Bifurcations and multistability in the extended Hindmarsh–Rose neuronal oscillator

Abstract We report on the bifurcation analysis of an extended Hindmarsh–Rose (eHR) neuronal oscillator. We prove that Hopf bifurcation occurs in this system, when an appropriate chosen bifurcation parameter varies and reaches its critical value. Applying the normal form theory, we derive a formula to determine the direction of the Hopf bifurcation and the stability of bifurcating periodic flows. To observe this latter bifurcation and to illustrate its theoretical analysis, numerical simulations are performed. Hence, we present an explanation of the discontinuous behavior of the amplitude of the repetitive response as a function of system’s parameters based on the presence of the subcritical unstable oscillations. Furthermore, the bifurcation structures of the system are studied, with special care on the effects of parameters associated with the slow current and the slower dynamical process. We find that the system presents diversity of bifurcations such as period-doubling, symmetry breaking, crises and reverse period-doubling, when the afore mentioned parameters are varied in tiny steps. The complexity of the bifurcation structures seems useful to understand how neurons encode information or how they respond to external stimuli. Furthermore, we find that the extended Hindmarsh–Rose model also presents the multistability of oscillatory and silent regimes for precise sets of its parameters. This phenomenon plays a practical role in short-term memory and appears to give an evolutionary advantage for neurons since they constitute part of multifunctional microcircuits such as central pattern generators.

[1]  Enno de Lange,et al.  The Hindmarsh-Rose neuron model: bifurcation analysis and piecewise-linear approximations. , 2008, Chaos.

[2]  G. Zocchi,et al.  Local cooperativity mechanism in the DNA melting transition. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[3]  Kyandoghere Kyamakya,et al.  Regular oscillations, chaos, and multistability in a system of two coupled van der Pol oscillators: numerical and experimental studies , 2014 .

[4]  Martin Hasler,et al.  Predicting single spikes and spike patterns with the Hindmarsh–Rose model , 2008, Biological Cybernetics.

[5]  Maxim Bazhenov,et al.  Coexistence of tonic firing and bursting in cortical neurons. , 2006, Physical review. E, Statistical, nonlinear, and soft matter physics.

[6]  Andrey Shilnikov,et al.  Six Types of Multistability in a Neuronal Model Based on Slow Calcium Current , 2011, PloS one.

[7]  J. Rinzel,et al.  Control of repetitive firing in squid axon membrane as a model for a neuroneoscillator. , 1980, The Journal of physiology.

[8]  Andrey Shilnikov,et al.  Mechanism of bistability: tonic spiking and bursting in a neuron model. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[9]  J. Milton,et al.  Multistability in recurrent neural loops arising from delay. , 2000, Journal of neurophysiology.

[10]  Jinhu Lu,et al.  A New Chaotic Attractor Coined , 2002, Int. J. Bifurc. Chaos.

[11]  B. Hassard,et al.  Theory and applications of Hopf bifurcation , 1981 .

[12]  Vaithianathan Venkatasubramanian,et al.  Coexistence of four different attractors in a fundamental power system model , 1999 .

[13]  P. Bressloff,et al.  Bursting: The genesis of rhythm in the nervous system , 2005 .

[14]  Asaf Keller,et al.  Membrane Bistability in Olfactory Bulb Mitral Cells , 2001, The Journal of Neuroscience.

[15]  Teresa Ree Chay,et al.  Chaos in a three-variable model of an excitable cell , 1985 .

[16]  P. Holmes,et al.  Nonlinear Oscillations, Dynamical Systems, and Bifurcations of Vector Fields , 1983, Applied Mathematical Sciences.

[17]  Tao Liu,et al.  A Modified Lorenz System , 2006 .

[18]  Pérez-García,et al.  Ordered and chaotic behavior of two coupled van der Pol oscillators. , 1993, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[19]  R. D. Pinto,et al.  Recovery of hidden information through synaptic dynamics. , 2002 .

[20]  Alessandro Torcini,et al.  Dynamical phases of the Hindmarsh-Rose neuronal model: studies of the transition from bursting to spiking chaos. , 2007, Chaos.

[21]  G. R. Luckhurst,et al.  Director alignment by crossed electric and magnetic fields: a deuterium NMR study. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[22]  Andrey Shilnikov,et al.  Transition between tonic spiking and bursting in a neuron model via the blue-sky catastrophe. , 2005, Physical review letters.

[23]  B. Hassard Bifurcation of periodic solutions of Hodgkin-Huxley model for the squid giant axon. , 1978, Journal of theoretical biology.

[24]  H. Sompolinsky,et al.  Bistability of cerebellar Purkinje cells modulated by sensory stimulation , 2005, Nature Neuroscience.

[25]  J. Hindmarsh,et al.  A model of the nerve impulse using two first-order differential equations , 1982, Nature.

[26]  Martin Tobias Huber,et al.  Computer Simulations of Neuronal Signal Transduction: The Role of Nonlinear Dynamics and Noise , 1998 .

[27]  R. Genesio,et al.  On the dynamics of chaotic spiking-bursting transition in the Hindmarsh-Rose neuron. , 2009, Chaos.

[28]  C Bozzi,et al.  Branching fractions and CP asymmetries in B0-->pi0pi0, B+-->pi+pi0, and B+-->K+pi0 decays and isospin analysis of the B-->pipi system. , 2005, Physical review letters.

[29]  J. M. Gonzalez-Miranda Complex bifurcation Structures in the Hindmarsh-rose Neuron Model , 2007, Int. J. Bifurc. Chaos.

