop deep brain stimulation is Superior in ameliorating parkinsonism. Neuron 72:370–384.
44. Rowland NC, De Hemptinne C, Swann NC, Qasim S, Miocinovic S, Ostrem JL, Knight RT, Starr PA (2015) Task-related activity in sensorimotor cortex in Parkinson’s disease and essential tremor: changes in beta and gamma bands. Front Hum Neurosci 9:512.
45. Salkoff DB, Zagha E, Yüzgec¸ Ö, McCormick DA (2015) Synaptic mechanisms of tight spike synchrony at gamma frequency in cerebral cortex. J Neurosci 35:10236–10251.
46. Scheffer-Teixeira R, Belchior H, Leão RN, Ribeiro S, Tort AB (2013) On high-frequency field oscillations (>100 Hz) and the spectral leakage of spiking activity. J Neurosci 33:1535–1539.
47. Shahlaie K, Larson PS, Starr PA (2011) Intraoperative computed tomography for deep brain stimulation surgery: technique and accuracy assessment. Neurosurgery 68:114–124; discussion 124.
48. Siegel M, Donner TH, Engel AK (2012) Spectral fingerprints of large-scale neuronal interactions. Nat Rev Neurosci 13:121–134.
49. Silberstein P, Pogosyan A, Kühn AA, Hotton G, Tisch S, Kupsch A, Dowsey-Limousin P, Hariz MI, Brown P (2005) Cortico-cortical coupling in Parkinson’s disease and its modulation by therapy. Brain 128:1277–1291.
50. Sohal VS (2012) Insights into cortical oscillations arising from optogenetic studies. Biol Psychiatry 71:1039–1045.
51. Starr PA, Christine CW, Theodosopoulos PV, Lindsey N, Byrd D, Mosley A, Marks WJ Jr (2002) Implantation of deep brain stimulators into the subthalamic nucleus: technical approach and magnetic resonance imaging-verified lead locations. J Neurosurg 97:370–387.
52. Teles-Grilo Ruivo LM, Mellor JR (2013) Cholinergic modulation of hippocampal network function. Front Synaptic Neurosci 5:2.
53. Thiele SL, Chen B, Lo C, Gertler TS, Warre R, Surmeier JD, Brotchie JM, Nash JE (2014) Selective loss of bi-directional synaptic plasticity in the direct and indirect striatal output pathways accompanies generation of parkinsonism and l-DOPA induced dyskinesia in mouse models. Neurobiol Dis 71:334–344.
54. Trottenberg T, Fogelson N, Kühn AA, Kivi A, Kupsch A, Schneider GH, Brown P (2006) Subthalamic gamma activity in patients with Parkinson’s disease. Exp Neurol 200:56–65.
55. Voytek B, Knight RT (2015) Dynamic network communication as a unifying neural basis for cognition, development, aging, and disease. Biol Psychiatry 77:1089–1097.
56. Weinberger M, Dostrovsky JO (2011) A basis for the pathological oscillations in basal ganglia: the crucial role of dopamine. Neuroreport 22: 151–156.
57. Weinberger M, Hutchison WD, Alavi M, Hodaie M, Lozano AM, Moro E, Dostrovsky JO (2012) Oscillatory activity in the globus pallidus internus: comparison between Parkinson’s disease and dystonia. Clin Neurophysiol 123:358–368.
58. Williams D, Tijssen M, Van Bruggen G, Bosch A, Insola A, Di Lazzaro V, Mazzone P, Oliviero A, Quartarone A, Speelman H, Brown P (2002) Dopamine-dependent changes in the functional connectivity between basal ganglia and cerebral cortex in humans. Brain 125:1558–1569.
59. Yelnik J, Damier P, Bejjani BP, Francois C, Gervais D, Dormont D, Arnulf I, MBonnet A, Cornu P, Pidoux B, Agid Y (2000) Functional mapping of the human globus pallidus: contrasting effect of stimulation in the internal and external pallidum in Parkinson’s disease. Neuroscience 101: 77–87.
60. Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, O’Shea DJ, Sohal VS, Goshen I, Finkelstein J, Paz JT, Stehfest K, Fudim R, Ramakrishnan C, Huguenard JR, Hegemann P, Deisseroth K (2011) Neocortical excitation/ inhibition balance in information processing and social dysfunction. Nature 477:171–178.
61. Yousry TA, Schmid UD, Alkadhi H, Schmidt D, Peraud A, Buettner A, Winkler P (1997) Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. Brain 120:141–157.
62. Zheng Z, Li Y, Li J, Zhang Y, Zhang X, Zhuang P (2010) Stimulationinduced dyskinesia in the early stage after subthalamic deep brain stimulation. Stereotact Funct Neurosurg 88:29–34.
63. Zwieg MH, Campbell G (1993) Receiver-operating characteristic (ROC) plots: a fundamental evaluation tool in clinical medicine. Clin Chem 39:561–577.