{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,27]],"date-time":"2026-10-27T01:42:39Z","timestamp":1793065359986,"version":"4.5.0"},"reference-count":103,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,4,19]],"date-time":"2022-04-19T00:00:00Z","timestamp":1650326400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Netw. Physiol."],"abstract":"<jats:p>Hypersynchrony of neuronal activity is associated with several neurological disorders, including essential tremor and Parkinson\u2019s disease (PD). Chronic high-frequency deep brain stimulation (HF DBS) is the standard of care for medically refractory PD. Symptoms may effectively be suppressed by HF DBS, but return shortly after cessation of stimulation. Coordinated reset (CR) stimulation is a theory-based stimulation technique that was designed to specifically counteract neuronal synchrony by desynchronization. During CR, phase-shifted stimuli are delivered to multiple neuronal subpopulations. Computational studies on CR stimulation of plastic neuronal networks revealed long-lasting desynchronization effects obtained by down-regulating abnormal synaptic connectivity. This way, networks are moved into attractors of stable desynchronized states such that stimulation-induced desynchronization persists after cessation of stimulation. Preclinical and clinical studies confirmed corresponding long-lasting therapeutic and desynchronizing effects in PD. As PD symptoms are associated with different pathological synchronous rhythms, stimulation-induced long-lasting desynchronization effects should favorably be robust to variations of the stimulation frequency. Recent computational studies suggested that this robustness can be improved by randomizing the timings of stimulus deliveries. We study the long-lasting effects of CR stimulation with randomized stimulus amplitudes and\/or randomized stimulus timing in networks of leaky integrate-and-fire (LIF) neurons with spike-timing-dependent plasticity. Performing computer simulations and analytical calculations, we study long-lasting desynchronization effects of CR with and without randomization of stimulus amplitudes alone, randomization of stimulus times alone as well as the combination of both. Varying the CR stimulation frequency (with respect to the frequency of abnormal target rhythm) and the number of separately stimulated neuronal subpopulations, we reveal parameter regions and related mechanisms where the two qualitatively different randomization mechanisms improve the robustness of long-lasting desynchronization effects of CR. In particular, for clinically relevant parameter ranges double-random CR stimulation, i.e., CR stimulation with the specific combination of stimulus amplitude randomization and stimulus time randomization, may outperform regular CR stimulation with respect to long-lasting desynchronization. In addition, our results provide the first evidence that an effective reduction of the overall stimulation current by stimulus amplitude randomization may improve the frequency robustness of long-lasting therapeutic effects of brain stimulation.<\/jats:p>","DOI":"10.3389\/fnetp.2022.864859","type":"journal-article","created":{"date-parts":[[2022,4,19]],"date-time":"2022-04-19T04:43:47Z","timestamp":1650343427000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":20,"title":["Long-Lasting Desynchronization of Plastic Neuronal Networks by Double-Random Coordinated Reset Stimulation"],"prefix":"10.3389","volume":"2","author":[{"given":"Ali","family":"Khaledi-Nasab","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Justus A.","family":"Kromer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter A.","family":"Tass","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,4,19]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"1178","DOI":"10.1038\/81453","article-title":"Synaptic Plasticity: Taming the Beast","volume":"3","author":"Abbott","year":"2000","journal-title":"Nat. Neurosci."},{"key":"B2","doi-asserted-by":"publisher","first-page":"231","DOI":"10.1002\/mds.10327","article-title":"Sensorimotor Integration in Movement Disorders","volume":"18","author":"Abbruzzese","year":"2003","journal-title":"Move. Disord."