Phase resetting curves allow for simple and accurate prediction of robust N:1 phase locking for strongly coupled neural oscillators.

Existence and stability criteria for harmonic locking modes were derived for two reciprocally pulse coupled oscillators based on their first and second order phase resetting curves. Our theoretical methods are general in the sense that no assumptions about the strength of coupling, type of synaptic coupling, and model are made. These methods were then tested using two reciprocally inhibitory Wang and Buzsáki model neurons. The existence of bands of 2:1, 3:1, 4:1, and 5:1 phase locking in the relative frequency parameter space was predicted correctly, as was the phase of the slow neuron's spike within the cycle of the fast neuron in which it occurred. For weak coupling the bands are very narrow, but strong coupling broadens the bands. The predictions of the pulse coupled method agreed with weak coupling methods in the weak coupling regime, but extended predictability into the strong coupling regime. We show that our prediction method generalizes to pairs of neural oscillators coupled through excitatory synapses, and to networks of multiple oscillatory neurons. The main limitation of the method is the central assumption that the effect of each input dies out before the next input is received.

[1]  Eric Shea-Brown,et al.  On the Phase Reduction and Response Dynamics of Neural Oscillator Populations , 2004, Neural Computation.

[2]  A. Pérez-Villalba Rhythms of the Brain, G. Buzsáki. Oxford University Press, Madison Avenue, New York (2006), Price: GB £42.00, p. 448, ISBN: 0-19-530106-4 , 2008 .

[3]  Carmen C. Canavier,et al.  Pulse coupled oscillators , 2007, Scholarpedia.

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

[5]  N. Moore,et al.  A Review of EEG Biofeedback Treatment of Anxiety Disorders , 2000, Clinical EEG.

[6]  S. Lowen The Biophysical Journal , 1960, Nature.

[7]  W. Klimesch,et al.  The interplay between theta and alpha oscillations in the human electroencephalogram reflects the transfer of information between memory systems , 2002, Neuroscience Letters.

[8]  P. Stein Application of the mathematics of coupled oscillator systems to the analysis of the neural control of locomotion. , 1977, Federation proceedings.

[9]  Niels Birbaumer,et al.  Cross-frequency phase synchronization: A brain mechanism of memory matching and attention , 2008, NeuroImage.

[10]  G. Ermentrout n:m Phase-locking of weakly coupled oscillators , 1981 .

[11]  R. Traub,et al.  Inhibition-based rhythms: experimental and mathematical observations on network dynamics. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[12]  G. Buzsáki,et al.  Gamma Oscillation by Synaptic Inhibition in a Hippocampal Interneuronal Network Model , 1996, The Journal of Neuroscience.

[13]  R. Pérez,et al.  Fine Structure of Phase Locking , 1982 .

[14]  John W. Clark,et al.  Control of multistability in ring circuits of oscillators , 1999, Biological Cybernetics.

[15]  Astrid A Prinz,et al.  Predictions of phase-locking in excitatory hybrid networks: excitation does not promote phase-locking in pattern-generating networks as reliably as inhibition. , 2009, Journal of neurophysiology.

[16]  A. Grassino,et al.  Respiratory phase locking during mechanical ventilation in anesthetized human subjects. , 1986, The American journal of physiology.

[17]  Carmen C Canavier,et al.  Functional phase response curves: a method for understanding synchronization of adapting neurons. , 2009, Journal of neurophysiology.

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

[19]  Jürgen Kurths,et al.  Phase Synchronization in Regular and Chaotic Systems , 2000, Int. J. Bifurc. Chaos.

[20]  P van Leeuwen,et al.  Musical rhythms in heart period dynamics: a cross-cultural and interdisciplinary approach to cardiac rhythms. , 1999, American journal of physiology. Heart and circulatory physiology.

[21]  John W. Clark,et al.  Phase response characteristics of model neurons determine which patterns are expressed in a ring circuit model of gait generation , 1997, Biological Cybernetics.

