Control of abnormal synchronization in neurological disorders

Frontiers in Neurology

Volumn 5, Issue DEC, 2014, Pages

  Popovych, Oleksandr V ^a   Tass, Peter A ^a,b,c  

^a FORSCHUNGSZENTRUM JÜLICH   (Germany)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Anti kindling; Coordinated reset neuromodulation; Electrical stimulation; Neuronal synchronization; Noise stimulation; Sensory stimulation; Spike timing dependent plasticity

Indexed keywords

AUDITORY STIMULATION; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; CELL POPULATION; CELL SYNCHRONIZATION; CONNECTOME; COORDINATED RESET NEUROMODULATION; HUMAN; INTERMETHOD COMPARISON; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE CONDUCTION; NERVOUS SYSTEM PARAMETERS; NEUROLOGIC DISEASE; NEURONAL SYNCHRONIZATION; NONHUMAN; REVIEW; SPIKE TIMING DEPENDENT PLASTICITY;

EID: 84920860952     PISSN: None     EISSN: 16642295     Source Type: Journal    
DOI: 10.3389/fneur.2014.00268     Document Type: Review

References (147)

1. 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 (1994) 117:531-43. doi: 10.1093/brain/117.3.531
2. 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 (1995) 74:1800-5.
3. Mormann F, Lehnertz K, David P, Elger CE. Mean phase coherence as a measure for phase synchronization and its application to the EEG of epilepsy patients. Physica D (2000) 144:358-69. doi:10.1016/j.clinph.2013.09.047
4. da Silva FHL, Blanes W, Kalitzin SN, Parra J, Suffczynski P, Velis DN. Dynamical diseases of brain systems: different routes to epileptic seizures. IEEE Trans Biomed Eng (2003) 50:540-8. doi:10.1109/TBME.2003.810703
5. Weisz N, Moratti S, Meinzer M, Dohrmann K, Elbert T. Tinnitus perception and distress is related to abnormal spontaneous brain activity as measured by magnetoencephalography. PLoS Med (2005) 2(6):e153. doi:10.1371/journal.pmed.0020153
6. Weisz N, Muller S, Schlee W, Dohrmann K, Hartmann T, Elbert T. The neural code of auditory phantom perception. J Neurosci (2007) 27:1479-84. doi:10.1523/JNEUROSCI.3711-06.2007
7. Hammond C, Bergman H, Brown P. Pathological synchronization in Parkinson's disease: networks, models and treatments. Trends Neurosci (2007) 30:357-64. doi:10.1016/j.tins.2007.05.004
8. Kane A, Hutchison WD, Hodaie M, Lozano AM, Dostrovsky JO. Enhanced synchronization of thalamic theta band local field potentials in patients with essential tremor. Exp Neurol (2009) 217:171-6. doi:10.1016/j.expneurol.2009.02.005
9. Schnitzler A, Munks C, Butz M, Timmermann L, Gross J. Synchronized brain network associated with essential tremor as revealed by magnetoencephalography. Mov Disord (2009) 24:1629-35. doi:10.1002/mds.22633
10. Roberts LE, Eggermont JJ, Caspary DM, Shore SE, Melcher JR, Kaltenbach JA. Ringing ears: the neuroscience of tinnitus. J Neurosci (2010) 30:14972-9. doi:10.1523/JNEUROSCI.4028-10.2010
11. Levy R, Hutchison WD, Lozano AM, Dostrovsky JO. High-frequency synchronization of neuronal activity in the subthalamic nucleus of parkinsonian patients with limb tremor. J Neurosci (2000) 20:7766-75.
