Delay-Induced Multistability and Loop Formation in Neuronal Networks with Spike-Timing-Dependent Plasticity

Spike-timing-dependent plasticity (STDP) adjusts synaptic strengths according to the precise timing of pre- and postsynaptic spike pairs. Theoretical and computational studies have revealed that STDP may contribute to the emergence of a variety of structural and dynamical states in plastic neuronal populations. In this manuscript, we show that by incorporating dendritic and axonal propagation delays in recurrent networks of oscillatory neurons, the asymptotic connectivity displays multistability, where different structures emerge depending on the initial distribution of the synaptic strengths. In particular, we show that the standard deviation of the initial distribution of synaptic weights, besides its mean, determines the main properties of the emergent structural connectivity such as the mean final synaptic weight, the number of two-neuron loops and the symmetry of the final structure. We also show that the firing rates of the neurons affect the evolution of the network, and a more symmetric configuration of the synapses emerges at higher firing rates. We justify the network results based on a two-neuron framework and show how the results translate to large recurrent networks.

[1]  Peter A Tass,et al.  Vibrotactile Coordinated Reset Stimulation for the Treatment of Neurological Diseases: Concepts and Device Specifications , 2017, Cureus.

[2]  V. Caso,et al.  Caudate infarcts and hemorrhages. , 2012, Frontiers of neurology and neuroscience.

[3]  P. J. Sjöström,et al.  Rate, Timing, and Cooperativity Jointly Determine Cortical Synaptic Plasticity , 2001, Neuron.

[4]  Georgios A. Keliris,et al.  Introduction to Research Topic – Binocular Rivalry: A Gateway to Studying Consciousness , 2012, Front. Hum. Neurosci..

[5]  Wulfram Gerstner,et al.  Phenomenological models of synaptic plasticity based on spike timing , 2008, Biological Cybernetics.

[6]  Peter A. Tass,et al.  Self-organized noise resistance of oscillatory neural networks with spike timing-dependent plasticity , 2013, Scientific Reports.

[7]  W. Gerstner,et al.  Triplets of Spikes in a Model of Spike Timing-Dependent Plasticity , 2006, The Journal of Neuroscience.

[8]  Matthieu Gilson,et al.  Emergence of network structure due to spike-timing-dependent plasticity in recurrent neuronal networks. I. Input selectivity–strengthening correlated input pathways , 2009, Biological Cybernetics.

[9]  Heinrich H. Bülthoff,et al.  Learned Non-Rigid Object Motion is a View-Invariant Cue to Recognizing Novel Objects , 2012, Front. Comput. Neurosci..

[10]  Peter A. Tass,et al.  Coordinated reset vibrotactile stimulation shows prolonged improvement in Parkinson's disease , 2017, Movement disorders : official journal of the Movement Disorder Society.

[11]  C. Canavier,et al.  Phase-Resetting Curves Determine Synchronization, Phase Locking, and Clustering in Networks of Neural Oscillators , 2009, The Journal of Neuroscience.

[12]  Matthieu Gilson,et al.  Emergence of network structure due to spike-timing-dependent plasticity in recurrent neuronal networks V: self-organization schemes and weight dependence , 2010, Biological Cybernetics.

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

[14]  Peter A. Tass,et al.  Dendritic and Axonal Propagation Delays Determine Emergent Structures of Neuronal Networks with Plastic Synapses , 2017, Scientific Reports.

[15]  L. Abbott,et al.  Competitive Hebbian learning through spike-timing-dependent synaptic plasticity , 2000, Nature Neuroscience.

[16]  Peter A. Tass,et al.  Desynchronizing electrical and sensory coordinated reset neuromodulation , 2012, Front. Hum. Neurosci..

[17]  P. Tass,et al.  Control of Abnormal Synchronization in Neurological Disorders , 2014, Front. Neurol..

[18]  Matthieu Gilson,et al.  Emergence of network structure due to spike-timing-dependent plasticity in recurrent neuronal networks. II. Input selectivity—symmetry breaking , 2009, Biological Cybernetics.

[19]  R. Kempter,et al.  Hebbian learning and spiking neurons , 1999 .

[20]  Baktash Babadi,et al.  Pairwise Analysis Can Account for Network Structures Arising from Spike-Timing Dependent Plasticity , 2013, PLoS Comput. Biol..

[21]  L. Abbott,et al.  Cortical Development and Remapping through Spike Timing-Dependent Plasticity , 2001, Neuron.

