×

Nonlinear dynamics of neuronal excitability, oscillations, and coincidence detection. (English) Zbl 1402.92111

Summary: We review some widely studied models and firing dynamics for neuronal systems, both at the single cell and network level, and dynamical systems techniques to study them. In particular, we focus on two topics in mathematical neuroscience that have attracted the attention of mathematicians for decades: single-cell excitability and bursting. We review the mathematical framework for three types of excitability and onset of repetitive firing behavior in single-neuron models and their relation with Hodgkin’s classification in 1948 of repetitive firing properties. We discuss the mathematical dissection of bursting oscillations using fast/slow analysis and demonstrate the approach using single-cell and mean-field network models. Finally, we illustrate the properties of type III excitability in which case repetitive firing for constant or slow inputs is absent. Rather, firing is in response only to rapid enough changes in the stimulus. Our case study involves neuronal computations for sound localization for which neurons in the auditory brain stem perform extraordinarily precise coincidence detection with submillisecond temporal resolution.

MSC:

92C20 Neural biology

References:

[1] Agmon-Snir, The Role Of Dendrites In Auditory Coincidence Detection, Nature 393 (6682) pp 268– (1998) · doi:10.1038/30505
[2] Ashida, Sound Localization: Jeffress And Beyond, Curr. Opin. Neurobiol. 21 (5) pp 745– (2011) · doi:10.1016/j.conb.2011.05.008
[3] Azouz, Adaptive Coincidence Detection And Dynamic Gain Control In Visual Cortical Neurons In Vivo, Neuron 37 (3) pp 513– (2003) · doi:10.1016/S0896-6273(02)01186-8
[4] Borisyuk, Understanding Neuronal Dynamics By Geometrical Dissection Of Minimal Models, Models And Methods In Neurophysics (Les Houches Summer School pp 19– (2003)
[5] Borisyuk, Bifurcation Analysis Of A Neural Network Model, Biol. Cybern. 66 (4) pp 319– (1992) · Zbl 0737.92001 · doi:10.1007/BF00203668
[6] Brand, Precise Inhibition Is Essential For Microsecond Interaural Time Difference Coding, Nature 417 (6888) pp 543– (2002) · doi:10.1038/417543a
[7] Bressloff, Stochastic Neural Field Theory And The System-Size Expansion, Siam J. Appl. Math. 70 (5) pp 1488– · Zbl 1198.92007 · doi:10.1137/090756971
[8] Brette, Adaptive Exponential Integrate-And-Fire Model As An Effective Description Of Neuronal Activity, J. Neurophysiol. 94 (5) pp 3637– (2005) · doi:10.1152/jn.00686.2005
[9] Burkitt, A Review Of The Integrate-And-Fire Neuron Model: II. Inhomogeneous Synaptic Input And Network Properties, Biol. Cybern. 95 (2) pp 97– (2006) · Zbl 1161.92314 · doi:10.1007/s00422-006-0082-8
[10] Butera, Models Of Respiratory Rhythm Generation In The PrebÖTzinger Complex. I. Bursting Pacemaker Neurons, J. Neurophysiol. 82 (1) pp 382– (1999)
[11] Butera, Models Of Respiratory Rhythm Generation In The PrebÖTzinger Complex. Ii. Populations Of Coupled Pacemaker Neurons, J. Neurophysiol. 82 (1) pp 398– (1999)
[12] Carr, Are Neurons Adapted For Specific Computations? pp 245– (2006)
[13] Carr, A Circuit For Detection Of Interaural Time Differences In The Brain Stem Of The Barn Owl, J. Neurosci. 10 (10) pp 3227– (1990)
[14] Chay, Minimal Model For Membrane Oscillations In The Pancreatic Beta-Cell, Biophys. J. 42 (2) pp 181– (1983) · doi:10.1016/S0006-3495(83)84384-7
[15] Clay, A Simple Modification Of The Hodgkin And Huxley Equations Explains Type 3 Excitability In Squid Giant Axons, J. R. Soc. Interface 5 (29) pp 1421– (2008) · doi:10.1098/rsif.2008.0166
[16] Cole, Nerve Membrane Excitation Without Threshold, Proc. Natl. Acad. Sci. U.S.A. 65 (4) pp 884– (1970) · doi:10.1073/pnas.65.4.884
[17] Deville, Two Distinct Mechanisms Of Coherence In Randomly Perturbed Dynamical Systems, Phys. Rev. E (3) 72 (3) pp 10– (2005)
[18] Ermentrout, Interdisciplinary Applied Mathematics 35 (2010)
[19] Fitzhugh, Thresholds And Plateaus In The Hodgkin-Huxley Nerve Equations, J. Gen. Physiol. 43 (5) pp 867– (1960) · doi:10.1085/jgp.43.5.867
[20] Fitzhugh, Impulses And Physiological States In Theoretical Models Of Nerve Membrane, Biophys. J. 1 (6) pp 445– (1961) · doi:10.1016/S0006-3495(61)86902-6
