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Wild oscillations in a nonlinear neuron model with resets. I: Bursting, spike-adding and chaos. (English) Zbl 1371.37032

Summary: In a series of two papers, we investigate the mechanisms by which complex oscillations are generated in a class of nonlinear dynamical systems with resets modeling the voltage and adaptation of neurons. This first paper presents mathematical analysis showing that the system can support bursts of any period as a function of model parameters, and that these are organized in a period-incrementing structure. In continuous dynamical systems with resets, such structures are complex to analyze. In the present context, we use the fact that bursting patterns correspond to periodic orbits of the adaptation map that governs the sequence of values of the adaptation variable at the resets. Using a slow-fast approach, we show that this map converges towards a piecewise linear discontinuous map whose orbits are exactly characterized. That map shows a period-incrementing structure with instantaneous transitions. We show that the period-incrementing structure persists for the full system with non-constant adaptation, but the transitions are more complex. We investigate the presence of chaos at the transitions.

MSC:

37C27 Periodic orbits of vector fields and flows
37E05 Dynamical systems involving maps of the interval
37N25 Dynamical systems in biology
92C20 Neural biology

References:

[1] B. Aulbach, On three definitions of chaos,, Nonlinear Dyn. Syst. Theory, 1, 23 (2001) · Zbl 0991.37010
[2] J. Banks, On Devaney’s definition of chaos,, Amer. Math. Monthly, 99, 332 (1992) · Zbl 0758.58019 · doi:10.2307/2324899
[3] I. Belykh, Synchronization of bursting neurons: What matters in the network topology,, Phys. Rev. Lett., 94 (2005) · doi:10.1103/PhysRevLett.94.188101
[4] L. S. Block, <em>Dynamics in One Dimension</em>,, Springer-Verlag (1992) · Zbl 0746.58007 · doi:10.1007/BFb0084762
[5] A. M. Blokh, Measurable dynamics of S-unimodal maps of the interval,, Ann. Sci. École Norm. Sup., 24, 545 (1991) · Zbl 0790.58024 · doi:10.24033/asens.1636
[6] R. Brette, Adaptive exponential integrate-and-fire model as an effective description of neuronal activity,, J. Neurophysiol., 94, 3637 (2005) · doi:10.1152/jn.00686.2005
[7] H. Bruin, Wild Cantor attractors exist,, Ann. of Math., 143, 97 (1996) · Zbl 0848.58016 · doi:10.2307/2118654
[8] N. Brunel, Lapicque’s 1907 paper: From frogs to integrate-and-fire,, Biol. Cybernet., 97, 337 (2007) · Zbl 1248.01018 · doi:10.1007/s00422-007-0190-0
[9] P. Collet, <em>Concepts and Results in Chaotic Dynamics: A Short Course</em>,, Theoretical and Mathematical Physics (2006) · Zbl 1107.37001
[10] S. Coombes, <em>Bursting: The Genesis of Rhythm in the Nervous System</em>,, World Scientific (2005) · Zbl 1094.92500 · doi:10.1142/5944
[11] P. de Maesschalck, Time analysis and entry-exit relation near planar turning points,, J. Differential Equations, 215, 225 (2005) · Zbl 1075.34048 · doi:10.1016/j.jde.2005.01.004
[12] W. de Melo, One-dimensional dynamics: The Schwarzian derivative and beyond,, Bull. Amer. Math. Soc. (N.S.), 18, 159 (1988) · Zbl 0651.58019 · doi:10.1090/S0273-0979-1988-15633-9
[13] S. J. Schiff, <em>One-Dimensional Dynamics</em>,, Results in Mathematics and Related Areas (3) (1993) · Zbl 1258.37046 · doi:10.1007/978-3-642-78043-1
[14] M. Desroche, Mixed-mode bursting oscillations: Dynamics created by a slow passage through spike-adding canard explosion in a square-wave burster,, Chaos, 23 (2013) · Zbl 1375.92014 · doi:10.1063/1.4827026
[15] A. Destexhe, Mechanisms underlying the synchronizing action of corticothalamic feedback through inhibition of thalamic relay cells,, J. Neurophysiol., 79, 999 (1998)
[16] R. L. Devaney, <em>An Introduction to Chaotic Dynamical Systems</em>,, Westview Press (2003) · Zbl 1025.37001
[17] F. Dumortier, Canard cycles and center manifolds,, Memoirs of the American Mathematical Soc., 121 (1996) · Zbl 0851.34057 · doi:10.1090/memo/0577
[18] E. Foxall, A contraction argument for two-dimensional spiking neuron models,, SIAM J. Appl. Dyn. Syst., 11, 540 (2012) · Zbl 1243.37065 · doi:10.1137/10081811X