[22]  G. Bi,et al.  Synaptic modification by correlated activity: Hebb's postulate revisited. , 2001, Annual review of neuroscience.

[23]  Jean-Pascal Pfister,et al.  STDP in Oscillatory Recurrent Networks: Theoretical Conditions for Desynchronization and Applications to Deep Brain Stimulation , 2010, Front. Comput. Neurosci..

[24]  P. Goldman-Rakic Development of cortical circuitry and cognitive function. , 1987, Child Development.

[25]  E. Vaucher,et al.  Activation of the mouse primary visual cortex by medial prefrontal subregion stimulation is not mediated by cholinergic basalo-cortical projections , 2015, Front. Syst. Neurosci..

[26]  H. Swadlow Efferent neurons and suspected interneurons in S-1 forelimb representation of the awake rabbit: receptive fields and axonal properties. , 1990, Journal of neurophysiology.

[27]  Jan Karbowski,et al.  Synchrony arising from a balanced synaptic plasticity in a network of heterogeneous neural oscillators. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[28]  Sen Song,et al.  Highly Nonrandom Features of Synaptic Connectivity in Local Cortical Circuits , 2005, PLoS biology.

[29]  Ernst,et al.  Synchronization induced by temporal delays in pulse-coupled oscillators. , 1995, Physical review letters.

[30]  Yoshiki Kuramoto,et al.  Chemical Oscillations, Waves, and Turbulence , 1984, Springer Series in Synergetics.

[31]  Matthieu Gilson,et al.  Emergence of network structure due to spike-timing-dependent plasticity in recurrent neuronal networks III: Partially connected neurons driven by spontaneous activity , 2009, Biological Cybernetics.

[32]  Peter A. Tass,et al.  Anti-kindling Induced by Two-Stage Coordinated Reset Stimulation with Weak Onset Intensity , 2016, Front. Comput. Neurosci..

[33]  Matthew D. Johnson,et al.  Coordinated Reset Deep Brain Stimulation of Subthalamic Nucleus Produces Long-Lasting, Dose-Dependent Motor Improvements in the 1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine Non-Human Primate Model of Parkinsonism , 2016, Brain Stimulation.

[34]  R. Douglas,et al.  Recurrent neuronal circuits in the neocortex , 2007, Current Biology.

[35]  Boris S. Gutkin,et al.  The Effects of Spike Frequency Adaptation and Negative Feedback on the Synchronization of Neural Oscillators , 2001, Neural Computation.

[36]  H. Markram,et al.  Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. , 1997, The Journal of physiology.

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

[38]  Bard Ermentrout,et al.  Type I Membranes, Phase Resetting Curves, and Synchrony , 1996, Neural Computation.

[39]  Leonhard Lücken,et al.  Noise-enhanced coupling between two oscillators with long-term plasticity. , 2015, Physical review. E.

[40]  Matthieu Gilson,et al.  Frontiers in Computational Neuroscience Computational Neuroscience , 2022 .

[41]  Richard Kempter,et al.  State-dependencies of learning across brain scales , 2015, Front. Comput. Neurosci..

[42]  Evgueniy V. Lubenov,et al.  Decoupling through Synchrony in Neuronal Circuits with Propagation Delays , 2008, Neuron.

[43]  Naoki Masuda,et al.  Formation of feedforward networks and frequency synchrony by spike-timing-dependent plasticity , 2007, Journal of Computational Neuroscience.

[44]  Alireza Valizadeh,et al.  High frequency neurons determine effective connectivity in neuronal networks , 2018, NeuroImage.

[45]  Rishidev Chaudhuri,et al.  Computational principles of memory , 2016, Nature Neuroscience.

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

[47]  Matthieu Gilson,et al.  Emergence of network structure due to spike-timing-dependent plasticity in recurrent neuronal networks IV , 2009, Biological Cybernetics.

[48]  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.

[49]  Wulfram Gerstner,et al.  Intrinsic Stabilization of Output Rates by Spike-Based Hebbian Learning , 2001, Neural Computation.

[50]  Anthony G. Hudetz,et al.  Functional and Topological Conditions for Explosive Synchronization Develop in Human Brain Networks with the Onset of Anesthetic-Induced Unconsciousness , 2016, Front. Comput. Neurosci..

[51]  I Segev,et al.  Signal delay and input synchronization in passive dendritic structures. , 1993, Journal of neurophysiology.

[52]  Toshio Aoyagi,et al.  Co-evolution of phases and connection strengths in a network of phase oscillators. , 2009, Physical review letters.