12. Levy R, Ashby P, Hutchison WD, Lang AE, Lozano AM, Dostrovsky JO. Dependence of subthalamic nucleus oscillations on movement and dopamine in Parkinson's disease. Brain (2002) 125:1196-209. doi:10.1093/brain/awf128
13. Kühn AA, Kupsch A, Schneider GH, Brown P. Reduction in subthalamic 8-35 hz oscillatory activity correlates with clinical improvement in Parkinson's disease. Eur J Neurosci (2006) 23:1956-60. doi:10.1111/j.1460-9568.2006.04717.x
14. Kühn AA, Tsui A, Aziz T, Ray N, Brücke 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) 215:380-7. doi:10.1016/j.expneurol.2008.11.008
15. Jenkinson N, Brown P. New insights into the relationship between dopamine, beta oscillations and motor function. Trends Neurosci (2011) 34:611-8. doi:10.1016/j.tins.2011.09.003
16. Wilson CL, Puntis M, Lacey MG. Overwhelmingly asynchronous firing of rat subthalamic nucleus neurones in brain slices provides little evidence for intrinsic interconnectivity. Neuroscience (2004) 123:187-200. doi:10.1016/j.neuroscience.2003.09.008
17. Moro E, Esselink RJA, Xie J, Hommel M, Benabid AL, Pollak P. The impact on Parkinson's disease of electrical parameter settings in STN stimulation. Neurology (2002) 59:706-13. doi:10.1212/WNL.59.5.706
18. Timmermann L, Wojtecki L, Gross J, Lehrke R, Voges J, Maarouf M, et al. Ten-Hertz stimulation of subthalamic nucleus deteriorates motor symptoms in Parkinson's disease. Mov Disord (2004) 19:1328-33. doi:10.1002/mds.20198
19. Eusebio A, Chen CC, Lu CS, Lee ST, Tsai CH, Limousin P, et al. Effects of low-frequency stimulation of the subthalamic nucleus on movement in Parkinson's disease. Exp Neurol (2008) 209:125-30. doi:10.1016/j.expneurol.2007.09.007
20. Barnikol UB, Popovych OV, Hauptmann C, Sturm V, Freund HJ, Tass PA. Tremor entrainment by patterned low-frequency stimulation. Phil Trans R Soc A (2008) 366:3545-73. doi:10.1098/rsta.2008.0104
21. Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K. Optical deconstruction of parkinsonian neural circuitry. Science (2009) 324:354-9. doi:10.1126/science.1167093
22. Chen CC, Lin WY, Chan HL, Hsu YT, Tu PH, Lee ST, et al. Stimulation of the subthalamic region at 20 hz slows the development of grip force in Parkinson's disease. Exp Neurol (2011) 231:91-6. doi:10.1016/j.expneurol.2011.05.018
23. Seki S, Eggermont JJ. Changes in spontaneous firing rate and neural synchrony in cat primary auditory cortex after localized tone-induced hearing loss. Hear Res (2003) 180:28-38. doi:10.1016/S0378-5955(03)00074-1
24. Eggermont JJ. Correlated neural activity as the driving force for functional changes in auditory cortex. Hear Res (2007) 229:69-80. doi:10.1016/j.heares.2007.01.008
25. Dohrmann K, Elbert T, Schlee W, Weisz N. Tuning the tinnitus percept by modification of synchronous brain activity. Restor Neurol Neurosci (2007) 25:371-8.
26. Silchenko AN, Adamchic I, Hauptmann C, Tass PA. Impact of acoustic coordinated reset neuromodulation on effective connectivity in a neural network of phantom sound. Neuroimage (2013) 77:133-47. doi:10.1016/j.neuroimage.2013.03.013
27. Adamchic I, Toth T, Hauptmann C, Tass PA. Reversing pathologically increased EEG power by acoustic coordinated reset neuromodulation. Hum Brain Mapp (2014) 35:2099-118. doi:10.1002/hbm.22314
28. Lorenz I, Muller N, Schlee W, Hartmann T, Weisz N. Loss of alpha power is related to increased gamma synchronization - a marker of reduced inhibition in tinnitus? Neurosci Lett (2009) 453:225-8. doi:10.1016/j.neulet.2009.02.028
29. Tass PA, Adamchic I, Freund HJ, von Stackelberg T, Hauptmann C. Counteracting tinnitus by acoustic coordinated reset neuromodulation. Restor Neurol Neurosci (2012) 30:137-59. doi:10.3233/RNN-2012-110218
30. Benabid AL, Pollak P, Gervason C, Hoffmann D, Gao DM, Hommel M, et al. Longterm suppression of tremor by chronic stimulation of ventral intermediate thalamic nucleus. Lancet (1991) 337:403-6. doi:10.1016/0140-6736(91)91175-T
31. Kringelbach ML, Jenkinson N, Owen SLF, Aziz TZ. Translational principles of deep brain stimulation. Nat Rev Neurosci (2007) 8:623-35. doi:10.1038/nrn2196
32. Wu C, Sharan AD. Neurostimulation for the treatment of epilepsy: a review of current surgical interventions. Neuromodulation (2013) 16:10-24. doi:10.1111/j.1525-1403.2012.00501.x
33. McIntyre CC, Grill WM, Sherman DL, Thakor NV. Cellular effects of deep brain stimulation: model-based analysis of activation and inhibition. J Neurophysiol (2004) 91:1457-69. doi:10.1152/jn.00989.2003
34. Benabid AL, Benazzous A, Pollak P. Mechanisms of deep brain stimulation. Mov Disord (2002) 17:S73-4. doi:10.1002/mds.10145
35. Welter ML, Houeto JL, Bonnet AM, Bejjani PB, Mesnage V, Dormont D, et al. Effects of high-frequency stimulation on subthalamic neuronal activity in parkinsonian patients. Arch Neurol (2004) 61:89-96. doi:10.1001/archneur.61.1.89
36. Meissner W, Leblois A, Hansel D, Bioulac B, Gross CE, Benazzouz A, et al. Subthalamic high frequency stimulation resets subthalamic firing and reduces abnormal oscillations. Brain (2005) 128:2372-82. doi:10.1093/brain/awh616
37. Dostrovsky JO, Levy R, Wu JP, Hutchison WD, Tasker RR, Lozano AM. Microstimulation-induced inhibition of neuronal firing in human globus pallidus. J Neurophysiol (2000) 84:570-4.