},{"key":"B3","doi-asserted-by":"publisher","first-page":"1679","DOI":"10.1002\/mds.25923","article-title":"Coordinated Reset Neuromodulation for Parkinson's Disease: Proof\u2010of\u2010concept Study","volume":"29","author":"Adamchic","year":"2014","journal-title":"Mov. Disord."},{"key":"B4","doi-asserted-by":"publisher","first-page":"034101","DOI":"10.1103\/PhysRevLett.102.034101","article-title":"Co-evolution of Phases and Connection Strengths in a Network of Phase Oscillators","volume":"102","author":"Aoki","year":"2009","journal-title":"Phys. Rev. Lett."},{"key":"B5","doi-asserted-by":"publisher","first-page":"e0142143","DOI":"10.1371\/journal.pone.0142143","article-title":"Network Physiology: How Organ Systems Dynamically Interact","volume":"10","author":"Bartsch","year":"2015","journal-title":"PloS ONE"},{"key":"B6","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/ncomms1705","article-title":"Network Physiology Reveals Relations between Network Topology and Physiological Function","volume":"3","author":"Bashan","year":"2012","journal-title":"Nat. Commun."},{"key":"B7","doi-asserted-by":"publisher","first-page":"088301","DOI":"10.1103\/PhysRevLett.124.088301","article-title":"Birth and Stabilization of Phase Clusters by Multiplexing of Adaptive Networks","volume":"124","author":"Berner","year":"2020","journal-title":"Phys. Rev. Lett."},{"key":"B8","doi-asserted-by":"publisher","first-page":"7617","DOI":"10.1523\/jneurosci.19-17-07617.1999","article-title":"Mechanisms Underlying Spontaneous Oscillation and Rhythmic Firing in Rat Subthalamic Neurons","volume":"19","author":"Bevan","year":"1999","journal-title":"J. Neurosci."},{"key":"B9","doi-asserted-by":"publisher","first-page":"10464","DOI":"10.1523\/JNEUROSCI.18-24-10464.1998","article-title":"Synaptic Modifications in Cultured Hippocampal Neurons: Dependence on Spike Timing, Synaptic Strength, and Postsynaptic Cell Type","volume":"18","author":"Bi","year":"1998","journal-title":"J. Neurosci."},{"key":"B10","doi-asserted-by":"publisher","first-page":"364","DOI":"10.1152\/jn.00906.2010","article-title":"Stimulus Features Underlying Reduced Tremor Suppression with Temporally Patterned Deep Brain Stimulation","volume":"107","author":"Birdno","year":"2012","journal-title":"J. Neurophysiol."},{"key":"B11","doi-asserted-by":"publisher","first-page":"358","DOI":"10.1016\/j.tins.2017.04.001","article-title":"The Role of Astrocyte Dysfunction in Parkinson's Disease Pathogenesis","volume":"40","author":"Booth","year":"2017","journal-title":"Trends Neurosciences"},{"key":"B12","doi-asserted-by":"publisher","first-page":"60","DOI":"10.1016\/j.expneurol.2012.09.008","article-title":"Improved Efficacy of Temporally Non-regular Deep Brain Stimulation in Parkinson's Disease","volume":"239","author":"Brocker","year":"2013","journal-title":"Exp. Neurol."},{"key":"B13","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1002\/mds.10358","article-title":"Oscillatory Nature of Human Basal Ganglia Activity: Relationship to the Pathophysiology of Parkinson's Disease","volume":"18","author":"Brown","year":"2003","journal-title":"Mov. Disord."},{"key":"B14","doi-asserted-by":"publisher","first-page":"885","DOI":"10.1162\/089976604773135041","article-title":"Spike-timing-dependent Plasticity: The Relationship to Rate-Based Learning for Models with Weight Dynamics Determined by a Stable Fixed point","volume":"16","author":"Burkitt","year":"2004","journal-title":"Neural Comput."},{"key":"B15","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1146\/annurev.neuro.31.060407.125639","article-title":"Spike Timing-dependent Plasticity: A Hebbian Learning Rule","volume":"31","author":"Caporale","year":"2008","journal-title":"Annu. Rev. Neurosci."