Closed-loop deep brain stimulation is superior in ameliorating parkinsonism

Neuron

Volumn 72, Issue 2, 2011, Pages 370-384

  Rosin, Boris ^a   Slovik, Maya ^a   Mitelman, Rea ^a,b   Rivlin Etzion, Michal ^a,b   Haber, Suzanne N ^c   Israel, Zvi ^a   Vaadia, Eilon ^a,b   Bergman, Hagai ^a,b  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE;

AKINESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BASAL GANGLION; BRAIN CELL; BRAIN CORTEX; BRAIN DEPTH STIMULATION; CHLOROCEBUS; CLOSED LOOP BRAIN DEPTH STIMULATION; CONTROLLED STUDY; DISEASE MODEL; NERVE CELL MEMBRANE POTENTIAL; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; TREATMENT RESPONSE;

ANIMALS; BASAL GANGLIA; CERCOPITHECUS AETHIOPS; DEEP BRAIN STIMULATION; GLOBUS PALLIDUS; MPTP POISONING; NEURONS; PARKINSON DISEASE, SECONDARY; TREATMENT OUTCOME;

EID: 80054842563     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2011.08.023     Document Type: Article

References (80)

1. Albin R.L., Young A.B., Penney J.B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989, 12:366-375.
2. Alexander G.E., Crutcher M.D. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 1990, 13:266-271.
3. Alexander G.E., DeLong M.R., Strick P.L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 1986, 9:357-381.
4. Baker K.B., Zhang J., Vitek J.L. Pallidal stimulation: Effect of pattern and rate on bradykinesia in the non-human primate model of Parkinson's disease. Exp. Neurol. 2011, 231:309-313.
5. Bar-Gad I., Havazelet-Heimer G., Goldberg J.A., Ruppin E., Bergman H. Reinforcement-driven dimensionality reduction-a model for information processing in the basal ganglia. J. Basic Clin. Physiol. Pharmacol. 2000, 11:305-320.
6. Bar-Gad I., Elias S., Vaadia E., Bergman H. Complex locking rather than complete cessation of neuronal activity in the globus pallidus of a 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-treated primate in response to pallidal microstimulation. J. Neurosci. 2004, 24:7410-7419.
7. Batista C.A., Lopes S.R., Viana R.L., Batista A.M. Delayed feedback control of bursting synchronization in a scale-free neuronal network. Neural Netw. 2010, 23:114-124.
8. Benabid A.L., Chabardes S., Torres N., Piallat B., Krack P., Fraix V., Pollak P. Functional neurosurgery for movement disorders: a historical perspective. Prog. Brain Res. 2009, 175:379-391.
9. Bergman H., Wichmann T., DeLong M.R. Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 1990, 249:1436-1438.
10. Bergman H., Wichmann T., Karmon B., DeLong M.R. The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J. Neurophysiol. 1994, 72:507-520.
11. Boraud T., Bezard E., Bioulac B., Gross C. High frequency stimulation of the internal Globus Pallidus (GPi) simultaneously improves parkinsonian symptoms and reduces the firing frequency of GPi neurons in the MPTP-treated monkey. Neurosci. Lett. 1996, 215:17-20.
12. Bronstein J.M., Tagliati M., Alterman R.L., Lozano A.M., Volkmann J., Stefani A., Horak F.B., Okun M.S., Foote K.D., Krack P., et al. Deep brain stimulation for Parkinson disease: an expert consensus and review of key issues. Arch. Neurol. 2011, 68:165.
13. Brown P. Oscillatory nature of human basal ganglia activity: relationship to the pathophysiology of Parkinson's disease. Mov. Disord. 2003, 18:357-363.
14. Brown P. Bad oscillations in Parkinson's disease. J. Neural Transm. Suppl. 2006, 27-30.
15. Carlson J.D., Cleary D.R., Cetas J.S., Heinricher M.M., Burchiel K.J. Deep brain stimulation does not silence neurons in subthalamic nucleus in Parkinson's patients. J. Neurophysiol. 2010, 103:962-967.
16. Cassim F., Labyt E., Devos D., Defebvre L., Destée A., Derambure P. Relationship between oscillations in the basal ganglia and synchronization of cortical activity. Epileptic Disord. 2002, 4(Suppl 3):S31-S45.
17. Chan V., Starr P.A., Turner R.S. Bursts and oscillations as independent properties of neural activity in the parkinsonian globus pallidus internus. Neurobiol. Dis. 2011, 41:2-10.