38. Benazzouz A, Gao DM, Ni ZG, Piallat B, Bouali-Benazzouz R, Benabid AL. Effect of high-frequency stimulation of the subthalamic nucleus on the neuronal activities of the substantia nigra pars reticulata and ventrolateral nucleus of the thalamus in the rat. Neuroscience (2000) 99:289-95. doi:10.1016/S0306-4522(00)00199-8
39. Beurrier C, Bioulac B, Audin J, Hammond C. High-frequency stimulation produces a transient blockade of voltage-gated currents in subthalamic neurons. J Neurophysiol (2001) 85:1351-6.
40. Hammond C, Ammari R, Bioulac B, Garcia L. Latest view on the mechanism of action of deep brain stimulation. Mov Disord (2008) 23:2111-21. doi:10.1002/mds.22120
41. Hashimoto T, Elder CM, Okun MS, Patrick SK, Vitek JL. Stimulation of the subthalamic nucleus changes the firing pattern of pallidal neurons. J Neurosci (2003) 23:1916-23.
42. Rubin JE, Terman D. High frequency stimulation of the subthalamic nucleus eliminates pathological thalamic rhythmicity in a computational model. J Comput Neurosci (2004) 16:211-35. doi:10.1023/B:JCNS.0000025686.47117.67
43. Miocinovic S, Parent M, Butson CR, Hahn PJ, Russo GS, Vitek JL, et al. Computational analysis of subthalamic nucleus and lenticular fasciculus activation during therapeutic deep brain stimulation. J Neurophysiol (2006) 96:1569-80. doi:10.1152/jn.00305.2006
44. Anderson ME, Postupna N, Ruffo M. Effects of high-frequency stimulation in the internal globus pallidus on the activity of thalamic neurons in the awake monkey. J Neurophysiol (2003) 89:1150-60. doi:10.1152/jn.00475.2002
45. McIntyre CC, Savasta M, Goff LKL, Vitek JL. Uncovering the mechanism(s) of action of deep brain stimulation: activation, inhibition, or both. Clin Neurophysiol (2004) 115:1239-48. doi:10.1016/j.clinph.2003.12.024
46. Benabid AL, Wallace B, Mitrofanis J, Xia R, Piallat B, Chabardes S, et al. A putative generalized model of the effects and mechanism of action of high frequency electrical stimulation of the central nervous system. Acta Neurol Belg (2005) 105:149-57.