[19] A. Granados, Border collision bifurcations of stroboscopic maps in periodically driven spiking models,, SIAM J. Appl. Dyn. Syst., 13, 1387 (2014) · Zbl 1322.37016 · doi:10.1137/13094637X
[20] J. Guckenheimer, Sensitive dependence to initial conditions for one-dimensional maps,, Comm. Math. Phys., 70, 133 (1979) · Zbl 0429.58012 · doi:10.1007/BF01982351
[21] P. Hartman, <em>Ordinary Differential Equations</em>,, Classics in Applied Mathematics (2002) · Zbl 1009.34001 · doi:10.1137/1.9780898719222
[22] L. D. Iasemidis, Review: Chaos theory and epilepsy,, The Neuroscientist, 2, 118 (1996) · doi:10.1177/107385849600200213
[23] B. Ibarz, Map-based models in neuronal dynamics,, Phys. Rep., 501, 1 (2011) · doi:10.1016/j.physrep.2010.12.003
[24] E. M. Izhikevich, Neural excitability, spiking, and bursting, Internat., J. Bifur. Chaos Appl., 10, 1171 (2000) · Zbl 1090.92505 · doi:10.1142/S0218127400000840
[25] M. Juan, Simple model of spiking neurons,, IEEE Trans. Neural Netw., 14, 1569 (2003)
[26] M. Juan, Which model to use for cortical spiking neurons?,, IEEE Trans. Neural Netw., 15, 1063 (2004)
[27] P. Hartman, <em>Dynamical Systems in Neuroscience: The Geometry of Excitability And Bursting</em>,, MIT Press (2007)
[28] P. Hartman, <em>Bursting</em>,, Scholarpedia (2006)
[29] E. M. Izhikevich, Large-scale model of mammalian thalamocortical systems,, Proc. Natl. Acad. Sci. USA, 105, 3593 (2007) · doi:10.1073/pnas.0712231105
[30] E. M. Izhikevich, Bursts as a unit of neural information: Selective communication via resonance,, Trends in Neurosciences, 26, 161 (2003) · doi:10.1016/S0166-2236(03)00034-1
[31] B. Jia, Dynamics of period-doubling bifurcation to chaos in the spontaneous neural firing patterns,, Cognitive Neurodynamics, 6, 89 (2012) · doi:10.1007/s11571-011-9184-7
[32] N. D. Jimenez, Locally contractive dynamics in generalized integrate-and-fire neurons,, SIAM J. Appl. Dyn. Syst., 12, 1474 (2013) · Zbl 1284.37030 · doi:10.1137/120900435
[33] R. Jolivet, A benchmark test for a quantitative assessment of simple neuron models,, J. Neurosci. Meth, 169, 417 (2008) · doi:10.1016/j.jneumeth.2007.11.006
[34] M. Juan, Interpreting a period-adding bifurcation scenario in neural bursting patterns using border-collision bifurcation in a discontinuous map of a slow control variable,, Chin. Phys. B, 19 (2010) · doi:10.1088/1674-1056/19/8/080513
[35] A. Kepecs, Information encoding and computation with spikes and bursts,, Network: Comp. Neural Syst., 14, 103 (2003) · doi:10.1080/net.14.1.103.118
[36] A. Kepecs, Bursting neurons signal input slope,, J. Neurosci., 22, 9053 (2002)
[37] L. Lapicque, Recherches quantitatifs sur l’excitation des nerfs traitee comme une polarisation,, J. Physiol. Paris, 9, 620 (1907)
[38] E. Lee, Uniqueness and stability of periodic bursting solutions,, J. Differential Equations, 158, 48 (1999) · Zbl 0935.34045 · doi:10.1016/S0022-0396(99)80018-7
[39] M. Levi, A period-adding phenomenon,, SIAM J. Appl. Math., 50, 943 (1990) · Zbl 0724.34041 · doi:10.1137/0150058
[40] T.-Y. Li, No division implies chaos,, Trans. Amer. Math. Soc., 273, 191 (1982) · Zbl 0495.58018 · doi:10.1090/S0002-9947-1982-0664037-3
[41] B. G. Lindsey, Computational models and emergent properties of respiratory neural networks,, Compr. Physiol. (2012) · doi:10.1002/cphy.c110016
[42] E. Manica, First return maps for the dynamics of synaptically coupled conditional bursters,, Biol. Cybern., 103, 87 (2010) · Zbl 1266.37052 · doi:10.1007/s00422-010-0399-1
[43] E. Marder, Motor pattern generation,, Curr. Opin. Neurobiol., 10, 691 (2000) · doi:10.1016/S0959-4388(00)00157-4
[44] E. Marder, Central pattern generators and the control of rhythmic movements,, Curr. Biol., 11 (2001) · doi:10.1016/S0960-9822(01)00581-4
[45] G. S. Medvedev, Reduction of a model of an excitable cell to a one-dimensional map,, Phys. D, 202, 37 (2005) · Zbl 1144.92307 · doi:10.1016/j.physd.2005.01.021
[46] H. G. Meijer, Modeling focal epileptic activity in the Wilson-Cowan model with depolarization block,, J. Math. Neurosci., 5 (2015) · Zbl 1357.92013 · doi:10.1186/s13408-015-0019-4