18. de Solages C., Hill B.C., Koop M.M., Henderson J.M., Bronte-Stewart H. Bilateral symmetry and coherence of subthalamic nuclei beta band activity in Parkinson's disease. Exp. Neurol. 2010, 221:260-266.
19. Deniau J.M., Degos B., Bosch C., Maurice N. Deep brain stimulation mechanisms: beyond the concept of local functional inhibition. Eur. J. Neurosci. 2010, 32:1080-1091.
20. Deuschl G., Herzog J., Kleiner-Fisman G., Kubu C., Lozano A.M., Lyons K.E., Rodriguez-Oroz M.C., Tamma F., Tröster A.I., Vitek J.L., et al. Deep brain stimulation: postoperative issues. Mov. Disord. 2006, 21(Suppl 14):S219-S237.
21. Dorval A.D., Kuncel A.M., Birdno M.J., Turner D.A., Grill W.M. Deep brain stimulation alleviates parkinsonian bradykinesia by regularizing pallidal activity. J. Neurophysiol. 2010, 104:911-921.
22. Dostrovsky J.O., Levy R., Wu J.P., Hutchison W.D., Tasker R.R., Lozano A.M. Microstimulation-induced inhibition of neuronal firing in human globus pallidus. J. Neurophysiol. 2000, 84:570-574.
23. Eusebio A., Brown P. Oscillatory activity in the basal ganglia. Parkinsonism Relat. Disord. 2007, 13(Suppl 3):S434-S436.
24. Eusebio A., Brown P. Synchronisation in the beta frequency-band-the bad boy of parkinsonism or an innocent bystander?. Exp. Neurol. 2009, 217:1-3.
25. Feng X.J., Greenwald B., Rabitz H., Shea-Brown E., Kosut R. Toward closed-loop optimization of deep brain stimulation for Parkinson's disease: concepts and lessons from a computational model. J. Neural Eng. 2007, 4:L14-L21.
26. Follett K.A., Weaver F.M., Stern M., Hur K., Harris C.L., Luo P., Marks W.J., Rothlind J., Sagher O., Moy C., et al. Pallidal versus subthalamic deep-brain stimulation for Parkinson's disease. N. Engl. J. Med. 2010, 362:2077-2091. CSP 468 Study Group.
27. Frank M.J., Samanta J., Moustafa A.A., Sherman S.J. Hold your horses: impulsivity, deep brain stimulation, and medication in parkinsonism. Science 2007, 318:1309-1312.
28. Frankemolle A.M., Wu J., Noecker A.M., Voelcker-Rehage C., Ho J.C., Vitek J.L., McIntyre C.C., Alberts J.L. Reversing cognitive-motor impairments in Parkinson's disease patients using a computational modelling approach to deep brain stimulation programming. Brain 2010, 133:746-761.
29. Goldberg J.A., Boraud T., Maraton S., Haber S.N., Vaadia E., Bergman H. Enhanced synchrony among primary motor cortex neurons in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine primate model of Parkinson's disease. J. Neurosci. 2002, 22:4639-4653.
30. Goldberg J.A., Rokni U., Boraud T., Vaadia E., Bergman H. Spike synchronization in the cortex/basal-ganglia networks of Parkinsonian primates reflects global dynamics of the local field potentials. J. Neurosci. 2004, 24:6003-6010.
31. Gubellini P., Salin P., Kerkerian-Le Goff L., Baunez C. Deep brain stimulation in neurological diseases and experimental models: from molecule to complex behavior. Prog. Neurobiol. 2009, 89:79-123.
32. Hammond C., Bergman H., Brown P. Pathological synchronization in Parkinson's disease: networks, models and treatments. Trends Neurosci. 2007, 30:357-364.
33. Heimer G., Bar-Gad I., Goldberg J.A., Bergman H. Dopamine replacement therapy reverses abnormal synchronization of pallidal neurons in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine primate model of parkinsonism. J. Neurosci. 2002, 22:7850-7855.
34. Heimer G., Rivlin M., Israel Z., Bergman H. Synchronizing activity of basal ganglia and pathophysiology of Parkinson's disease. J. Neural Transm. Suppl. 2006, 17-20.
35. Hill D.N., Mehta S.B., Kleinfeld D. Quality metrics to accompany spike sorting of extracellular signals. J. Neurosci. 2011, 31:8699-8705.
36. Hurtado J.M., Rubchinsky L.L., Sigvardt K.A., Wheelock V.L., Pappas C.T. Temporal evolution of oscillations and synchrony in GPi/muscle pairs in Parkinson's disease. J. Neurophysiol. 2005, 93:1569-1584.
37. Hutchison W.D., Dostrovsky J.O., Walters J.R., Courtemanche R., Boraud T., Goldberg J., Brown P. Neuronal oscillations in the basal ganglia and movement disorders: evidence from whole animal and human recordings. J. Neurosci. 2004, 24:9240-9243.