47. Brown P, Mazzone P, Oliviero A, Altibrandi MG, Pilato F, Tonali PA, et al. Effects of stimulation of the subthalamic area on oscillatory pallidal activity in Parkinson's disease. Exp Neurol (2004) 188:480-90. doi:10.1016/j.expneurol.2004.05.009
48. Kühn AA, Kempf F, Brücke C, Doyle LG, Martinez-Torres I, Pogosyan A, et al. High-frequency stimulation of the subthalamic nucleus suppresses ß oscillatory activity in patients with Parkinson's disease in parallel with improvement in motor performance. J Neurosci (2008) 28(24):6165-73. doi:10.1523/JNEUROSCI.0282-08.2008
49. Bronte-Stewart H, Barberini C, Koop MM, Hill BC, Henderson JM, Wingeier B. The STN beta-band profile in Parkinson's disease is stationary and shows prolonged attenuation after deep brain stimulation. Exp Neurol (2009) 215:20-8. doi:10.1016/j.expneurol.2008.09.008
50. Eusebio A, Thevathasan W, Gaynor LD, Pogosyan A, Bye E, Foltynie T, et al. Deep brain stimulation can suppress pathological synchronisation in parkinsonian patients. J Neurol Neurosurg Psychiatry (2011) 82:569-73. doi:10.1136/jnnp.2010.217489
51. Wilson CJ, Beverlin B II, Netoff T. Chaotic desynchronization as the therapeutic mechanism of deep brain stimulation. Front Syst Neurosci (2011) 5:50. doi:10.3389/fnsys.2011.00050
52. Popovych OV, Tass PA. Macroscopic entrainment of periodically forced oscillatory ensembles. Prog Biophys Mol Biol (2011) 105:98-108. doi:10.1016/j.pbiomolbio.2010.09.018
53. Hauptmann C, Tass PA. Therapeutic rewiring by means of desynchronizing brain stimulation. Biosystems (2007) 89:173-81. doi:10.1016/j.biosystems.2006.04.015
54. Foffani G, Ardolino G, Egidi M, Caputo E, Bossi B, Priori A. Subthalamic oscillatory activities at beta or higher frequency do not change after high-frequency DBS in Parkinson's disease. Brain Res Bull (2006) 69:123-30. doi:10.1016/j.brainresbull.2005.11.012
55. Priori A, Ardolino G, Marceglia S, Mrakic-Sposta S, Locatelli M, Tamma F, et al. Low-frequency subthalamic oscillations increase after deep brain stimulation in Parkinson's disease. Brain Res Bull (2006) 71:149-54. doi:10.1016/j.brainresbull.2006.08.015
56. Temperli P, Ghika J, Villemure JG, Burkhard P, Bogousslavsky J, Vingerhoets F. How do parkinsonian signs return after discontinuation of subthalamic DBS? Neurology (2003) 60:78-81. doi:10.1212/WNL.60.1.78
57. Welter ML, Schüpbach M, Czernecki V, Karachi C, Fernandez-Vidal S, Golmard JL, et al. Optimal target localization for subthalamic stimulation in patients with Parkinson disease. Neurology (2014) 82:1352-61. doi:10.1212/WNL.0000000000000315
58. Pyragas K, Novicenko V, Tass PA. Mechanism of suppression of sustained neuronal spiking under high-frequency stimulation. Biol Cybern (2013) 107:669-84. doi:10.1007/s00422-013-0567-1
59. Tasker RR. Depp brain stimulation is preferable to thalamotomy for tremor suppression. Surg Neurol (1998) 49:145-54. doi:10.1016/S0090-3019(97)00459-X
60. Volkmann J. Deep brain stimulation for the treatment of Parkinson's disease. J Clin Neurophysiol (2004) 21:6-17. doi:10.1097/00004691-200401000-00003
61. Rodriguez-Oroz MC, Obeso JA, Lang AE, Houeto JL, Pollak P, Rehncrona S, et al. Bilateral deep brain stimulation in Parkinson's disease: a multicentre study with 4 years follow-up. Brain (2005) 128:2240-9. doi:10.1093/brain/awh571
62. Deuschl G, Schade-Brittinger C, Krack P, Volkmann J, Schäfer H, Bötzel K, et al. A randomized trial of deep-brain stimulation for Parkinson's disease. N Engl J Med (2006) 355:896-908. doi:10.1056/NEJMoa060281
