Desynchronizing the abnormally synchronized neural activity in the subthalamic nucleus: A modeling study

Expert Review of Medical Devices

Volumn 4, Issue 5, 2007, Pages 633-650

  Hauptmann, Christian ^a   Popovych, Oleksandr ^a   Tass, Peter A ^a,b,c  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

^b UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^c Brain Imaging Center West   (Germany)

Author keywords

Deep brain stimulation; Delayed feedback; Microscopic modeling; Parkinsonian disease

Indexed keywords

BRAIN CORTEX; BRAIN DEPTH STIMULATION; BRAIN NERVE CELL; CELL POPULATION; CONFERENCE PAPER; CORTICAL SYNCHRONIZATION; ELECTRIC POTENTIAL; EXCITATORY POSTSYNAPTIC POTENTIAL; FEEDBACK SYSTEM; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERMETHOD COMPARISON; MATHEMATICAL MODEL; NERVE CELL INHIBITION; NEUROPATHOLOGY; PARKINSON DISEASE; QUANTITATIVE ANALYSIS; SUBTHALAMIC NUCLEUS;

DEEP BRAIN STIMULATION; ELECTRIC STIMULATION; HUMANS; MODELS, NEUROLOGICAL; NEURONS; PARKINSON DISEASE; SUBTHALAMIC NUCLEUS;

PARKINSONIA;

EID: 34848872496     PISSN: 17434440     EISSN: 17452422     Source Type: Journal    
DOI: 10.1586/17434440.4.5.633     Document Type: Conference Paper

References (84)