},{"key":"B16","doi-asserted-by":"publisher","first-page":"305","DOI":"10.1016\/j.brs.2011.03.011","article-title":"Tremor-specific Neuronal Oscillation Pattern in Dorsal Subthalamic Nucleus of Parkinsonian Patients","volume":"5","author":"Contarino","year":"2012","journal-title":"Brain Stimulation"},{"key":"B17","doi-asserted-by":"publisher","first-page":"1163","DOI":"10.1212\/wnl.0000000000000823","article-title":"Directional Steering: a Novel Approach to Deep Brain Stimulation","volume":"83","author":"Contarino","year":"2014","journal-title":"Neurology"},{"key":"B18","doi-asserted-by":"publisher","first-page":"687","DOI":"10.1038\/nrneurol.2013.224","article-title":"Pathophysiology of Somatosensory Abnormalities in Parkinson Disease","volume":"9","author":"Conte","year":"2013","journal-title":"Nat. Rev. Neurol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"911","DOI":"10.1152\/jn.00103.2010","article-title":"Deep Brain Stimulation Alleviates Parkinsonian Bradykinesia by Regularizing Pallidal Activity","volume":"104","author":"Dorval","year":"2010","journal-title":"J. Neurophysiol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"154","DOI":"10.3389\/fncom.2014.00154","article-title":"Coordinated Reset Stimulation in a Large-Scale Model of the Stn-Gpe Circuit","volume":"8","author":"Ebert","year":"2014","journal-title":"Front. Comput. Neurosci."},{"key":"B21","doi-asserted-by":"publisher","first-page":"e0189109","DOI":"10.1371\/journal.pone.0189109","article-title":"The Role of Cortical Oscillations in a Spiking Neural Network Model of the Basal Ganglia","volume":"12","author":"Fountas","year":"2017","journal-title":"PLoS ONE"},{"key":"B22","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1016\/j.tins.2007.05.004","article-title":"Pathological Synchronization in Parkinson's Disease: Networks, Models and Treatments","volume":"30","author":"Hammond","year":"2007","journal-title":"Trends Neurosciences"},{"key":"B23","doi-asserted-by":"publisher","first-page":"759","DOI":"10.1016\/j.neucom.2004.10.072","article-title":"Delayed Feedback Control of Synchronization in Locally Coupled Neuronal Networks","author":"Hauptmann","year":"","journal-title":"Neurocomputing"},{"key":"B24","doi-asserted-by":"publisher","first-page":"463","DOI":"10.1007\/s00422-005-0020-1","article-title":"Effectively Desynchronizing Deep Brain Stimulation Based on a Coordinated Delayed Feedback Stimulation via Several Sites: a Computational Study","volume":"93","author":"Hauptmann","year":"","journal-title":"Biol. Cybern."},{"key":"B25","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1142\/S0219493705001420","article-title":"Multisite Coordinated Delayed Feedback for an Effective Desynchronization of Neuronal Networks","volume":"5","author":"Hauptmann","year":"","journal-title":"Stoch. Dyn."},{"key":"B26","doi-asserted-by":"publisher","first-page":"056008","DOI":"10.1088\/1741-2560\/7\/5\/056008","article-title":"Restoration of Segregated, Physiological Neuronal Connectivity by Desynchronizing Stimulation","volume":"7","author":"Hauptmann","year":"2010","journal-title":"J. Neural Eng."},{"key":"B27","doi-asserted-by":"publisher","first-page":"330","DOI":"10.1016\/j.brs.2021.01.015","article-title":"Accumbens Coordinated Reset Stimulation in Mice Exhibits Ameliorating Aftereffects on Binge Alcohol Drinking","volume":"14","author":"Ho","year":"2021","journal-title":"Brain Stimulation"},{"key":"B28","doi-asserted-by":"publisher","first-page":"e1005011","DOI":"10.1371\/journal.pcbi.1005011","article-title":"Phasic Burst Stimulation: A Closed-Loop Approach to Tuning Deep Brain Stimulation Parameters for Parkinson's Disease","volume":"12","author":"Holt","year":"2016","journal-title":"Plos Comput. Biol."},{"key":"B29","doi-asserted-by":"publisher","first-page":"100201","DOI":"10.1088\/1367-2630\/18\/10\/100201","article-title":"Focus on the Emerging New fields of Network Physiology and Network Medicine","volume":"18","author":"Ivanov","year":"2016","journal-title":"New J. Phys."},{"key":"B30","doi-asserted-by":"publisher","first-page":"031902","DOI":"10.1103\/PhysRevE.65.031902","article-title":"Synchrony Arising from a Balanced Synaptic Plasticity in a Network of Heterogeneous Neural Oscillators","volume":"65","author":"Karbowski","year":"2002","journal-title":"Phys. Rev. E"},{"key":"B31","doi-asserted-by":"publisher","first-page":"719680","DOI":"10.3389\/fphys.2021.719680","article-title":"Long-lasting Desynchronization Effects of Coordinated Reset Stimulation Improved by Random Jitters","volume":"12","author":"Khaledi-Nasab","year":"","journal-title":"Front. Physiol."