63. Tass PA. Phase Resetting in Medicine and Biology: Stochastic Modelling and Data Analysis. Berlin: Springer (1999).
64. Tass PA. Desynchronizing double-pulse phase resetting and application to deep brain stimulation. Biol Cybern (2001) 85:343-54. doi:10.1007/s004220100268
65. Tass PA. Desynchronization of brain rhythms with soft phase-resetting techniques. Biol Cybern (2002) 87:102-15. doi:10.1007/s00422-002-0322-5
66. Tass PA. A model of desynchronizing deep brain stimulation with a demand-controlled coordinated reset of neural subpopulations. Biol Cybern (2003) 89:81-8. doi:10.1007/s00422-003-0425-7
67. Tass PA. Desynchronization by means of a coordinated reset of neural sub-populations - a novel technique for demand-controlled deep brain stimulation. Prog Theor Phys Suppl (2003) 150:281-96. doi:10.1143/PTPS.150.281
68. Rosenblum MG, Pikovsky AS. Controlling synchronization in an ensemble of globally coupled oscillators. Phys Rev Lett (2004) 92:114102. doi:10.1103/PhysRevLett.92.114102
69. Hauptmann C, Popovych O, Tass PA. Effectively desynchronizing deep brain stimulation based on a coordinated delayed feedback stimulation via several sites: a computational study. Biol Cybern (2005) 93:463-70. doi:10.1007/s00422-005-0020-1
70. Popovych OV, Hauptmann C, Tass PA. Effective desynchronization by nonlinear delayed feedback. Phys Rev Lett (2005) 94:164102. doi:10.1103/PhysRevLett.94.164102
71. Kiss IZ, Rusin CG, Kori H, Hudson JL. Engineering complex dynamical structures: sequential patterns and desynchronization. Science (2007) 316:1886-9. doi:10.1126/science.1140858
72. Pyragas K, Popovych OV, Tass PA. Controlling synchrony in oscillatory networks with a separate stimulation-registration setup. Europhys Lett (2007) 80:40002. doi:10.1209/0295-5075/80/40002
73. Tukhlina N, Rosenblum M, Pikovsky A, Kurths J. Feedback suppression of neural synchrony by vanishing stimulation. Phys Rev E Stat Nonlin Soft Matter Phys (2007) 75:011918. doi:10.1103/PhysRevE.75.011918
74. Luo M, Wu YJ, Peng JH. Washout filter aided mean field feedback desynchronization in an ensemble of globally coupled neural oscillators. Biol Cybern (2009) 101:241-6. doi:10.1007/s00422-009-0334-5
75. Danzl P, Hespanha J, Moehlis J. Event-based minimum-time control of oscillatory neuron models. Biol Cybern (2009) 101:387-99. doi:10.1007/s00422-009-0344-3
76. Popovych OV, Tass PA. Synchronization control of interacting oscillatory ensembles by mixed nonlinear delayed feedback. Phys Rev E Stat Nonlin Soft Matter Phys (2010) 82:026204. doi:10.1103/PhysRevE.82.026204
77. Nabi A, Moehlis J. Single input optimal control for globally coupled neuron networks. J Neural Eng (2011) 8:065008. doi:10.1088/1741-2560/8/6/065008
78. Hebb D. The Organization of Behavior: A Neuropsychological Theory. Wiley Book in Clinical Psychology (New York: Wiley) (1949).
79. Gerstner W, Kempter R, van Hemmen JL, Wagner H. A neuronal learning rule for sub-millisecond temporal coding. Nature (1996) 383:76-8. doi:10.1038/383076a0
80. Markram H, Lübke J, Frotscher M, Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science (1997) 275:213-5. doi:10.1126/science.275.5297.213
81. Bi GQ, Poo MM. Synaptic modications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type. J Neurosci (1998) 18:10464-72.
82. Feldman DE. Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron (2000) 27:45-56. doi:10.1016/S0896-6273(00)00008-8
83. Bi GQ. Spatiotemporal specificity of synaptic plasticity: cellular rules and mechanisms. Biol Cybern (2002) 87:319-32. doi:10.1007/s00422-002-0349-7
84. Wittenberg GM, Wang SSH. Malleability of spike-timing-dependent plasticity at the CA3-CA1 synapse. J Neurosci (2006) 26:6610-7. doi:10.1523/JNEUROSCI.5388-05.2006
85. Caporale N, Dan Y. Spike timing-dependent plasticity: a Hebbian learning rule. Annu Rev Neurosci (2008) 31:25-46. doi:10.1146/annurev.neuro.31.060407.125639
86. Nowotny T, Zhigulin VP, Selverston AI, Abarbanel HDI, Rabinovich MI. Enhancement of synchronization in a hybrid neural circuit by spike-timing dependent plasticity. J Neurosci (2003) 23:9776-85.
87. Goddar G. Development of epileptic seizures through brain stimulation at low intensity. Nature (1967) 214:1020-1. doi:10.1038/2141020a0
88. Speckmann E, Elger C. The neurophysiological basis of epileptic activity: a condensed overview. Epilepsy Res Suppl (1991) 2:1-7.