1. Nini A, Feingold A, Slovin H, Bergmann H. Neurons in the globus pallidus do not show correlated activity in the normal monkey, but phase-locked oscillations appear in the MPTP model of parkinsonism. J. Neurophysiol. 74, 1800-1805 (1995).
2. Brown P, Oliviero, A, Mazzone P, Insola A, Tonali P, Di Lazzaro V. Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson's disease. J. Neurosci. 21, 1033-1038 (2001).
3. Hutchison WD, Lozano AM, Tasker RR, Lang AE, Dostrovsky JO. Identification and characterization of neurons with tremor-frequency activity in human globus pallidus. Exp. Brain Res. 113, 557-563 (1997).
4. Hurtado JM, Gray CM, Tamas LB, Sigvardt KA. Dynamics of tremor-related oscillations in the human globus pallidus: a single case study. Proc. Natl Acad. Sci. USA 96, 1674-1679 (1999).
5. Magill PJ, Bolam JP, Bevan MD. Dopamine regulates the impact of the cerebral cortex on the subthalamic nucleus-globus pallidus network. Neuroscience 106(2), 313-320 (2001).
6. Trottenberg T, Kupsch A, Schneider GH, Brown P, Kuehn AA. Frequency-dependent distribution of local field potential activity within the subthalamic nucleus in Parkinson's disease. Exp. Neurol. 205, 287-291 (2007).
7. Benabid AL, Pollak P, Gervason C et al. Longterm suppression of tremor by chronic stimulation of ventral intermediate thalamic nucleus. Lancet 337, 403-406 (1991).
8. Blond S, Caparros-Lefebvre D, Parker F et al. Control of tremor and involuntary movement disorders by chronic stereotactic stimulation of the ventral intermediate thalamic nucleus. J. Neurosurg. 77, 62-68 (1992).
9. Benabid AL, Benazzous A, Pollak P. Mechanisms of deep brain stimulation. Mov. Disord. 17, 73-74 (2002).
10. Benabid A-L, Wallace B, Mitrofanis J et al. A putative gerneralized model of the effects and mechanism of action of high frequency electrical stimulation of the central nervous system. Acta Neurol. Belg. 105, 149-157 (2005).
11. Beurrier C, Garcia L, Bioulac B, Hammond C. Subthalamic nucleus: a clock inside basal ganglia? Thalamus Relat. Syst. 2, 1-8 (2002).
12. Beurrier C, Bioulac B, Audin J, Hammond C. High-frequency stimulation produces a transient blockade of voltage-gated currents in subthalamic neurons. J. Neurophysiol. 85(4), 1351-1356 (2001).
13. Grill WM, McIntyre CC. Extracellular excitation of central neurons: implications for the mechanisms of deep brain stimulation. Thalamus Relat. Syst. 1, 269-277 (2001).
14. Lenz FA, Kwan HC, Martin RL, Tasker RR, Dostrovsky JO, Lenz YE. Single unit analysis of the human ventral thalamic nuclear group. Tremor-related activity in functionally identified cells. Brain 117, 531-543 (1994).
15. Shen K, Zhu Z, Munhall A, Johnson SW. Synaptic plasticity in rat subthalamic nucleus induced by high-frequency stimulation. Synapse 50, 314-319 (2003).
16. Hashimoto T, Elder CM, Okun MS, Patrick SK, Vitek JL. Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons. J. Neurosci. 23(5), 1916-1923 (2003).
17. Garcia L, D'Alessandro G, Fernagut PO, Bioulac B. Hammond C. Impact of high-frequency stimulation parameters on the pattern of discharge of subthalamic neurons. J. Neurophysiol. 94, 3662-3669 (2005).
18. McIntyre CC, Grill WM, Sherman DL, Thakor NV. Cellular effects of deep brain stimulation: model-based analysis of activation and inhibition. J. Neurophysiol. 91, 1457-1469 (2004).
19. Rubin D, Terman J. High frequency stimulation of the subthalamic nucleus eliminates pathological thalamic rhythmicity in a computational model. J. Comput. Neurosci. 16, 211-235 (2004).
20. Miocinovic S, Parent M, Butson CR et al. Computational analysis of subthalamic nucleus and lenticular fasciculus activation during therapeutic deep brain stimulation. J. Neurophysiol. 96, 1569-1580 (2006).
21. Tasker RR. Deep brain stimulation is preferable to thalamotomy for tremor suppression. Surg. Neurol. 49, 145-154 (1998).
22. Schuurman PR, Bosch DA, Bossuyt PM et al. A comparison of continuous thalamic stimulation and thalamotomy for suppression of severe tremor. N. Engl. J. Med. 342, 461-468 (2000).
23. Volkmann J. Deep brain stimulation for the treatment of Parkinson's disease. J. Clin. Neurophysiol. 21, 6-17 (2004).
24. Rodriguez-Oroz M, Obeso J, Lang A et al. Bilateral deep brain stimulation in Parkinson's disease: a multicentre study with 4 years follow-up. Brain 128, 2240-2249 (2005).
25. Deuschl G, Schade-Brittinger C, Krack P et al. A randomized trial of deep-brain stimulation for Parkinson's disease. N. Engl. J. Med. 355, 896-908 (2006).
