Abstract
We present nonlinear delayed feedback stimulation as a technique for effective desynchronization. This method is intriguingly robust with respect to system and stimulation parameter variations. We demonstrate its broad applicability by applying it to different generic oscillator networks as well as to a population of bursting neurons. Nonlinear delayed feedback specifically counteracts abnormal interactions and, thus, restores the natural frequencies of the individual oscillatory units. Nevertheless, nonlinear delayed feedback enables to strongly detune the macroscopic frequency of the collective oscillation. We propose nonlinear delayed feedback stimulation for the therapy of neurological diseases characterized by abnormal synchrony.
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Ahissar E (1998) Temporal-code to rate-code conversion by neuronal phase-locked loops. Neural Comput 10:597–650
Ahissar E, Vaadia E (1990) Oscillatory activity of single units in a somatosensory cortex of an awake monkey and their possible role in texture analysis. Proc Natl Acad Sci USA 87:8935–8939
Alberts WW, Wright EJ, Feinstein B (1969) Cortical potentials and parkinsonian tremor. Nature 221:670–672
Atay FM (2003) Distributed delays facilitate amplitude death of coupled oscillators. Phys Rev Lett 91:094101
Atay FM, Jost J, Wende A (2004) Delays, connection topology, and synchronization of coupled chaotic maps. Phys Rev Lett 92:144101
Bellman R, Cooke KL (1963) Differential-difference equations. Academic, New York
Benabid AL, Pollak P, Louveau A, Henry S, de Rougemont J (1987) Combined (thalamotomy and stimulation) stereotactic surgery of the vim thalamic nucleus for bilateral parkinson’s disease. Appl Neurophysiol 50:344–346
Benabid AL, Pollak P, Gervason C, Hoffmann D, Gao DM, Hommel M, Perret JE, de Rougemount J (1991) Longterm suppression of tremor by chronic stimulation of ventral intermediate thalamic nucleus. The Lancet 337:403–406
Benabid AL, Benazzous A, Pollak P (2002) Mechanisms of deep brain stimulation. Mov Disord 17:73–74
Daido H (1997) Order function theory of macroscopic phase-locking in globally and weakly coupled limit-cycle oscillators. Int J Bifurcat Chaos 7(4):807–829
Dolan K, Witt A, Spano ML, Neiman A, Moss F (1999) Surrogates for finding unstable periodic orbits in noisy data sets. Phys Rev E 59:5235–5241
Eckhorn R, Bauer R, Jordan W, Brosch M, Kruse W, Munk M, Reitboeck HJ (1988) Coherent oscillations: a mechanism of feature linking in the visual cortex? Multiple electrode and correlation analyses in the cat. Biol Cybern 60(2):121–130
Ernst U, Pawelzik K, Geisel T (1995) Synchronization induced by temporal delays in pulse-coupled oscillators. Phys Rev Lett 74:1570–1573
Ernst U, Pawelzik K, Geisel T (1998) Delay-induced multistable synchronization of biological oscillators. Phys Rev E 57:2150–2162
Filali M, Hutchison WD, Palter VN, Lozano AM, Dostrovsky JO (2004) Stimulation-induced inhibition of neuronal firing in human subthalamic nucleus. Exp Brain Res 156(3):274–281
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
Gray CM, Singer W (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci USA 86(5):1698–1702
Grill WM, McIntyre CC (2001) Extracellular excitation of central neurons: implications for the mechanisms of deep brain stimulation. Thalamus Relat Syst 1:269–277
Hansel D, Mato G, Meunier C (1993) Phase dynamics of weakly coupled Hodgkin–Huxley neurons. Europhys Lett 23:367–372
Hauptmann C, Mackey MC (2003) Stimulus dependent onset latency of the inhibitory recurrent activity. Biol Cybern 88:459–467
Hauptmann C, Popovych O, Tass PA (2005a) Delayed feedback control of synchronization in locally coupled neuronal networks. Neurocomputing 65–66:759–767
Hauptmann C, Popovych O, Tass PA (2005b) Effectively desynchronizing deep brain stimulation based on a coordinated delayed feedback stimulation via several sites: a computational study. Biol Cybern 93:463–470