},{"key":"B32","doi-asserted-by":"publisher","first-page":"622620","DOI":"10.3389\/fphys.2020.622620","article-title":"Long-lasting Desynchronization of Plastic Neural Networks by Random Reset Stimulation","volume":"11","author":"Khaledi-Nasab","year":"","journal-title":"Front. Physiol."},{"key":"B33","doi-asserted-by":"publisher","first-page":"1925","DOI":"10.1056\/nejmoa035275","article-title":"Five-Year Follow-Up of Bilateral Stimulation of the Subthalamic Nucleus in Advanced Parkinson's Disease","volume":"349","author":"Krack","year":"2003","journal-title":"N. Engl. J. Med."},{"key":"B34","doi-asserted-by":"publisher","first-page":"S188","DOI":"10.1002\/mds.10163","article-title":"Postoperative Management of Subthalamic Nucleus Stimulation for Parkinson's Disease","volume":"17","author":"Krack","year":"2002","journal-title":"Mov. Disord."},{"key":"B35","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1038\/s41582-020-00426-z","article-title":"Technology of Deep Brain Stimulation: Current Status and Future Directions","volume":"17","author":"Krauss","year":"2021","journal-title":"Nat. Rev. Neurol."},{"key":"B36","doi-asserted-by":"publisher","first-page":"083134","DOI":"10.1063\/5.0015196","article-title":"Impact of Number of Stimulation Sites on Long-Lasting Desynchronization Effects of Coordinated Reset Stimulation","volume":"30","author":"Kromer","year":"2020","journal-title":"Chaos"},{"key":"B37","doi-asserted-by":"publisher","first-page":"033101","DOI":"10.1103\/PhysRevResearch.2.033101","article-title":"Long-lasting Desynchronization by Decoupling Stimulation","volume":"2","author":"Kromer","year":"2020","journal-title":"Phys. Rev. Res."},{"key":"B38","doi-asserted-by":"publisher","first-page":"1956","DOI":"10.1111\/j.1460-9568.2006.04717.x","article-title":"Reduction in Subthalamic 8-35 Hz Oscillatory Activity Correlates with Clinical Improvement in Parkinson's Disease","volume":"23","author":"K\u00fchn","year":"2006","journal-title":"Eur. J. Neurosci."},{"key":"B39","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-642-69689-3","volume-title":"Chemical Oscillations, Waves, and Turbulence","author":"Kuramoto","year":"1984"},{"key":"B40","doi-asserted-by":"publisher","first-page":"3525","DOI":"10.1152\/jn.00808.2007","article-title":"Resonant Antidromic Cortical Circuit Activation as a Consequence of High-Frequency Subthalamic Deep-Brain Stimulation","volume":"98","author":"Li","year":"2007","journal-title":"J. Neurophysiol."},{"key":"B41","doi-asserted-by":"publisher","first-page":"5319","DOI":"10.1038\/ncomms6319","article-title":"Formation and Maintenance of Neuronal Assemblies through Synaptic Plasticity","volume":"5","author":"Litwin-Kumar","year":"2014","journal-title":"Nat. Commun."},{"key":"B42","doi-asserted-by":"publisher","first-page":"103466","DOI":"10.1016\/j.bspc.2021.103466","article-title":"Oscillation Suppression Effects of Intermittent Noisy Deep Brain Stimulation Induced by Coordinated Reset Pattern Based on a Computational Model","volume":"73","author":"Liu","year":"2022","journal-title":"Biomed. Signal Process. Control."},{"key":"B43","doi-asserted-by":"publisher","first-page":"62","DOI":"10.3389\/fncir.2015.00062","article-title":"Plasticity of Brain Wave Network Interactions and Evolution across Physiologic States","volume":"9","author":"Liu","year":"2015","journal-title":"Front. Neural Circuits"},{"key":"B44","doi-asserted-by":"publisher","first-page":"1849","DOI":"10.3389\/fphys.2018.01849","article-title":"Dendritic and Axonal Propagation Delays May Shape Neuronal Networks with Plastic Synapses","volume":"9","author":"Madadi Asl","year":"2018","journal-title":"Front. Physiol."