[30]  A. Shilnikov,et al.  Bistability of bursting and silence regimes in a model of a leech heart interneuron. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[31]  J. Yorke,et al.  Chaos, Strange Attractors, and Fractal Basin Boundaries in Nonlinear Dynamics , 1987, Science.

[32]  O Kiehn,et al.  Serotonin‐induced bistability of turtle motoneurones caused by a nifedipine‐sensitive calcium plateau potential. , 1989, The Journal of physiology.

[33]  Cerdeira,et al.  Dynamical behavior of the firings in a coupled neuronal system. , 1993, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[34]  Samuel Bowong,et al.  A New Adaptive Chaos Synchronization Principle for a Class of Chaotic Systems , 2005 .

[35]  Hansel,et al.  Synchronization and computation in a chaotic neural network. , 1992, Physical review letters.

[36]  A. Wolf,et al.  Determining Lyapunov exponents from a time series , 1985 .

[37]  F. Arecchi,et al.  Experimental evidence of subharmonic bifurcations, multistability, and turbulence in a Q-switched gas laser , 1982 .

[38]  J. Hindmarsh,et al.  A model of neuronal bursting using three coupled first order differential equations , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[39]  E. Lorenz Deterministic nonperiodic flow , 1963 .

[40]  A. Nayfeh,et al.  Applied nonlinear dynamics : analytical, computational, and experimental methods , 1995 .

[41]  Ulrike Feudel,et al.  Complex Dynamics in multistable Systems , 2008, Int. J. Bifurc. Chaos.

[42]  Pastor-Díaz,et al.  Dynamics of two coupled van der Pol oscillators. , 1995, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[43]  Shandelle M Henson,et al.  Multiple mixed-type attractors in a competition model , 2007, Journal of biological dynamics.

[44]  Boris S. Gutkin,et al.  Inhibition of rhythmic neural spiking by noise: the occurrence of a minimum in activity with increasing noise , 2009, Naturwissenschaften.

[45]  J. Yorke,et al.  Crises, sudden changes in chaotic attractors, and transient chaos , 1983 .

[46]  Ronald L. Calabrese,et al.  High Prevalence of Multistability of Rest States and Bursting in a Database of a Model Neuron , 2013, PLoS Comput. Biol..

[47]  Guanrong Chen,et al.  Analysis of a new chaotic system , 2005 .

[48]  Hilaire Bertrand Fotsin,et al.  The Combined Effect of Dynamic Chemical and Electrical Synapses in Time-Delay-Induced Phase-Transition to Synchrony in Coupled Bursting Neurons , 2014, Int. J. Bifurc. Chaos.

[49]  R. D. Pinto,et al.  Reliable circuits from irregular neurons: A dynamical approach to understanding central pattern generators , 2000, Journal of Physiology-Paris.

[50]  P Varona,et al.  Synchronous behavior of two coupled electronic neurons. , 2000, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[51]  J. Rinzel On repetitive activity in nerve. , 1978, Federation proceedings.

[52]  J. Hounsgaard,et al.  Development and regulation of response properties in spinal cord motoneurons , 2000, Brain Research Bulletin.

[53]  Grebogi,et al.  Critical exponents for crisis-induced intermittency. , 1987, Physical review. A, General physics.

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

[55]  Lu Qi-Shao,et al.  Codimension-Two Bifurcation Analysis in Hindmarsh--Rose Model with Two Parameters , 2005 .

[56]  B. Hassard,et al.  Bifurcation formulae derived from center manifold theory , 1978 .

[57]  Xiaobing Zhou,et al.  Hopf bifurcation analysis of the Liu system , 2008 .

[58]  Masoller Coexistence of attractors in a laser diode with optical feedback from a large external cavity. , 1994, Physical review. A, Atomic, molecular, and optical physics.

[59]  J. M. Gonzalez-Miranda,et al.  Block structured dynamics and neuronal coding. , 2005, Physical review. E, Statistical, nonlinear, and soft matter physics.

[60]  P. Arena,et al.  Locally active Hindmarsh–Rose neurons , 2006 .

[61]  J. M. Gonzalez-Miranda,et al.  Observation of a continuous interior crisis in the Hindmarsh-Rose neuron model. , 2003, Chaos.

[62]  Allen I. Selverston,et al.  Modeling observed chaotic oscillations in bursting neurons: the role of calcium dynamics and IP3 , 2000, Biological Cybernetics.

[63]  R. Abraham,et al.  A chaotic blue sky catastrophe in forced relaxation oscillations , 1986 .

[64]  Guanrong Chen,et al.  On a four-dimensional chaotic system , 2005 .

[65]  Guanrong Chen,et al.  YET ANOTHER CHAOTIC ATTRACTOR , 1999 .

[66]  C. Morris,et al.  Voltage oscillations in the barnacle giant muscle fiber. , 1981, Biophysical journal.

[67]  Eugene M. Izhikevich,et al.  Which model to use for cortical spiking neurons? , 2004, IEEE Transactions on Neural Networks.

[68]  Michael Peter Kennedy,et al.  Nonlinear analysis of the Colpitts oscillator and applications to design , 1999 .

[69]  G. Ermentrout,et al.  Analysis of neural excitability and oscillations , 1989 .

[70]  O. Rössler An equation for continuous chaos , 1976 .

[71]  A. Hodgkin,et al.  A quantitative description of membrane current and its application to conduction and excitation in nerve , 1952, The Journal of physiology.