[53]  Alessandro Torcini,et al.  Emergence of slow collective oscillations in neural networks with spike-timing dependent plasticity. , 2013, Physical review letters.

[54]  G. Edelman,et al.  Spike-timing dynamics of neuronal groups. , 2004, Cerebral cortex.

[55]  M. Awan,et al.  Correlation of TP53 Overexpression and Clinical Parameters with Five-Year Survival in Oral Squamous Cell Carcinoma Patients , 2017, Cureus.

[56]  W. Levick,et al.  Lateral geniculate relay of slowly conducting retinal afferents to cat visual cortex. , 1976, The Journal of physiology.

[57]  Haim Sompolinsky,et al.  Learning Input Correlations through Nonlinear Temporally Asymmetric Hebbian Plasticity , 2003, The Journal of Neuroscience.

[58]  Christian Hauptmann,et al.  Counteracting tinnitus by acoustic coordinated reset neuromodulation. , 2012, Restorative neurology and neuroscience.

[59]  Peter A. Tass,et al.  Augmented brain function by coordinated reset stimulation with slowly varying sequences , 2015, Front. Syst. Neurosci..

[60]  A Valizadeh,et al.  Effect of synaptic plasticity on the structure and dynamics of disordered networks of coupled neurons. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[61]  E. Izhikevich,et al.  Weakly connected neural networks , 1997 .

[62]  Guillermo A. Cecchi,et al.  A Theory of Loop Formation and Elimination by Spike Timing-Dependent Plasticity , 2009, Front. Neural Circuits.

[63]  Eugene M. Izhikevich,et al.  Weakly pulse-coupled oscillators, FM interactions, synchronization, and oscillatory associative memory , 1999, IEEE Trans. Neural Networks.

[64]  Katsunori Kitano,et al.  Interplay between a phase response curve and spike-timing-dependent plasticity leading to wireless clustering. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[65]  Nikos K. Logothetis,et al.  Frontiers in Computational Neuroscience Computational Neuroscience , 2022 .

[66]  Andreas Schierwagen,et al.  Dendritic morphology and signal delay in superior colliculus neurons , 2001, Neurocomputing.

[67]  L. Abbott,et al.  Synaptic plasticity: taming the beast , 2000, Nature Neuroscience.

[68]  Y. Kawaguchi,et al.  Recurrent Connection Patterns of Corticostriatal Pyramidal Cells in Frontal Cortex , 2006, The Journal of Neuroscience.

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

[70]  Christian Hauptmann,et al.  Coordinated reset has sustained aftereffects in Parkinsonian monkeys , 2012, Annals of neurology.

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

[72]  H. Jörntell,et al.  Presynaptic Calcium Signalling in Cerebellar Mossy Fibres , 2009, Front. Neural Circuits.

[73]  Markus Diesmann,et al.  Spike-Timing-Dependent Plasticity in Balanced Random Networks , 2007, Neural Computation.

[74]  Günther Palm,et al.  Does Spike-Timing-Dependent Synaptic Plasticity Couple or Decouple Neurons Firing in Synchrony? , 2012, Front. Comput. Neurosci..

[75]  Leeanne M. Carey,et al.  Fish Oil Diet Associated with Acute Reperfusion Related Hemorrhage, and with Reduced Stroke-Related Sickness Behaviors and Motor Impairment , 2014, Front. Neurol..

[76]  Christian Hauptmann,et al.  Coordinated reset neuromodulation for Parkinson's disease: Proof-of-concept study , 2014, Movement disorders : official journal of the Movement Disorder Society.

[77]  Leonardo L. Gollo,et al.  Stimulus-dependent synchronization in delayed-coupled neuronal networks , 2016, Scientific Reports.

[78]  S. Sadeghi,et al.  Synchronization of delayed coupled neurons in presence of inhomogeneity , 2012, Journal of Computational Neuroscience.

[79]  Alireza Valizadeh,et al.  Self-organization of synchronous activity propagation in neuronal networks driven by local excitation , 2015, Front. Comput. Neurosci..

[80]  Matthieu Gilson,et al.  Frequency Selectivity Emerging from Spike-Timing-Dependent Plasticity , 2012, Neural Computation.

[81]  H. Swadlow,et al.  Corticogeniculate neurons, corticotectal neurons, and suspected interneurons in visual cortex of awake rabbits: receptive-field properties, axonal properties, and effects of EEG arousal. , 1987, Journal of neurophysiology.