26. Tass PA. Phase Resetting in Medicine and Biology. Springer Veriag, NY, USA (1999).
27. Tass PA. Desynchronization of brain rhythms with soft phase-resetting techniques. Biol. Cybern. 87, 102-115 (2002).
28. Tass PA. Effective desynchronization with bipolar double-pulse stimulation. Phys. Rev. E 66, 036226 (2002).
29. Tass PA. A model of desynchronizing deep brain stimulation with a demand-controlled coordinated reset of neural subpopulations. Biol. Cybern. 89, 81-88 (2003).
30. Tass PA, Hauptmann C, Popovych O. Development of therapeutic brain stimulation techniques with methods from nonlinear dynamics and statistical physics. Int. J. Bifurcat. Chaos 16(7), 1889-1911 (2006).
31. Hauptmann C, Tass PA. Therapeutic rewiring by means of desynchronizing brain stimulation. Biosystems 89, 173-181 (2007).
32. Hauptmann C, Popovych O, Tass PA. Delayed feedback control of synchronization in locally coupled neuronal networks. Neurocomputing 65-66, 759-767 (2005).
33. Hauptmann C, Popovych O, Tass PA. Effectively desynchronizing deep brain stimulation based on a coordinated delayed feedback stimulation via several sites. Biol. Cybern. 93, 463-470 (2005).
34. Hauptmann C, Popovych O, Tass PA. Multisite coordinated delayed feedback for an effective desynchronization of neuronal networks. Stochastics Dynamics 5(2), 307-319 (2005).
35. Popovych O, Hauptmann C, Tass PA. Effective desynchronization by nonlinear delayed feedback. Phys. Rev. Lett. 94, 164102-164105 (2005).
36. Popovych O, Hauptmann C, Tass PA. Control of neuronal synchrony by nonlinear delayed feedback. Biol. Cybern. 95, 69-85 (2006).
37. Popovych O, Hauptmann C, Tass PA. Desynchronization and decoupling of interacting oscillators by nonlinear delayed feedback. Int, J. Bifurcat. Chaos 16(7), 1977-1987 (2006).
38. Haken H. Advanced Synergeacs. Springer, Berlin, Germany (1983).
39. Ranck JB. Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res. 98, 417-440 (1975).
40. McIntyre CC, Grill WM. Excitation of central nervous system neurons by nonuniform electric fields. Biophysical J. 76, 878-888 (1999).
41. Nowak LG, Bullier J. Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. I. Evidence from chronaxie measurements. Exp. Brain Res. 118, 477-488 (1998).
42. Nowak LG, Bullier J. Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. II. Evidence from selective inactivation of cell bodies and axon initial segments. Exp. Brain Res. 118, 489-500 (1998).
43. Morris C, Lecar H. Voltage oscillations in the barnacle giant muscle fiber. Biophysical J. 35, 193-213 (1981).
44. Rinzel J, Ermentrout GB. Analysis of Neural Excitability and Oscillations. In: Methods in Neuronal Modelling from Synapses to Networks. Koch CH, Segev I (Eds). MIT Press, MA, USA 135-169 (1989).
45. Hodgkin A, Huxley AF. A quantitative description of membrane current and application to conduction and excitation. J. Physiol. 117, 500-544 (1952).
46. Hauptmann C, Mackey MC. Stimulus dependent onset latency of the inhibitory recurrent activity. Biol. Cybern. 88, 459-467 (2003).
47. Luhmann HJ, Mudrick-Donnon LA, Mittmann T, Heinemann U. Ischaemia-induced long-term hyperexcitability in rat neocortex. Eur J. Neurosci. 7, 180-191 (1995).
48. Zirh TA, Lenz FA, Reich SG, Dougherty PM. Patterns of bursting occurring in thalamic cells during parkinsonian tremor. Neuroscience 83, 107-121 (1998).
49. Kitai ST, Kita H. Anatomy and physiology of the subthalamic nucleus: a driving force of the basal ganglia. In: The Basal Ganglia II: Structure and Function: Current Concepts. Plenum, NY, USA 357-373 (1987).
50. Wichmann T, Bergman H, Starr PA, Subramanian T, Watts RL, DeLong MR. Comparison of MPTP-induced changes in spontaneous neuronal discharge in the internal pallidal segment and in the substantia nigra pars reticulata in primates. Exp. Brain Res. 125, 397-409 (1999).
51. Bolam JP, Hanley JJ, Booth PAC, Bevan MD. Synaptic organisation of the basal ganglia. J. Anat. 196, 527-542 (2000).
52. Hamani C, Saint-Cyr JA, Fraser J, Kaplitt M, Lozano AM. The subthalamic nucleus in the context of movement disorders. Brain 127, 4-20 (2004).
53. Dolan K, Witt A, Spano ML, Neiman A, Moss F. Surrogates for finding unstable periodic orbits in noisy data sets. Phys. Rev E 59, 5235-5241 (1999).
54. Levesque J-C, Parent A. GABAergic interneurons in human subthamic nucleus. Mov. Disord. 20, 574-584 (2005).
55. Kita H, Chang HT, Kitai ST. The morphology of intracellularly labeled rat subthalamic neurons: a light microscopic analysis. J. Comp. Neurol. 215, 245-257 (1983).