},{"key":"B45","doi-asserted-by":"publisher","first-page":"066207","DOI":"10.1103\/PhysRevE.75.066207","article-title":"Multistability in the Kuramoto Model with Synaptic Plasticity","volume":"75","author":"Maistrenko","year":"2007","journal-title":"Phys. Rev. E"},{"key":"B46","doi-asserted-by":"publisher","first-page":"e1006113","DOI":"10.1371\/journal.pcbi.1006113","article-title":"How Stimulation Frequency and Intensity Impact on the Long-Lasting Effects of Coordinated Reset Stimulation","volume":"14","author":"Manos","year":"2018","journal-title":"Plos Comput. Biol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"213","DOI":"10.1126\/science.275.5297.213","article-title":"Regulation of Synaptic Efficacy by Coincidence of Postsynaptic Aps and Epsps","volume":"275","author":"Markram","year":"1997","journal-title":"Science"},{"key":"B48","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1007\/s10827-007-0022-1","article-title":"Formation of Feedforward Networks and Frequency Synchrony by Spike-timing-dependent Plasticity","volume":"22","author":"Masuda","year":"2007","journal-title":"J. Comput. Neurosci."},{"key":"B49","doi-asserted-by":"publisher","first-page":"1042","DOI":"10.1016\/j.neuron.2019.03.004","article-title":"Circuit Mechanisms of Parkinson's Disease","volume":"101","author":"McGregor","year":"2019","journal-title":"Neuron"},{"key":"B50","first-page":"43","article-title":"On Circulating Excitations in Heart Muscle and Their Possible Relation to Tachycardia and Fibrillation","volume":"8","author":"Mines","year":"1914","journal-title":"Trans. R. Soc. Can."},{"key":"B51","doi-asserted-by":"publisher","first-page":"459","DOI":"10.1007\/s00422-008-0233-1","article-title":"Phenomenological Models of Synaptic Plasticity Based on Spike Timing","volume":"98","author":"Morrison","year":"2008","journal-title":"Biol. Cybern."},{"key":"B52","doi-asserted-by":"publisher","first-page":"734344","DOI":"10.3389\/fnetp.2021.734344","article-title":"Treatment Tone Spacing and Acute Effects of Acoustic Coordinated Reset Stimulation in Tinnitus Patients","volume":"1","author":"Munjal","year":"2021","journal-title":"Front. Netw. Physiol."},{"key":"B53","doi-asserted-by":"publisher","first-page":"1800","DOI":"10.1152\/jn.1995.74.4.1800","article-title":"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","volume":"74","author":"Nini","year":"1995","journal-title":"J. Neurophysiol."},{"key":"B54","doi-asserted-by":"publisher","first-page":"e1004458","DOI":"10.1371\/journal.pcbi.1004458","article-title":"Self-organization of Microcircuits in Networks of Spiking Neurons with Plastic Synapses","volume":"11","author":"Ocker","year":"2015","journal-title":"Plos Comput. Biol."},{"key":"B55","doi-asserted-by":"publisher","first-page":"624317","DOI":"10.3389\/fphys.2021.624317","article-title":"Coordinated Reset Vibrotactile Stimulation Induces Sustained Cumulative Benefits in Parkinson's Disease","volume":"12","author":"Pfeifer","year":"2021","journal-title":"Front. Physiol."},{"key":"B56","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1007\/s00422-006-0066-8","article-title":"Control of Neuronal Synchrony by Nonlinear Delayed Feedback","volume":"95","author":"Popovych","year":"","journal-title":"Biol. Cybern."},{"key":"B57","doi-asserted-by":"publisher","first-page":"1977","DOI":"10.1142\/S0218127406015830","article-title":"Desynchronization and Decoupling of Interacting Oscillators by Nonlinear Delayed Feedback","volume":"16","author":"Popovych","year":"","journal-title":"Int. J. Bifurcation Chaos"},{"key":"B58","doi-asserted-by":"publisher","first-page":"164102","DOI":"10.1103\/PhysRevLett.94.164102","article-title":"Effective Desynchronization by Nonlinear Delayed Feedback","volume":"94","author":"Popovych","year":"2005","journal-title":"Phys. Rev. Lett."},{"key":"B59","doi-asserted-by":"publisher","first-page":"58","DOI":"10.3389\/fnhum.2012.00058","article-title":"Desynchronizing Electrical and Sensory Coordinated Reset Neuromodulation","volume":"6","author":"Popovych","year":"2012","journal-title":"Front. Hum. Neurosci."