Hauptmann C, Popovych O, Tass PA (2005c) Multisite coordinated delayed feedback for an effective desynchronization of neuronal networks. Stochast Dyn 5(2):307–319
Hellwig B (2000) A quantitative analysis of the local connectivity between pyramidal neurons in layers 2/3 of the rat visual cortex. Biol Cybern 82:111–121
Hoppensteadt FC (1997) An introduction to the mathematics of neurons: modeling in the frequency domain. Cambridge University Press, Cambridge
Kim S, Park SH, Ryu CS (1997) Multistability in coupled oscillator systems with time delay. Phys Rev Lett 79:2911–2914
Kumar R, Lozano AM, Sime E, Lang AE (2003) Long-term follow-up of thalamic deep brain stimulation for essential and parkinsonian tremor. Neurology 61(11):1601–1604
Kuramoto Y (1984) Chemical oscillations, waves, and turbulence. Springer, Berlin Heidelberg New York
Kuznetsov YuA (1998) Elements of applied bifurcation theory. Springer, Berlin Heidelberg New York
Lenz FA, Kwan HC, Martin RL, Tasker RR, Dostrovsky JO, Lenz YE (1994) Single unit analysis of the human ventral thalamic nuclear group. Tremor-related activity in functionally identified cells Brain 117:531–543
Luhmann HJ, Mudrick-Donnon LA, Mittmann T, Heinemann U (1995) Ischaemia-induced long-term hyperexcitability in rat neocortex. Eur J Neurosci 7:180–191
Maistrenko Yu, Popovych O, Burylko O, Tass PA (2004) Mechanism of desynchronization in the finite-dimensional Kuramoto model. Phys Rev Lett 93:084102
Matthews PC, Strogatz SH (1990) Phase diagram for the collective behavior of limit-cycle oscillators. Phys Rev Lett 65:1701–1704
McIntyre CC, Grill WM (1999) Excitation of central nervous system neurons by nonuniform electric fields. Biophys J 76:878–888
McIntyre CC, Savasta M, Kerkerian-Le, Goff L, Vitek JL (2004) Uncovering the mechanism(s) of action of deep brain stimulation: activation, inhibition, or both. Clin Neurophysiol 115(6):1239–1248
Meissner W, Leblois A, Hansel D, Bioulac B, Gross CE, Benazzouz A, Boraud T (2005) Subthalamic high frequency stimulation resets subthalamic firing and reduces abnormal oscillations. Brain 128:2372–2382
Morris C, Lecar H (1981) Voltage oscillations in the barnacle giant muscle fiber. Biophys J 35:193–213
Nini A, Feingold A, Slovin H, Bergmann H (1995) 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
Nowak LG, Bullier J (1998a) 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
Nowak LG, Bullier J (1998b) 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
Nunez PL (1981) Electric fields of the brain. Oxford University Press, New York
Pare D, Curro’Dossi R, Steriade M (1990) Neuronal basis of the parkinsonian resting tremor: a hypothesis and its implications for treatment. Neuroscience 35:217–226
Pikovsky AS, Rosenblum MG, Kurths J (1996) Synchronization in a population of globally coupled chaotic oscillators. Europhys Lett 34(3):165–170
Pikovsky A, Rosenblum M, Kurths J (2001) Synchronization, a universal concept in nonlinear sciences. Cambridge University Press, Cambridge
van der Pol B (1920) A theory of the amplitude of free and forced triode vibration. Radio Rev 1:704–754
van der Pol B (1927) Forced oscillations in a circuit with non-linear resistance. Phil Mag Ser 7 3:65–80
van der Pol B, van der Mark J (1928) The heartbeat considered as a relaxation oscillation, and an electrical model of the heart. Phil Mag Suppl 6:763–775
Popovych OV, Hauptmann C, Tass PA (2005a) Effective desynchronization by nonlinear delayed feedback. Phys Rev Lett 94:164102
Popovych OV, Maistrenko YuL, Tass PA (2005b) Phase chaos in coupled oscillators. Phys Rev E 71:065201(R)
Pyragas K (1992) Continuous control of chaos by self-controlling feedback. Phys Lett A 170:421–428
Ranck JB (1975) Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 98:417–468