[47] J. Milnor, On the concept of attractor,, Comm. Math. Phys., 99, 177 (1985) · Zbl 0595.58028 · doi:10.1007/BF01212280
[48] J. Milnor, On iterated maps of the interval,, in Dynamical Systems. Lecture Notes in Math., 1342, 465 (1988) · Zbl 0664.58015 · doi:10.1007/BFb0082847
[49] M. Misiurewicz, Horseshoes for continuous mappings of the interval,, in Dynamical Systems, 125 (1980) · Zbl 0459.54031
[50] R. Naud, Firing patterns in the adaptive exponential integrate-and-fire model,, Biol. Cybern., 99, 335 (2008) · Zbl 1161.92012 · doi:10.1007/s00422-008-0264-7
[51] A.-M. M. Oswald, Parallel processing of sensory input by bursts and isolated spikes,, J. Neurosci., 24, 4351 (2004) · doi:10.1523/JNEUROSCI.0459-04.2004
[52] K. Pakdaman, Single neuron with recurrent excitation: Effect of the transmission delay,, Neur. Netw., 9, 797 (1996) · doi:10.1016/0893-6080(95)00097-6
[53] D. A. Prince, Neurophysiology of epilepsy,, Ann. Rev. Neurosci., 1, 395 (1978) · doi:10.1146/annurev.ne.01.030178.002143
[54] S. R. Pring, The dynamics of regularized discontinuous maps with applications to impacting systems,, SIAM J. Appl. Dyn. Syst., 9, 188 (2010) · Zbl 1192.37071 · doi:10.1137/080743123
[55] J. Rinzel, A formal classification of bursting mechanisms in excitable systems,, in Mathematical Topics in Population Biology, 71, 267 (1987) · Zbl 0646.92004 · doi:10.1007/978-3-642-93360-8_26
[56] J. Rinzel, A one-variable map analysis of bursting in the Belousov-Zhabotinskii reaction,, in Oscillations in Mathematical Biology (Garden City, 51, 1 (1982) · doi:10.1007/978-3-642-46480-5_1
[57] J. E. Rubin, Wild oscillations in a nonlinear neuron model with resets: (II) Mixed-mode oscillations,, Discr. Cont. Dyn. Sys. B. (2017) · Zbl 1375.34075
[58] J. E. Rubin, Basal ganglia activity patterns in parkinsonism and computational modeling of their downstream effects,, Europ. J. Neurosci., 36, 2213 (2012) · doi:10.1111/j.1460-9568.2012.08108.x
[59] N. F. Rulkov, Oscillations in large-scale cortical networks: Map-based model,, J. Comput. Neurosci., 17, 203 (2004) · doi:10.1023/B:JCNS.0000037683.55688.7e
[60] N. F. Rulkov, Modeling of spiking-bursting neural behavior using two-dimensional map,, Phys. Rev. E, 65 (2002) · Zbl 1244.34077 · doi:10.1103/PhysRevE.65.041922
[61] I. Samengo, Conversion of phase information into a spike-count code by bursting neurons,, PLoS One, 5 (2010) · doi:10.1371/journal.pone.0009669
[62] S. J. Schiff, Controlling chaos in the brain,, Nature, 370, 615 (1994) · doi:10.1038/370615a0
[63] W. Schultz, Predictive reward signal of dopamine neurons,, J. Neurophysiol., 80, 1 (1998)
[64] S. Silverman, On maps with dense orbits and the definition of chaos,, Rocky Mountain J. Math., 22, 353 (1992) · Zbl 0758.58024 · doi:10.1216/rmjm/1181072815
[65] J. Tabak, Fast-activating voltage-and calcium-dependent potassium (BK) conductance promotes bursting in pituitary cells: a dynamic clamp study,, J. Neurosci., 31, 16855 (2011)
[66] H. Thunberg, Periodicity versus chaos in one-dimensional dynamics,, SIAM Rev., 43, 3 (2001) · Zbl 1049.37027 · doi:10.1137/S0036144500376649
[67] J. Touboul, Bifurcation analysis of a general class of nonlinear integrate-and-fire neurons,, SIAM J. Appl. Math., 68, 1045 (2008) · Zbl 1149.34027 · doi:10.1137/070687268
[68] J. Touboul, Importance of the cutoff value in the quadratic adaptive integrate-and-fire model,, Neural Comput., 21, 2114 (2009) · Zbl 1167.92008 · doi:10.1162/neco.2009.09-08-853
[69] J. Touboul, Dynamics and bifurcations of the adaptive exponential integrate-and-fire model,, Biol. Cybern., 99, 319 (2008) · Zbl 1161.92016 · doi:10.1007/s00422-008-0267-4
[70] S. van Strien, Spiking dynamics of bidimensional integrate-and-fire neurons,, SIAM J. Appl. Dyn. Syst., 8, 1462 (2009) · Zbl 1204.37019 · doi:10.1137/080742762
[71] S. van Strien, Hyperbolicity and invariant measures for general C2 interval maps satisfying the Misiurewicz condition,, Comm. Math. Phys., 128, 437 (1990) · Zbl 0702.58020 · doi:10.1007/BF02096868
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