},{"key":"B60","doi-asserted-by":"publisher","first-page":"026204","DOI":"10.1103\/PhysRevE.82.026204","article-title":"Synchronization Control of Interacting Oscillatory Ensembles by Mixed Nonlinear Delayed Feedback","volume":"82","author":"Popovych","year":"2010","journal-title":"Phys. Rev. E"},{"key":"B61","doi-asserted-by":"publisher","first-page":"40002","DOI":"10.1209\/0295-5075\/80\/40002","article-title":"Controlling Synchrony in Oscillatory Networks with a Separate Stimulation-Registration Setup","volume":"80","author":"Pyragas","year":"2007","journal-title":"Europhys. Lett."},{"key":"B62","doi-asserted-by":"publisher","first-page":"84","DOI":"10.1002\/1531-8257(200001)15:1<84::aid-mds1014>3.0.co;2-k","article-title":"Multiple Oscillators Are Causing Parkinsonian and Essential Tremor","volume":"15","author":"Raethjen","year":"2000","journal-title":"Mov. Disord."},{"key":"B63","doi-asserted-by":"publisher","DOI":"10.1093\/brain\/awac012","article-title":"A Brain Network for Deep Brain Stimulation Induced Cognitive Decline in Parkinson's Disease","author":"Reich","year":"2022","journal-title":"Brain"},{"key":"B64","doi-asserted-by":"publisher","first-page":"114102","DOI":"10.1103\/PhysRevLett.92.114102","article-title":"Controlling Synchronization in an Ensemble of Globally Coupled Oscillators","volume":"92","author":"Rosenblum","year":"","journal-title":"Phys. Rev. Lett."},{"key":"B65","doi-asserted-by":"publisher","first-page":"041904","DOI":"10.1103\/PhysRevE.70.041904","article-title":"Delayed Feedback Control of Collective Synchrony: An Approach to Suppression of Pathological Brain Rhythms","volume":"70","author":"Rosenblum","year":"","journal-title":"Phys. Rev. E"},{"key":"B66","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1016\/S1383-8121(01)80012-9","article-title":"Chapter 9 Phase Synchronization: From Theory to Data Analysis","volume-title":"Neuro-Informatics and Neural Modelling, Handbook of Biological Physics","author":"Rosenblum","year":"2001"},{"key":"B67","doi-asserted-by":"publisher","first-page":"211","DOI":"10.1023\/b:jcns.0000025686.47117.67","article-title":"High Frequency Stimulation of the Subthalamic Nucleus Eliminates Pathological Thalamic Rhythmicity in a Computational Model","volume":"16","author":"Rubin","year":"2004","journal-title":"J. Comput. Neurosci."},{"key":"B68","doi-asserted-by":"publisher","first-page":"364","DOI":"10.1103\/physrevlett.86.364","article-title":"Equilibrium Properties of Temporally Asymmetric Hebbian Plasticity","volume":"86","author":"Rubin","year":"2001","journal-title":"Phys. Rev. Lett."},{"key":"B69","doi-asserted-by":"publisher","first-page":"041906","DOI":"10.1103\/PhysRevE.65.041906","article-title":"Plasticity and Learning in a Network of Coupled Phase Oscillators","volume":"65","author":"Seliger","year":"2002","journal-title":"Phys. Rev. E"},{"key":"B70","doi-asserted-by":"publisher","first-page":"1149","DOI":"10.1016\/S0896-6273(01)00542-6","article-title":"Rate, Timing, and Cooperativity Jointly Determine Cortical Synaptic Plasticity","volume":"32","author":"Sj\u00f6str\u00f6m","year":"2001","journal-title":"Neuron"},{"key":"B71","doi-asserted-by":"publisher","first-page":"919","DOI":"10.1038\/78829","article-title":"Competitive Hebbian Learning through Spike-timing-dependent Synaptic Plasticity","volume":"3","author":"Song","year":"2000","journal-title":"Nat. Neurosci."},{"key":"B72","doi-asserted-by":"publisher","first-page":"100","DOI":"10.1007\/s13311-018-0667-7","article-title":"Directional Deep Brain Stimulation","volume":"16","author":"Steigerwald","year":"2019","journal-title":"Neurotherapeutics"},{"key":"B73","doi-asserted-by":"publisher","first-page":"2515","DOI":"10.1152\/jn.90574.2008","article-title":"Neuronal Activity of the Human Subthalamic Nucleus in the Parkinsonian and Nonparkinsonian State","volume":"100","author":"Steigerwald","year":"2008","journal-title":"J. Neurophysiol."},{"key":"B74","doi-asserted-by":"publisher","first-page":"179","DOI":"10.1002\/mds.27223","article-title":"Coordinated Reset Vibrotactile Stimulation Shows Prolonged Improvement in Parkinson's Disease","volume":"33","author":"Syrkin-Nikolau","year":"2018","journal-title":"Mov. Disord."