[22]  L. Glass,et al.  A simple model for phase locking of biological oscillators , 1979, Journal of mathematical biology.

[23]  Sorinel Adrian Oprisan,et al.  Prediction of Entrainment And 1:1 Phase-Locked Modes in Two-Neuron Networks Based on the Phase Resetting Curve Method , 2008, The International journal of neuroscience.

[24]  Adriano B. L. Tort,et al.  On the formation of gamma-coherent cell assemblies by oriens lacunosum-moleculare interneurons in the hippocampus , 2007, Proceedings of the National Academy of Sciences.

[25]  G. Ermentrout,et al.  Multiple pulse interactions and averaging in systems of coupled neural oscillators , 1991 .

[26]  A. Hodgkin The local electric changes associated with repetitive action in a non‐medullated axon , 1948, The Journal of physiology.

[27]  M D Prokhorov,et al.  Synchronization between main rhythmic processes in the human cardiovascular system. , 2003, Physical review. E, Statistical, nonlinear, and soft matter physics.

[28]  Carmen C. Canavier,et al.  Using phase resetting to predict 1:1 and 2:2 locking in two neuron networks in which firing order is not always preserved , 2008, Journal of Computational Neuroscience.

[29]  Stein Ps Application of the mathematics of coupled oscillator systems to the analysis of the neural control of locomotion. , 1977 .

[30]  R. I. Kitney,et al.  Transient phase locking patterns among respiration, heart rate and blood pressure during cardiorespiratory synchronisation in humans , 2000, Medical and Biological Engineering and Computing.

[31]  Bard Ermentrout,et al.  Simulating, analyzing, and animating dynamical systems - a guide to XPPAUT for researchers and students , 2002, Software, environments, tools.

[32]  Juergen Kurths,et al.  Phase Synchronization in Regular and Chaotic Systems: a Tutorial , 1999 .

[33]  J. Aschoff Naps as Integral Parts of the Wake Time within the Human Sleep-Wake Cycle , 1994, Journal of biological rhythms.

[34]  F K Skinner,et al.  Using heterogeneity to predict inhibitory network model characteristics. , 2005, Journal of neurophysiology.

[35]  Nancy Kopell,et al.  Synchronization of Strongly Coupled Excitatory Neurons: Relating Network Behavior to Biophysics , 2003, Journal of Computational Neuroscience.

[36]  David Friedman,et al.  Cross-frequency phase coupling of brain rhythms during the orienting response , 2008, Brain Research.

[37]  John W. Clark,et al.  Multimodal behavior in a four neuron ring circuit: mode switching , 2004, IEEE Transactions on Biomedical Engineering.

[38]  Visarath In,et al.  Multifrequency synthesis using two coupled nonlinear oscillator arrays. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[39]  Myongkeun Oh,et al.  Loss of phase-locking in non-weakly coupled inhibitory networks of type-I model neurons , 2008, Journal of Computational Neuroscience.

[40]  Corey D. Acker,et al.  Synchronization in hybrid neuronal networks of the hippocampal formation. , 2005, Journal of neurophysiology.

[41]  H. Freund,et al.  The cerebral oscillatory network of parkinsonian resting tremor. , 2003, Brain : a journal of neurology.

[42]  Miles A. Whittington,et al.  Low-Dimensional Maps Encoding Dynamics in Entorhinal Cortex and Hippocampus , 2006, Neural Computation.

[43]  A. Prinz,et al.  Phase resetting and phase locking in hybrid circuits of one model and one biological neuron. , 2004, Biophysical journal.

[44]  D. Bramble,et al.  Running and breathing in mammals. , 1983, Science.

[45]  Carmen C. Canavier,et al.  Phase response curve , 2006, Scholarpedia.

[46]  J Grasman The mathematical modeling of entrained biological oscillators. , 1984, Bulletin of mathematical biology.

[47]  H. Bergman,et al.  Pathological synchronization in Parkinson's disease: networks, models and treatments , 2007, Trends in Neurosciences.