Long-lasting desynchronization in rat hippocampal slice induced by coordinated reset stimulation.

In computational models it has been shown that appropriate stimulation protocols may reshape the connectivity pattern of neural or oscillator networks with synaptic plasticity in a way that the network learns or unlearns strong synchronization. The underlying mechanism is that a network is shifted from one attractor to another, so that long-lasting stimulation effects are caused which persist after the cessation of stimulation. Here we study long-lasting effects of multisite electrical stimulation in a rat hippocampal slice rendered epileptic by magnesium withdrawal. We show that desynchronizing coordinated reset stimulation causes a long-lasting desynchronization between hippocampal neuronal populations together with a widespread decrease in the amplitude of the epileptiform activity. In contrast, periodic stimulation induces a long-lasting increase in both synchronization and amplitude.

[1]  Rafael Yuste,et al.  Genesis of dendritic spines: insights from ultrastructural and imaging studies , 2004, Nature Reviews Neuroscience.

[2]  Peter A. Tass,et al.  Therapeutic rewiring by means of desynchronizing brain stimulation , 2007, Biosyst..

[3]  D M Durand,et al.  Suppression of epileptiform activity by high frequency sinusoidal fields in rat hippocampal slices , 2001, The Journal of physiology.

[4]  H. Markram,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997, Science.

[5]  Bruce J. Gluckman,et al.  Adaptive Electric Field Control of Epileptic Seizures , 2001, The Journal of Neuroscience.

[6]  S. Schiff,et al.  Periodic pacing an in vitro epileptic focus. , 1995, Journal of neurophysiology.

[7]  Dominique M Durand,et al.  Effects of applied currents on spontaneous epileptiform activity induced by low calcium in the rat hippocampus , 1998, Brain Research.

[8]  Martin Hasler,et al.  Synchronization of bursting neurons: what matters in the network topology. , 2005, Physical review letters.

[9]  W. R. Adey,et al.  Long-term effects of sinusoidal extracellular electric fields in penicillin-treated rat hippocampal slices , 1986, Brain Research.

[10]  Peter A. Tass,et al.  Long-term anti-kindling effects of desynchronizing brain stimulation: a theoretical study , 2005, Biological Cybernetics.

[11]  Christian Hauptmann,et al.  Therapeutic modulation of synaptic connectivity with desynchronizing brain stimulation. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[12]  H. Vaughan,et al.  Averaged multiple unit activity as an estimate of phasic changes in local neuronal activity: effects of volume-conducted potentials , 1980, Journal of Neuroscience Methods.

[13]  S. Wang,et al.  Malleability of Spike-Timing-Dependent Plasticity at the CA3–CA1 Synapse , 2006, The Journal of Neuroscience.

[14]  H. Scharfman,et al.  Synchronization of area CA3 hippocampal pyramidal cells and non-granule cells of the dentate gyrus in bicuculline-treated rat hippocampal slices , 1994, Neuroscience.

[15]  D. Amaral,et al.  Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat , 1990, The Journal of comparative neurology.

[16]  G. Bi,et al.  Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type , 1998, The Journal of Neuroscience.

[17]  S. Mallat A wavelet tour of signal processing , 1998 .

[18]  Lev S Tsimring,et al.  Plasticity and learning in a network of coupled phase oscillators. , 2001, Physical review. E, Statistical, nonlinear, and soft matter physics.

[19]  H. Markram,et al.  Spontaneous and evoked synaptic rewiring in the neonatal neocortex , 2006, Proceedings of the National Academy of Sciences.

[20]  Peter A. Tass,et al.  A model of desynchronizing deep brain stimulation with a demand-controlled coordinated reset of neural subpopulations , 2003, Biological Cybernetics.

[21]  Edward Ott,et al.  Emergence of coherence in complex networks of heterogeneous dynamical systems. , 2006, Physical review letters.

[22]  Jürgen Kurths,et al.  Detection of n:m Phase Locking from Noisy Data: Application to Magnetoencephalography , 1998 .

[23]  Corey M. McCann,et al.  Rapid and modifiable neurotransmitter receptor dynamics at a neuronal synapse in vivo , 2008, Nature Neuroscience.

[24]  F. Engert,et al.  Dendritic spine changes associated with hippocampal long-term synaptic plasticity , 1999, Nature.

[25]  Jürgen Kurths,et al.  Synchronization: Phase locking and frequency entrainment , 2001 .

[26]  Alexey A Koronovskii,et al.  Detecting synchronization of self-sustained oscillators by external driving with varying frequency. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[27]  Christian Hauptmann,et al.  Multistability in the Kuramoto model with synaptic plasticity. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[28]  Dominique M Durand,et al.  Local Suppression of Epileptiform Activity by Electrical Stimulation in Rat Hippocampus In Vitro , 2003, The Journal of physiology.

[29]  Wulfram Gerstner,et al.  A neuronal learning rule for sub-millisecond temporal coding , 1996, Nature.

[30]  C. Bernard,et al.  Model of local connectivity patterns in CA3 and CA1 areas of the hippocampus , 1994, Hippocampus.

[31]  J. Jefferys,et al.  Low‐calcium field burst discharges of CA1 pyramidal neurones in rat hippocampal slices. , 1984, The Journal of physiology.

[32]  S. Strogatz Exploring complex networks , 2001, Nature.

[33]  W. Ditto,et al.  Electric field suppression of epileptiform activity in hippocampal slices. , 1996, Journal of neurophysiology.

[34]  Wilkie A. Wilson,et al.  Magnesium-free medium activates seizure-like events in the rat hippocampal slice , 1986, Brain Research.