Reddy DVR, Sen A, Johnston GL (1998) Time delay induced death in coupled limit cycle oscillators. Phys Rev Lett 80:5109–5112
Reddy DVR, Sen A, Johnston GL (1999) Time delay effects on coupled limit cycle oscillators at Hopf bifurcation. Physica D 129(1–2):15–34
Reddy DVR, Sen A, Johnston GL (2000) Experimental evidence of time-delay-induced death in coupled limit-cycle oscillators. Phys Rev Lett 85:3381–3384
Rinzel J, Ermentrout GB (1989) Analysis of neural excitability and oscillations. In: Koch CH, Segev I (eds) Methods in neuronal modelling from synapses to networks. MIT Press, Cambridge, pp 135–169
Rodriguez-Oroz MC, Obeso JA, Lang AE, Houeto J-L, Pollak P, Rehncrona S, Kulisevsky J, Albanese A, Volkmann J, Hariz MI, , Speelman JD, Guridi J, Zamarbide I, Gironell A, Molet J, Pascual-Sedano B, Pidoux B, Bonnet AM, Agid Y, Xie J, Benabid A-L, Lozano AM, Saint-Cyr J, Romito L, Contarino MF, Scerrati M, Van Blercom N (2005) Bilateral deep brain stimulation in parkinson’s disease: a multicentre study with 4 years follow-up. Brain 128(10):2240–2249
Rosenblum MG, Pikovsky AS (2004a) Controlling synchronizatio n in an ensemble of globally coupled oscillators. Phys Rev Lett 92:114102
Rosenblum MG, Pikovsky AS (2004b) Delayed feedback control of collective synchrony: an approach to suppression of pathological brain rhythms. Phys Rev E 70:041904
Rosenblum MG, Pikovsky AS, Kurths J (1996) Phase synchronization of chaotic oscillators. Phys Rev Lett 76(11):1804–1807
Rössler OE (1976) An equation for continuous chaos. Phys Lett A 57:397–398
Schuster HG, Wagner P (1989) Mutual entrainment of two limit cycle oscillators with time delayed coupling. Prog Theor Phys 81:939–945
Singer W, Gray CM (1995) Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18:555–586
Steriade M, Jones EG, Llinas RR (1990) Thalamic oscillations and signaling. Wiley, New York
Tass PA (1999) Phase resetting in medicine and biology: stochastic modelling and data analysis. Springer, Berlin Heidelberg New York
Tass PA (2001a) Desynchronizing double-pulse phase resetting and application to deep brain stimulation. Biol Cybern 85:343–354
Tass PA (2001b) Effective desynchronization by means of double-pulse phase resetting. Europhys Lett 53:15–21
Tass PA (2001c) Effective desynchronization with a resetting pulse train followed by a single pulse. Europhys Lett 55:171–177
Tass PA (2002a) Desynchronization of brain rhythms with soft phase-resetting techniques. Biol Cybern 87:102–115
Tass PA (2002b) Effective desynchronization with bipolar double-pulse stimulation. Phys Rev E 66:036226
Tass PA (2003a) A model of desynchronizing deep brain stimulation with a demand-controlled coordinated reset of neural subpopulations. Biol Cybern 89:81–88
Tass PA (2003b) Stochastic phase resetting of two coupled phase oscillators stimulated at different times. Phys Rev E 67:051902
Terman D, Rubin JE, Yew AC, Wilson CJ (2002) Activity patterns in a model for the subthalamopallidal network of the basal ganglia. J Neurosci 22:2963–2976
Traub RD, Miles R (1991) Neural networks of the hippocampus. Cambridge University Press, Cambridge
VanWiggeren GD, Roy R (1998) Communication with chaotic lasers. Science 279(5354):1198–1200
Volkmann J (2004) Deep brain stimulation for the treatment of Parkinson’s disease. J Clin Neurophysiol 21:6–17
Wichmann T, Bergman H, Starr PA, Subramanian T, Watts RL, (1999) 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
Yeung MKS, Strogatz SH (1999) Time delay in the Kuramoto model of coupled oscillators. Phys Rev Lett 82:648–651
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Popovych, O.V., Hauptmann, C. & Tass, P.A. Control of Neuronal Synchrony by Nonlinear Delayed Feedback. Biol Cybern 95, 69–85 (2006). https://doi.org/10.1007/s00422-006-0066-8
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DOI: https://doi.org/10.1007/s00422-006-0066-8