89. Morimoto K, Fahnestock M, Racine RJ. Kindling and status epilepticus models of epilepsy: rewiring the brain. Prog Neurobiol (2004) 73:1-60. doi:10.1016/j.pneurobio.2004.03.009
90. Tass PA, Majtanik M. Long-term anti-kindling effects of desynchronizing brain stimulation: a theoretical study. Biol Cybern (2006) 94:58-66. doi:10.1007/s00422-005-0028-6
91. Tass PA, Hauptmann C. Therapeutic modulation of synaptic connectivity with desynchronizing brain stimulation. Int J Psychophysiol (2007) 64:53-61. doi:10.1016/j.ijpsycho.2006.07.013
92. Hauptmann C, Tass PA. Cumulative and after-effects of short and weak coordinated reset stimulation: a modeling study. J Neural Eng (2009) 6:016004. doi:10.1088/1741-2560/6/1/016004
93. Hauptmann C, Tass PA. Restoration of segregated, physiological neuronal connectivity by desynchronizing stimulation. J Neural Eng (2010) 7:056008. doi:10.1088/1741-2560/7/5/056008
94. Tass PA, Popovych OV. Unlearning tinnitus-related cerebral synchrony with acoustic coordinated reset stimulation: theoretical concept and modelling. Biol Cybern (2012) 106:27-36. doi:10.1007/s00422-012-0479-5
95. Popovych OV, Tass PA. Desynchronizing electrical and sensory coordinated reset neuromodulation. Front Hum Neurosci (2012) 6:58. doi:10.3389/fnhum.2012.00058
96. Best EN. Null space in the Hodgkin-Huxley equations: a critical test. Biophys J (1979) 27:87-104. doi:10.1016/S0006-3495(79)85204-2
97. Demir SS, Butera RJ, DeFranceschi AA, Clark JW, Byrne JH. Phase sensitivity end entrainment in a modeled bursting neuron. Biophys J (1997) 72:579-94. doi:10.1016/S0006-3495(97)78697-1
98. Tateno T, Robinson HPC. Phase resetting curves and oscillatory stability in interneurons of rat somatosensory cortex. Biophys J (2007) 92:683-95. doi:10.1529/biophysj.106.088021
99. Neiman A, Russell D, Yakusheva T, DiLullo A, Tass PA. Response clustering in transient stochastic synchronization and desynchronization of coupled neuronal bursters. Phys Rev E Stat Nonlin Soft Matter Phys (2007) 76:021908. doi:10.1103/PhysRevE.76.021908
100. Perkel DH, Schulman JH, Segundo JP, Bullock TH, Moore GP. Pacemaker neurons - effects of regularly spaced synaptic input. Science (1964) 145:61-3. doi:10.1126/science.145.3627.61
101. Pinsker HM. Aplysia bursting neurons as endogenous oscillators.1. phase-response curves for pulsed inhibitory synaptic input. J Neurophysiol (1977) 40:527-43.
102. Lerma J, Garcia-Austt E. Hippocampal theta rhythm during paradoxical sleep - effects of afferent stimuli and phase-relationships with phasic events. Electroencephalogr Clin Neurophysiol (1985) 60:46-54. doi:10.1016/0013-4694(85)90950-2
103. Jackson A, Spinks RL, Freeman TCB, Wolpert DM, Lemon RN. Rhythm generation in monkey motor cortex explored using pyramidal tract stimulation. J Physiol (2002) 541:685-99. doi:10.1113/jphysiol.2001.015099
104. Prinz AA, Thirumalai V, Marder E. The functional consequences of changes in the strength and duration of synaptic inputs to oscillatory neurons. J Neurosci (2003) 23:943-54.
