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Long-term anti-kindling effects of desynchronizing brain stimulation: a theoretical study

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Abstract

In a modeling study we show that desynchronization stimulation may have powerful anti-kindling effects. For this, we incorporate spike-timing-dependent plasticity into a generic network of coupled phase oscillators, which serves as a model network of synaptically interacting neurons. Two states may coexist under spontaneous conditions: a state of uncorrelated firing and a state of pathological synchrony. Appropriate stimulation protocols make the network learn or unlearn the pathological synaptic interactions, respectively. Low-frequency periodic pulse train stimulation causes a kindling. Permanent high-frequency stimulation, used as golden standard for deep brain stimulation in medically refractory movement disorders, basically freezes the synaptic weights. In contrast, desynchronization stimulation, e.g., by means of a multi-site coordinated reset, has powerful long-term anti-kindling effects and enables the network to unlearn pathologically strong synaptic interactions. We propose desynchronization stimulation for the therapy of movement disorders and epilepsies.

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References

  • Abbott LF, Nelson SB (2000) Synaptic plasticity: taming the beast. Nat Neurosci 3:1178–1183

    Article  PubMed  CAS  Google Scholar 

  • Albensi BC, Ata G, Schmidt E, Waterman JD, Janigro D (2004) Activation of long-term synaptic plasticity causes suppression of epileptiform activity in rat hippocampal slices. Brain Res 998:56–64

    Article  PubMed  CAS  Google Scholar 

  • Benabid A, Pollak P, Gervason C, Hoffmann D, Gao DM, Hommel M, Perret JE, de Rougemont J (1991) Long-term suppression of tremor by chronic stimulation of the ventral intermediate thalamic nucleus. Lancet 337(8738):403–6

    Article  PubMed  CAS  Google Scholar 

  • Bergman H, Feingold A, Nini A, Raz A, Slovin H, Abeles M, Vaadia E (1998) Physiological aspects of information processing in the basal ganglia of normal and parkinsonian primates. Trends Neurosci. (21):32–38

  • Best EN (1979) Null space in the Hodgkin-Huxley equations. Biophys J 27:87–104

    PubMed  CAS  Google Scholar 

  • Bi GQ, Poo MM (1998) Activity-induced synaptic modifications in hippocampal culture, dependence on spike timing, synaptic strength and cell type. J Neurosci 18:10464–10472

    PubMed  CAS  Google Scholar 

  • Debanne D, Gahweiler BH, Thompson SM (1998) Long-term synaptic plasticity between pairs of individual CA3 pyramidal cells in rat hippocampal slice cultures. J Physiol (London) 507:237–247

    Article  CAS  Google Scholar 

  • Dietz V, Müller R (2004) Degradation of neuronal function following a spinal cord injury: mechanisms and countermeasures. Brain 127:2221–2231

    Article  PubMed  Google Scholar 

  • Feldman DE (2000) Timing-based LTP and LTD at vertical inputs to layer II/III pyramidal cells in rat barrel cortex. Neuron 27:45–56

    Article  PubMed  CAS  Google Scholar 

  • Goddar G (1967) Development of epileptic seizures through brain stimulation at low intensity. Nature 214:1020–1021

    Article  PubMed  Google Scholar 

  • Guttman R, Lewis S, Rinzel J (1980) Control of repetitive firing in squid axon membrane as a model for a neuroneoscillator. J Physiol (London) 395:377–395

    Google Scholar 

  • Hebb DO (1949) The orgnization of behavior. Wiley, New York

    Google Scholar 

  • Honeycutt RL (1992) Stochastic Runge-Kutta algorithms. I. White noise. Phys Rev A 45(2):600–603

    Article  PubMed  CAS  Google Scholar 

  • Izhikevich E, Gally J, Edelman G (2004) Spike-timing dynamics of neural groups. Cereb Cortex 14:933–944

    Article  PubMed  Google Scholar 

  • Kilgard MP, Merzenich MM (1998) Cortical map reorganization enabled by nucleus basalis activity. Science 279:1714–1718

    Article  PubMed  CAS  Google Scholar 

  • Kuramoto Y (1984) Chemical oscillations, waves, and turbulence. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Lenz F, Kwan H, Martin R, Tasker R, Dostrovsky J, Lenz Y (1994) Single unit analysis of the human ventral thalamic nuclear group. Tremor-related activity in functionally identified cells. Brain 117:531–543

    Google Scholar 

  • Limousin P, Speelman J, Gielen F, Janssens M (1999) Multicentre European study of thalamic stimulation in parkinsonian and essential tremor. J Neurol Neurosurg Psychiatry 66(3):289–296

    Article  PubMed  CAS  Google Scholar 

  • Markram H, Lübke J, Frotscher M, Sakmann B (1997) Regulation of synaptic efficacy by coincidence of postsynaptic APs and EPSPs. Science 275:213–215

    Article  PubMed  CAS  Google Scholar 

  • McInryre C, Savasta M, Kerkerian-Le Goff K, Vitek J (2004) Uncovering the mechanism(s) of action of deep brain stimulation: activation, inhibition, or both. Clin Neurophysiol 115:1239–1248