38. Johnson M.D., McIntyre C.C. Quantifying the neural elements activated and inhibited by globus pallidus deep brain stimulation. J. Neurophysiol. 2008, 100:2549-2563.
39. Johnson M.D., Vitek J.L., McIntyre C.C. Pallidal stimulation that improves parkinsonian motor symptoms also modulates neuronal firing patterns in primary motor cortex in the MPTP-treated monkey. Exp. Neurol. 2009, 219:359-362.
40. Kühn A.A., Tsui A., Aziz T., Ray N., Brücke C., Kupsch A., Schneider G.H., Brown P. Pathological synchronisation in the subthalamic nucleus of patients with Parkinson's disease relates to both bradykinesia and rigidity. Exp. Neurol. 2009, 215:380-387.
41. Lafreniere-Roula M., Kim E., Hutchison W.D., Lozano A.M., Hodaie M., Dostrovsky J.O. High-frequency microstimulation in human globus pallidus and substantia nigra. Exp. Brain Res. 2010, 205:251-261.
42. Lalo E., Thobois S., Sharott A., Polo G., Mertens P., Pogosyan A., Brown P. Patterns of bidirectional communication between cortex and basal ganglia during movement in patients with Parkinson disease. J. Neurosci. 2008, 28:3008-3016.
43. Langston J.W., Irwin I., Langston E.B. A comparison of the acute and chronic effects of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine (MPTP)-induced parkinsonism in humans and the squirrel monkey. Neurology 1984, 34(Suppl. 1):268.
44. Lathi B.P. Linear Systems and Signals 2004, Oxford University Press, New York.
45. Leblois A., Meissner W., Bioulac B., Gross C.E., Hansel D., Boraud T. Late emergence of synchronized oscillatory activity in the pallidum during progressive Parkinsonism. Eur. J. Neurosci. 2007, 26:1701-1713.
46. Lee J.Y., Jeon B.S., Paek S.H., Lim Y.H., Kim M.R., Kim C. Reprogramming guided by the fused images of MRI and CT in subthalamic nucleus stimulation in Parkinson disease. Clin. Neurol. Neurosurg. 2010, 112:47-53.
47. Levy R., Hutchison W.D., Lozano A.M., Dostrovsky J.O. Synchronized neuronal discharge in the basal ganglia of parkinsonian patients is limited to oscillatory activity. J. Neurosci. 2002, 22:2855-2861.
48. Lozano A.M., Eltahawy H. How does DBS work?. Suppl. Clin. Neurophysiol. 2004, 57:733-736.
49. Magill P.J., Sharott A., Bolam J.P., Brown P. Brain state-dependency of coherent oscillatory activity in the cerebral cortex and basal ganglia of the rat. J. Neurophysiol. 2004, 92:2122-2136.
50. Mallet N., Pogosyan A., Sharott A., Csicsvari J., Bolam J.P., Brown P., Magill P.J. Disrupted dopamine transmission and the emergence of exaggerated beta oscillations in subthalamic nucleus and cerebral cortex. J. Neurosci. 2008, 28:4795-4806.
51. McCairn K.W., Turner R.S. Deep brain stimulation of the globus pallidus internus in the parkinsonian primate: local entrainment and suppression of low-frequency oscillations. J. Neurophysiol. 2009, 101:1941-1960.
52. McIntyre C.C., Savasta M., Kerkerian-Le Goff L., Vitek J.L. Uncovering the mechanism(s) of action of deep brain stimulation: activation, inhibition, or both. Clin. Neurophysiol. 2004, 115:1239-1248.
53. McIntyre C.C., Frankenmolle A.M., Wu J., Noecker A.M., Alberts J.L. Customizing deep brain stimulation to the patient using computational models. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009, 2009:4228-4229.
54. Mikos A., Bowers D., Noecker A.M., McIntyre C.C., Won M., Chaturvedi A., Foote K.D., Okun M.S. Patient-specific analysis of the relationship between the volume of tissue activated during DBS and verbal fluency. Neuroimage 2011, 54(Suppl 1):S238-S246.
55. Mink J.W. The basal ganglia: focused selection and inhibition of competing motor programs. Prog. Neurobiol. 1996, 50:381-425.
56. Moran A., Bar-Gad I. Revealing neuronal functional organization through the relation between multi-scale oscillatory extracellular signals. J. Neurosci. Methods 2010, 186:116-129.
57. Moro E., Poon Y.Y., Lozano A.M., Saint-Cyr J.A., Lang A.E. Subthalamic nucleus stimulation: improvements in outcome with reprogramming. Arch. Neurol. 2006, 63:1266-1272.