},{"key":"B75","doi-asserted-by":"crossref","DOI":"10.1007\/978-3-540-38161-7","volume-title":"Phase Resetting in Medicine and Biology: Stochastic Modelling and Data Analysis","author":"Tass","year":"1999"},{"key":"B76","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1007\/s00422-003-0425-7","article-title":"A Model of Desynchronizing Deep Brain Stimulation with a Demand-Controlled Coordinated Reset of Neural Subpopulations","volume":"89","author":"Tass","year":"","journal-title":"Biol. Cybernetics"},{"key":"B77","doi-asserted-by":"publisher","first-page":"137","DOI":"10.3233\/RNN-2012-110218","article-title":"Counteracting Tinnitus by Acoustic Coordinated Reset Neuromodulation","volume":"30","author":"Tass","year":"","journal-title":"Restor. Neurol. Neurosci."},{"key":"B78","doi-asserted-by":"publisher","first-page":"281","DOI":"10.1143\/PTPS.150.281","article-title":"Desynchronization by Means of a Coordinated Reset of Neural Sub-populations","volume":"150","author":"Tass","year":"","journal-title":"Prog. Theor. Phys. Suppl."},{"key":"B79","doi-asserted-by":"publisher","first-page":"102","DOI":"10.1007\/s00422-002-0322-5","article-title":"Desynchronization of Brain Rhythms with Soft Phase-Resetting Techniques","volume":"87","author":"Tass","year":"2002","journal-title":"Biol. Cybern."},{"key":"B80","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1209\/epl\/i2001-00117-6","article-title":"Effective Desynchronization by Means of Double-Pulse Phase Resetting","volume":"53","author":"Tass","year":"2001","journal-title":"Europhys. Lett."},{"key":"B81","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1007\/s00422-005-0028-6","article-title":"Long-term Anti-kindling Effects of Desynchronizing Brain Stimulation: A Theoretical Study","volume":"94","author":"Tass","year":"2006","journal-title":"Biol. Cybern."},{"key":"B82","doi-asserted-by":"publisher","first-page":"816","DOI":"10.1002\/ana.23663","article-title":"Coordinated Reset Has Sustained Aftereffects in Parkinsonian Monkeys","volume":"72","author":"Tass","year":"","journal-title":"Ann. Neurol."},{"key":"B83","doi-asserted-by":"publisher","first-page":"011902","DOI":"10.1103\/PhysRevE.80.011902","article-title":"Long-lasting Desynchronization in Rat Hippocampal Slice Induced by Coordinated Reset Stimulation","volume":"80","author":"Tass","year":"2009","journal-title":"Phys. Rev. E"},{"key":"B84","doi-asserted-by":"publisher","first-page":"301","DOI":"10.1143\/PTPS.139.301","article-title":"Stochastic Phase Resetting: a Theory for Deep Brain Stimulation","volume":"139","author":"Tass","year":"2000","journal-title":"Prog. Theor. Phys. Suppl."},{"key":"B85","doi-asserted-by":"publisher","first-page":"e1535","DOI":"10.7759\/cureus.1535","article-title":"Vibrotactile Coordinated Reset Stimulation for the Treatment of Neurological Diseases: Concepts and Device Specifications","volume":"9","author":"Tass","year":"2017","journal-title":"Cureus"},{"key":"B86","doi-asserted-by":"publisher","first-page":"016009","DOI":"10.1088\/1741-2560\/7\/1\/016009","article-title":"The Causal Relationship between Subcortical Local Field Potential Oscillations and Parkinsonian Resting Tremor","volume":"7","author":"Tass","year":"2010","journal-title":"J. Neural Eng."},{"key":"B87","doi-asserted-by":"publisher","first-page":"1495","DOI":"10.4103\/1673-5374.329001","article-title":"Vibrotactile Coordinated Reset Stimulation for the Treatment of Parkinson's Disease","volume":"17","author":"Tass","year":"2022","journal-title":"Neural Regen. Res."},{"key":"B88","doi-asserted-by":"publisher","first-page":"78","DOI":"10.1212\/WNL.60.1.78","article-title":"How Do Parkinsonian Signs Return after Discontinuation of Subthalamic DBS?","volume":"60","author":"Temperli","year":"2003","journal-title":"Neurology"},{"key":"B89","doi-asserted-by":"publisher","first-page":"2963","DOI":"10.1523\/jneurosci.22-07-02963.2002","article-title":"Activity Patterns in a Model for the Subthalamopallidal Network of the Basal Ganglia","volume":"22","author":"Terman","year":"2002","journal-title":"J. Neurosci."