105. Givens B. Stimulus-evoked resetting of the dentate theta rhythm: relation to working memory. Neuroreport (1996) 8:159-63. doi:10.1097/00001756-199612200-00032
106. Makeig S, Westerfield M, Jung TP, Enghoff S, Townsend J, Courchesne E, et al. Dynamic brain sources of visual evoked responses. Science (2002) 295:690-4. doi:10.1126/science.1066168
107. Jansen BH, Agarwal G, Hegde A, Boutros NN. Phase synchronization of the ongoing EEG and auditory EP generation. Clin Neurophysiol (2003) 114:79-85. doi:10.1016/S1388-2457(02)00327-9
108. Ross B, Herdman AT, Pantev C. Stimulus induced desynchronization of human auditory 40-hz steady-state responses. J Neurophysiol (2005) 94:4082-93. doi:10.1152/jn.00469.2005
109. Van der Werf YD, Paus T. The neural response to transcranial magnetic stimulation of the human motor cortex. I. Intracortical and cortico-cortical contributions. Exp Brain Res (2006) 175:231-45. doi:10.1007/s00221-006-0551-2
110. Tass PA, Silchenko AN, Hauptmann C, Barnikol UB, Speckmann EJ. Long-lasting desynchronization in rat hippocampal slice induced by coordinated reset stimulation. Phys Rev E Stat Nonlin Soft Matter Phys (2009) 80:011902. doi:10.1103/PhysRevE.80.011902
111. Tass PA, Qin L, Hauptmann C, Doveros S, Bezard E, Boraud T, et al. Coordinated reset has sustained aftereffects in parkinsonian monkeys. Ann Neurol (2012) 72:816-20. doi:10.1002/ana.23663
112. Adamchic I, Hauptmann C, Barnikol UB, Pawelczyk N, Popovych O, Barnikol TT, et al. Coordinated reset neuromodulation for Parkinson's disease: proof-of-concept study. Mov Disord (2014) 29:1679-84. doi:10.1002/mds.25923
113. Hodgkin A, Huxley AF. A quantitative description of membrane current and application to conduction and excitation. J Physiol (1952) 117:500-44.
114. Hansel D, Mato G, Meunier C. Phase dynamics of weakly coupled Hodgkin-Huxley neurons. Europhys Lett (1993) 23:367-72. doi:10.1209/0295-5075/23/5/011
115. Kalitzin S, van Dijk BW, Spekreijse H. Self-organized dynamics in plastic neural networks: bistability and coherence. Biol Cybern (2000) 83:139-50. doi:10.1007/s004220000157
116. Maistrenko YL, Lysyansky B, Hauptmann C, Burylko O, Tass PA. Multistability in the Kuramoto model with synaptic plasticity. Phys Rev E Stat Nonlin Soft Matter Phys (2007) 75:066207. doi:10.1103/PhysRevE.75.066207
117. Brette R, Gerstner W. Adaptive exponential integrate-and-fire model as an effective description of neuronal activity. J Neurophysiol (2005) 94:3637-42. doi:10.1152/jn.00686.2005
118. Touboul J, Brette R. Dynamics and bifurcations of the adaptive exponential integrate-and-fire model. Biol Cybern (2008) 99:319-34. doi:10.1007/s00422-008-0267-4
119. Naud R, Marcille N, Clopath C, Gerstner W. Firing patterns in the adaptive exponential integrate-and-fire model. Biol Cybern (2008) 99:335-47. doi:10.1007/s00422-008-0264-7
120. Kuramoto Y. Chemical Oscillations, Waves, and Turbulence. Berlin: Springer (1984).
121. Pikovsky A, Rosenblum M, Kurths J. Synchronization, A Universal Concept in Nonlinear Sciences. Cambridge: Cambridge University Press (2001).
122. Lysyansky B, Popovych OV, Tass PA. Optimal number of stimulation contacts for coordinated reset neuromodulation. Front Neuroeng (2013) 6:5. doi:10.3389/fneng.2013.00005
123. Lysyansky B, Popovych OV, Tass PA. Desynchronizing anti-resonance effect of m: n on-off coordinated reset stimulation. J Neural Eng (2011) 8:036019. doi:10.1088/1741-2560/8/3/036019
124. Rinzel JA. A formal classification of bursting mechanisms in excitable systems. In: Teramoto E, Yamaguti M, editors. Mathematical Topics in Population Biology, Morphogenesis and Neurosciences, Lecture Notes in Biomathematics 71. New York, NY: Springer-Verlag (1987). p. 267-81.