58. Moro E., Lozano A.M., Pollak P., Agid Y., Rehncrona S., Volkmann J., Kulisevsky J., Obeso J.A., Albanese A., Hariz M.I., et al. Long-term results of a multicenter study on subthalamic and pallidal stimulation in Parkinson's disease. Mov. Disord. 2010, 25:578-586.
59. Nambu A., Tokuno H., Hamada I., Kita H., Imanishi M., Akazawa T., Ikeuchi Y., Hasegawa N. Excitatory cortical inputs to pallidal neurons via the subthalamic nucleus in the monkey. J. Neurophysiol. 2000, 84:289-300.
60. Nise N.S. Design via state space. Control Systems Engineering 2007, 636-690. John Wiley and Sons, Hoboken, NJ.
61. Parush N., Tishby N., Bergman H. Dopaminergic balance between reward maximization and policy complexity. Front Syst Neurosci 2011, 5:22.
62. Popovych O.V., Hauptmann C., Tass P.A. Effective desynchronization by nonlinear delayed feedback. Phys. Rev. Lett. 2005, 94:164102.
63. Raz A., Feingold A., Zelanskaya V., Vaadia E., Bergman H. Neuronal synchronization of tonically active neurons in the striatum of normal and parkinsonian primates. J. Neurophysiol. 1996, 76:2083-2088.
64. Raz A., Vaadia E., Bergman H. Firing patterns and correlations of spontaneous discharge of pallidal neurons in the normal and the tremulous 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine vervet model of parkinsonism. J. Neurosci. 2000, 20:8559-8571.
65. Redmond D.E., Roth R.H., Sladek J.R. MPTP produces classic parkinsonian syndrome in African green monkeys. Soc. Neurosci. Abstr. 1985, 11:166.
66. Rouse A.G., Stanslaski S.R., Cong P., Jensen R.M., Afshar P., Ullestad D., Gupta R., Molnar G.F., Moran D.W., Denison T.J. A chronic generalized bi-directional brain-machine interface. J. Neural Eng. 2011, 8:036018.
67. Stanslaski S., Cong P., Carlson D., Santa W., Jensen R., Molnar G., Marks W.J., Shafquat A., Denison T. An implantable bi-directional brain-machine interface system for chronic neuroprosthesis research. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2009, 2009:5494-5497.
68. Tass P.A. A model of desynchronizing deep brain stimulation with a demand-controlled coordinated reset of neural subpopulations. Biol. Cybern. 2003, 89:81-88.
69. Tass P., Smirnov D., Karavaev A., Barnikol U., Barnikol T., Adamchic I., Hauptmann C., Pawelcyzk N., Maarouf M., Sturm V., et al. The causal relationship between subcortical local field potential oscillations and Parkinsonian resting tremor. J. Neural Eng. 2010, 7:16009.
70. Timmermann L., Gross J., Dirks M., Volkmann J., Freund H.J., Schnitzler A. The cerebral oscillatory network of parkinsonian resting tremor. Brain 2003, 126:199-212.
71. Uhlhaas P.J., Singer W. Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 2006, 52:155-168.
72. Uhlhaas P.J., Singer W. Abnormal neural oscillations and synchrony in schizophrenia. Nat. Rev. Neurosci. 2010, 11:100-113.
73. van Rooden S.M., Colas F., Martínez-Martín P., Visser M., Verbaan D., Marinus J., Chaudhuri R.K., Kok J.N., van Hilten J.J. Clinical subtypes of Parkinson's disease. Mov. Disord. 2011, 26:51-58.
74. Vitek J.L. Mechanisms of deep brain stimulation: excitation or inhibition. Mov. Disord. 2002, 17(Suppl 3):S69-S72.
75. Vitek J.L. Deep brain stimulation: how does it work?. Cleve. Clin. J. Med. 2008, 75(Suppl 2):S59-S65.
76. Volkmann J., Moro E., Pahwa R. Basic algorithms for the programming of deep brain stimulation in Parkinson's disease. Mov. Disord. 2006, 21(Suppl 14):S284-S289.
77. Weaver F.M., Follett K., Stern M., Hur K., Harris C., Marks W.J., Rothlind J., Sagher O., Reda D., Moy C.S., 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. CSP 468 Study Group.
78. Weinberger M., Hutchison W.D., Dostrovsky J.O. Pathological subthalamic nucleus oscillations in PD: can they be the cause of bradykinesia and akinesia?. Exp. Neurol. 2009, 219:58-61.
79. Wichmann T., DeLong M.R. Basal ganglia discharge abnormalities in Parkinson's disease. J. Neural Transm. Suppl. 2006, 21-25.
80. Zaidel A., Arkadir D., Israel Z., Bergman H. Akineto-rigid vs. tremor syndromes in Parkinsonism. Curr. Opin. Neurol. 2009, 22:387-393.