},{"key":"B90","volume-title":"The Rewiring Brain: A Computational Approach to Structural Plasticity in the Adult Brain","author":"Van Ooyen","year":"2017"},{"key":"B91","doi-asserted-by":"publisher","first-page":"124","DOI":"10.1038\/mp.2011.61","article-title":"Deep Brain Stimulation and the Role of Astrocytes","volume":"17","author":"Vedam-Mai","year":"2012","journal-title":"Mol. Psychiatry"},{"key":"B103","doi-asserted-by":"publisher","first-page":"716046","DOI":"10.3389\/fneur.2022.716046","article-title":"Shuffling Improves the Acute and Carryover Effect of Subthalamic Coordinated Reset Deep Brain Stimulation","volume":"13","author":"Wang","year":"2022","journal-title":"Front. Neurol."},{"key":"B92","doi-asserted-by":"publisher","first-page":"609","DOI":"10.1016\/j.brs.2016.03.014","article-title":"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","volume":"9","author":"Wang","year":"2016","journal-title":"Brain Stimulation"},{"key":"B93","doi-asserted-by":"crossref","first-page":"1286","DOI":"10.1109\/IEMBS.1989.96197","article-title":"Desynchronization of Epileptiform Activity by Phase Resetting","volume-title":"Images of the Twenty-First Century. Proceedings of the Annual International Engineering in Medicine and Biology Society","author":"Warman","year":"1989"},{"key":"B94","doi-asserted-by":"publisher","first-page":"3248","DOI":"10.1152\/jn.00697.2006","article-title":"Beta Oscillatory Activity in the Subthalamic Nucleus and its Relation to Dopaminergic Response in Parkinson's Disease","volume":"96","author":"Weinberger","year":"2006","journal-title":"J. Neurophysiol."},{"key":"B95","volume-title":"Parkinson\u2019s Disease: A Complete Guide for Patients and Families","author":"Weiner","year":"2001"},{"key":"B96","doi-asserted-by":"publisher","first-page":"50","DOI":"10.3389\/fnsys.2011.00050","article-title":"Chaotic Desynchronization as the Therapeutic Mechanism of Deep Brain Stimulation","volume":"5","author":"Wilson","year":"2011","journal-title":"Front. Syst. Neurosci."},{"key":"B97","doi-asserted-by":"publisher","first-page":"761","DOI":"10.1126\/science.887919","article-title":"Phase Control of Neural Pacemakers","volume":"197","author":"Winfree","year":"1977","journal-title":"Science"},{"key":"B98","doi-asserted-by":"crossref","first-page":"313","DOI":"10.23919\/ECC51009.2020.9143609","article-title":"Frequency Clusters in Adaptive Networks","volume-title":"2020 European Control Conference (ECC)","author":"Yanchuk","year":"2020"},{"key":"B99","doi-asserted-by":"publisher","first-page":"465","DOI":"10.1209\/epl\/i2003-10124-1","article-title":"Dynamical Clustering in Oscillator Ensembles with Time-dependent Interactions","volume":"65","author":"Zanette","year":"2004","journal-title":"Europhys. Lett."},{"key":"B100","doi-asserted-by":"publisher","first-page":"49","DOI":"10.3389\/fnsys.2015.00049","article-title":"Augmented Brain Function by Coordinated Reset Stimulation with Slowly Varying Sequences","volume":"9","author":"Zeitler","year":"2015","journal-title":"Front. Syst. Neurosci."},{"key":"B101","doi-asserted-by":"publisher","first-page":"512","DOI":"10.3389\/fphys.2018.00512","article-title":"Computationally Developed Sham Stimulation Protocol for Multichannel Desynchronizing Stimulation","volume":"9","author":"Zeitler","year":"2018","journal-title":"Front. Physiol."},{"key":"B102","doi-asserted-by":"publisher","first-page":"065202","DOI":"10.1103\/PhysRevE.71.065202","article-title":"Desynchronization of Coupled Electrochemical Oscillators with Pulse Stimulations","volume":"71","author":"Zhai","year":"2005","journal-title":"Phys. Rev. E"}],"container-title":["Frontiers in Network Physiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnetp.2022.864859\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,4,19]],"date-time":"2022-04-19T04:43:55Z","timestamp":1650343435000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fnetp.2022.864859\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,4,19]]},"references-count":103,"alternative-id":["10.3389\/fnetp.2022.864859"],"URL":"https:\/\/doi.org\/10.3389\/fnetp.2022.864859","relation":{},"ISSN":["2674-0109"],"issn-type":[{"value":"2674-0109","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,4,19]]},"article-number":"864859"}}