56. Sato F, Parent M, Levesque M, Parent A. Axonal branching pattern of neurons of the subthalamic nucleus in primates. J. Comp. Neurol. 424, 142-152 (2000).
57. Humphries MD, Gurney KN. A pulsed neural network model of bursting in the basal ganglia. Neural Netw. 14, 845-863 (2001).
58. Gillies A, Willshaw D. Models of the subthalamic nucleus - the importance of intranuclear connectivity. Med. Eng. Phys. 26, 723-732 (2004).
59. Wilson CL, Puntis M, Lacey MG. Overwhelmingly asynchronous firing of rat subthalamic nucleus neurons in brain slices provides little evidence for intrinsic interconnectivity. Neuroscience 123, 187-200 (2004).
60. Terman D, Rubin JE, Yew AC, Wilson CJ. Activity patterns in a model for the subthalamopallidal network of the basal ganglia. J. Neurosci. 22, 2963-2976 (2002).
61. Beurrier C, Congar P, Bioulac B, Hammond C. Subthalamic nucleus neurons switch from single-spike activity to burst-firing mode. J. Neurosci. 19(2), 599-609 (1999).
62. Traub RD, Miles R. Neural Networks of the Hippocampus. Cambridge University Press, Cambridge, UK (1991).
63. Hellwig B. A quantitative analysis of the local connectivity between pyramidal neurons in layers 2/3 of the rat visual cortex. Biol. Cybern. 82, 111-121 (2000).
64. Nunez PL. Electric Fields of the Brain. Oxford University Press, NY, USA (1981).
65. Hairer E, Norsett SP, Wanner G. Solving Ordinary Differential Equations I. Springer Verlag, NY, USA (1987).
66. Kuramoto Y. Chemical Oscillations, Waves, and Turbulence. Springer Berlin Heidelberg, NY, USA (1984).
67. Pinsky PF, Rinzel J. Synchrony measures for biological neural networks. Biol. Cybern. 73, 129-137 (1995).
68. Bevan MD, Wilson CJ. Mechanisms underlying spontaneous oscillation and rhythmic firing in rat subthalamic neurons. J. Neurosci. 19, 7617-7628 (1999).
69. Tass PA. Stochastic phase resetting of two coupled phase oscillators stimulated at different times. Phys. Rev. E 67, 051902 (2003).
70. Best EN. Null space in the Hodgkin-Huxley equations: a critical test. Biophysical J. 27, 87-104 (1979).
71. Guttmann R, Lewis S, Rinzel J. Control of repetitive firing in squid axon membrane as a model for a neurone oscillator. J. Physiol. (Lond.) 305, 377-395 (1980).
72. Tricas TC, New JG. Sensitivity and response dynamics of elasmobranch electrosensory primary afferent neurons to near threshold fields. J. Comp. Pbysiol. A 182, 89-101 (1998).
73. Richardson KA, Gluckman BJ, Weinstein SL. In vivo modulation of hippocampal epileptiform activity with radial electric fields. Epilepsia 44, 768-777 (2003).
74. Rosenblum MG, Pikovsky AS. Controlling synchronization in an ensemble of globally coupled oscillators. Phys. Rev. Lett. 92, 114102 (2004).
75. Kiss ZHT, Mooney DM, Renaud L, Hu.B. Neuronal response to local electrical stimulation in rat thalamus: physiological implications for mechanisms of deep brain stimulation. Neuroscience 113, 137-143 (2002).
76. Neiman AB, Russel DF, Yakusheva TA, DiLullo A, Tass PA. Response clustering intransient stochastic synchronization and desynchronization of coupled neuronal bursters. Phys. Rev. E 76, 021908 (2007).
77. Berns GS, Sejnowski TJ. A computational model of how the basal ganglia produce sequences. J. Cogn. Neurosci. 10, 108-121 (1998).
78. Niktarash AH, Shahidi GA. Effects of the activity of the internal globus pallidus-pedunculopontine loop on the transmission of the subthalamic nucleus-external globus pallidus-pacemaker oscillatory activities to the cortex. J. Comput. Neurosci. 16, 113-127 (2004).
79. Tass PA, Majtanik M. Long-term anti-kindling effects of desynchronizing brain stimulation: a theoretical study. Biol. Cybern. 94, 58-66 (2006).
80. Tass PA, Hauptmann C. Therapeutic rewiring by means of desynchronizing brain stimulation. Nonlinear Phenom. Complex Systems 9(3), 298-312 (2006).
81. Levy R, Hutchison WD, Lozano AM, Dostrovsky JO. Synchronized neuronal discharge in the basal ganglia of parkinsonian patients is limited to oscillatory activity. J. Neurosci. 22(7), 2855-2861 (2002).
82. Freund H-J, Barnikol UB, Nolte D et al. Subthalamic-thalamic dbs in a case with spinocerebellar ataxia type 2 (SCA2) and severe tremor - unusual clinical benefit. Mov. Disord. 22(5), 732-735 (2006).
83. Pirker W, Back C, Gerschlager W, Laccone F, Alesch F. Chronic thalamic stimulation in a patient with spinocerebellar ataxia type 2. Mov. Disord. 18, 222-225 (2003).
84. Jones EG. The Thalamus. Plenum Press, NY, USA (1985).