    Article  PubMed  Google Scholar 

  • Morimoto K, Fahnestock M, Racine R (2004) Kindling and status epilepticus models of epilepsy: rewiring the brain. Prog Neurobiol 73:1–60

    Article  PubMed  CAS  Google Scholar 

  • Nini A, Feingold A, Slovin H, Bergman 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

    PubMed  CAS  Google Scholar 

  • Pare D, Curro’Dossi R, Steriade M (1990) Neuronal basis of the parkinsonian resting tremor: a hypothesis and its implications for treatment. Neurosi 35:217–226

    Article  CAS  Google Scholar 

  • Ranck J (1975) Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res 98:417–440

    Article  PubMed  Google Scholar 

  • Schuett S, Bonhoeffer T, Hübener M (2001) Pairing-induced changes of orientation maps in cat visual cortex. Neuron 32:325–337

    Article  PubMed  CAS  Google Scholar 

  • Seliger P, Young SC, Tsimring LS (2002) Plasticity and learning in a network of coupled phase oscillators. Phys Rev E 65:041906

    Article  CAS  Google Scholar 

  • Smirnakis S, Brewer A, Schmid M, Tolias A, Schüz A, Augath M, Inhoffen W, Wandell B, Logothetis N (2005) Lack of long-term cortical reorganization after macaque retinal lesions. Nature 435:300–307

    Article  PubMed  CAS  Google Scholar 

  • Song S, Miller KD, Abbott LF (2000) Competitive Hebian learning trough spike-timing-dependent synaptic plasticity. Nat Neurosci 3(9):919–926

    Article  PubMed  CAS  Google Scholar 

  • Speckmann E, Elger C (1991) The neurophysiological basis of epileptic activity: a condensed overview. Epilepsy Res Suppl 2:1–7

    PubMed  CAS  Google Scholar 

  • Strogatz SH (2000)From Kuramoto to Crawford: exploring the onset of synchronization in populations of coupled oscillators. Physica D 143:1–20

    Article  Google Scholar 

  • Tass PA (1999) Phase resetting in Medicine and Biology. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Tass PA (2001a) Desynchronizing double-pulse phase resetting and application to deep brain stimulation. Biol Cybern 85:343–354

    Article  PubMed  CAS  Google Scholar 

  • Tass PA (2001b) Effective desynchronization with a resetting pulse train followed by a single pulse. Europhys Lett 55(2):171–177

    Article  CAS  Google Scholar 

  • Tass PA (2002) Desynchronization of brain rhythms with soft phase-resetting techniques. Biol Cybern 87:102–115

    Article  PubMed  Google Scholar 

  • Tass PA (2003a) A model of desynchronizing deep brain stimulation with a demand-controlled coordinated reset of neural subpopulations. Biol Cybern 89:81–88

    Article  Google Scholar 

  • Tass PA (2003b) Desynchronization by means of a coordinated reset of neural sub-populations - a novel technique for demand-controlled deep brain stimulation. Prog Theor Phys Suppl (Kyoto) 150:281–296

    Article  Google Scholar 

  • Tass PA, Russel DF, Barnikol UB, Neiman AB, Yakusheva TA, Voges J, Sturm V, Freund HJ (2005) Selective disruption of neural synchronization by means of repeated transient phase reset. (submitted)

  • Volkmann J (2004) Deep brain stimulation for the treatment of parkinson’s disease. J Clin Neurophysiol 21:6–17

    Article  PubMed  Google Scholar 

  • Winfree AT (1980) The geometry of biological time. Springer, Berlin Heildeberg New York

    Google Scholar 

  • Yao H, Dan Y (2001) Stimulus timing-dependent plasticity in cortical processing of orientation. Neuron 32:315–323

    Article  PubMed  CAS  Google Scholar 

  • Zhou Q, Tao HW, Poo MM (2003) Reversal and stabilization of synaptic modifications in a developing visual system. Science 300:1953–1957

    Article  PubMed  CAS  Google Scholar 

Download references

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Authors and Affiliations

  1. Institute for Medicine and Virtual Institute of Neuromodulation, Research Center Jülich, Leo-Brand-Street, 52425, Jülich, Germany

    Peter A. Tass & Milan Majtanik

  2. Department of Stereotaxic and Functional Neurosurgery, University of Cologne, Joseph-Stelzmann-Street 9, 50924, Cologne, Germany

    Peter A. Tass

  3. Brain Imaging Center West, Leo-Brand-Street, 52425, Jülich, Germany

    Peter A. Tass

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  1. Peter A. Tass
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  2. Milan Majtanik
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Correspondence to Peter A. Tass.

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Tass, P.A., Majtanik, M. Long-term anti-kindling effects of desynchronizing brain stimulation: a theoretical study. Biol Cybern 94, 58–66 (2006). https://doi.org/10.1007/s00422-005-0028-6

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  • DOI: https://doi.org/10.1007/s00422-005-0028-6

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