125. Izhikevich EM. Synchronization of elliptic bursters. SIAM Rev (2001) 43:315-44. doi:10.1137/S0036144500382064
126. Rizzone M, Lanotte M, Bergamasco B, Tavella A, Torre E, Faccani G, et al. Deep brain stimulation of the subthalamic nucleus in Parkinson's disease: effects of variation in stimulation parameters. J Neurol Neurosurg Psychiatry (2001) 71:215-9. doi:10.1136/jnnp.71.2.215
127. Volkmann J, Herzog J, Kopper F, Deuschl G. Introduction to the programming of deep brain stimulators. Mov Disord (2002) 17:S181-7. doi:10.1002/mds.10162
128. Kuncel AM, Grill WM. Selection of stimulus parameters for deep brain stimulation. Clin Neurophysiol (2004) 115:2431-41. doi:10.1016/j.clinph.2004.05.031
129. Popovych OV, Yanchuk S, Tass PA. Self-organized noise resistance of oscillatory neural networks with spike timing-dependent plasticity. Sci Rep (2013) 3:2926. doi:10.1038/srep02926
130. Sakaguchi H. Cooperative phenomena in coupled oscillator systems under external fields. Prog Theor Phys (1988) 79:39-46. doi:10.1143/PTP.79.39
131. Masuda N, Kori H. Formation of feedforward networks and frequency synchrony by spike-timing-dependent plasticity. J Comput Neurosci (2007) 22:327-45. doi:10.1007/s10827-007-0022-1
132. Bayati M, Valizadeh A. Effect of synaptic plasticity on the structure and dynamics of disordered networks of coupled neurons. Phys Rev E Stat Nonlin Soft Matter Phys (2012) 86:011925. doi:10.1103/PhysRevE.86.011925
133. Hobson J, Chisholm E, El Refaie A. Sound therapy (masking) in the management of tinnitus in adults. Cochrane Database Syst Rev (2012) 11:CD006371. doi:10.1002/14651858.CD006371.pub3
134. Linderoth B, Foreman RD. Physiology of spinal cord stimulation: review and update. Neuromodulation (1999) 2:150-64. doi:10.1046/j.1525-1403.1999.00150.x
135. Oakley JC, Prager JP. Spinal cord stimulation - mechanisms of action. Spine (2002) 27:2574-83. doi:10.1097/00007632-200211150-00034
136. Sarnthein J, Stern J, Aufenberg C, Rousson V, Jeanmonod D. Increased EEG power and slowed dominant frequency in patients with neurogenic pain. Brain (2006) 129:55-64. doi:10.1093/brain/awh631
137. Sarnthein J, Jeanmonod D. High thalamocortical theta coherence in patients with neurogenic pain. Neuroimage (2008) 39:1910-7. doi:10.1016/j.neuroimage.2007.10.019
138. Walton KD, Dubois M, Llinas RR. Abnormal thalamocortical activity in patients with complex regional pain syndrome (CRPS) type I. Pain (2010) 150:41-51. doi:10.1016/j.pain.2010.02.023
139. Candy JM, Perry RH, Perry EK, Irving D, Blessed G, Fairbairn AF, et al. Pathological-changes in the nucleus of Meynert in Alzheimer's and Parkinson's diseases. J Neurol Sci (1983) 59:277-89. doi:10.1016/0022-510X(83)90045-X
140. Wolkin A, Sanfilipo M, Wolf AP, Angrist B, Brodie JD, Rotrosen J. Negative symptoms and hypofrontality in chronic-schizophrenia. Arch Gen Psychiatry (1992) 49:959-65. doi:10.1001/archpsyc.1992.01820120047007
141. Salehi A, Lucassen PJ, Pool CW, Gonatas NK, Ravid R, Swaab DF. Decreased neuronal-activity in the nucleus basalis of Meynert in Alzheimer's-disease as suggested by the size of the Golgi-apparatus. Neuroscience (1994) 59:871-80. doi:10.1016/0306-4522(94)90291-7
142. Kishimoto H, Yamada K, Iseki E, Kosaka K, Okoshi T. Brain imaging of affective disorders and schizophrenia. Psychiatry Clin Neurosci (1998) 52:S212-4. doi:10.1111/j.1440-1819.1998.tb03224.x
143. Bearden CE, Hoffman KM, Cannon TD. The neuropsychology and neuroanatomy of bipolar affective disorder: a critical review. Bipolar Disord (2001) 3:106-50. doi:10.1034/j.1399-5618.2001.030302.x
144. Lysyansky B, Popovych OV, Tass PA. Multi-frequency activation of neuronal networks by coordinated reset stimulation. Interface Focus (2011) 1:75-85. doi:10.1098/rsfs.2010.0010
145. Rosin B, Slovik M, Mitelman R, Rivlin-Etzion M, Haber SN, Israel Z, et al. Closed-loop deep brain stimulation is superior in ameliorating parkinsonism. Neuron (2011) 72:370-84. doi:10.1016/j.neuron.2011.08.023
146. 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) 74:449-57. doi:10.1002/ana.23951
147. Lücken L, Yanchuk S, Popovych OV, Tass PA. Desynchronization boost by non-uniform coordinated reset stimulation in ensembles of pulse-coupled neurons. Front Comput Neurosci (2013) 7:63. doi:10.3389/fncom.2013.00063