[21] Gai, Slope-Based Stochastic Resonance: How Noise Enables Phasic Neurons To Encode Slow Signals, Plos Comput. Biol. 6 (6) pp E1000825– (2010) · doi:10.1371/journal.pcbi.1000825
[22] Goldberg, Kc Channels At The Axon Initial Segment Dampen Near-Threshold Excitability Of Neocortical Fast-Spiking Gabaergic Interneurons, Neuron 58 (3) pp 387– (2008) · doi:10.1016/j.neuron.2008.03.003
[23] Grothe, Mechanisms Of Sound Localization In Mammals, Physiol.Rev. 90 (3) pp 983– (2010) · doi:10.1152/physrev.00026.2009
[24] Guttman, Control Of Repetitive Firing In Squid Axon Membrane As A Model For A Neuroneoscillator, J. Physiol. 305 pp 377– (1980) · doi:10.1113/jphysiol.1980.sp013370
[25] Hanggi, Reaction-Rate Theory: Fifty Years After Kramers, Rev. Modern Phys. 62 (2) pp 251– (1990) · doi:10.1103/RevModPhys.62.251
[26] Harper, Optimal Neural Population Coding Of An Auditory Spatial Cue, Nature 430 (7000) pp 682– (2004) · doi:10.1038/nature02768
[27] Hodgkin, The Local Electric Changes Associated With Repetitive Action In A Non-Medullated Axon, J. Physiol. 107 (2) pp 165– (1948) · doi:10.1113/jphysiol.1948.sp004260
[28] Hodgkin, A Quantitative Description Of Membrane Current And Its Application To Conduction And Excitation In Nerve, J. Physiol. 117 (4) pp 500– (1952) · doi:10.1113/jphysiol.1952.sp004764
[29] Izhikevich, Dynamical Systems In Neuroscience: The Geometry Of Excitability And Bursting. Computational Neuroscience (2007)
[30] Izhikevich, Hybrid Spiking Models, Philos. Trans. R. Soc. Lond. Ser. A Math. Phys. Eng. Sci. 368 (1930) pp 5061– (2010) · Zbl 1211.37108 · doi:10.1098/rsta.2010.0130
[31] Jeffress, A Place Theory Of Sound Localization, J. Comp. Physiol. Psychol. 41 (1) pp 35– (1948) · doi:10.1037/h0061495
[32] Jercog, Asymmetric Excitatory Synaptic Dynamics Underlie Interaural Time Difference Processing In The Auditory System, Plos Biol. 8 (6) (2010) · doi:10.1371/journal.pbio.1000406
[33] Keener, Mathematical Physiology. Vol. I: Cellular Physiology (2009) · Zbl 1273.92017 · doi:10.1007/978-0-387-75847-3
[34] Konishi, Auditory Function: Neurobiological Basis Of Hearing pp 721– (1988)
[35] Kramers, Brownian Motion In A Field Of Force And The Diffusion Model Of Chemical Reactions, Physica 7 pp 284– (1940) · Zbl 0061.46405 · doi:10.1016/S0031-8914(40)90098-2
[36] Lim, Noise-Induced Transitions In Slow Wave Neuronal Dynamics, J. Comput. Neurosci. 28 (1) pp 1– (2010) · doi:10.1007/s10827-009-0178-y
[37] Mainen, Influence Of Dendritic Structure On Firing Pattern In Model Neocortical Neurons, Nature 382 (6589) pp 363– (1996) · doi:10.1038/382363a0
[38] Marchetti, Modeling Spontaneous Activity In The Developing Spinal Cord Using Activity-Dependent Variations Of Intracellular Chloride, J. Neurosci. 25 (14) pp 3601– (2005) · doi:10.1523/JNEUROSCI.4290-04.2005
[39] Mathews, Control Of Submillisecond Synaptic Timing In Binaural Coincidence Detectors By K(V)1 Channels, Nat. Neurosci. 13 (5) pp 601– (2010) · doi:10.1038/nn.2530
[40] Meng, Type III Excitability, Slope Sensitivity And Coincidence Detection, Discrete Contin. Dyn. Syst. 32 (8) pp 2729– (2012) · Zbl 1241.92013 · doi:10.3934/dcds.2012.32.2729
[41] Miller, The Dependence Of Impulse Propagation Speed On Firing Frequency, Dispersion, For The Hodgkin-Huxley Model, Biophys. J. 34 (2) pp 227– (1981) · doi:10.1016/S0006-3495(81)84847-3
[42] Morris, Voltage Oscillations In The Barnacle Giant Muscle Fiber, Biophys. J. 35 (1) pp 193– (1981) · doi:10.1016/S0006-3495(81)84782-0
[43] Moss, Stochastic Resonance And Sensory Information Processing: A Tutorial And Review Of Application, Clin. Neurophysiol. 115 (2) pp 267– (2004) · doi:10.1016/j.clinph.2003.09.014
[44] Nagumo, An Active Pulse Transmission Line Simulating A Nerve Axon, Proc. Ire 50 (10) pp 2061– (1962) · doi:10.1109/JRPROC.1962.288235
[45] Oertel, Detection Of Synchrony In The Activity Of Auditory Nerve Fibers By Octopus Cells Of The Mammalian Cochlear Nucleus, Proc. Natl. Acad. Sci. U.S.A. 97 (22) pp 11773– (2000) · doi:10.1073/pnas.97.22.11773
[46] Pinsky, Intrinsic And Network Rhythmogenesis In A Reduced Traub Model For Ca3 Neurons, J. Comput. Neurosci. 1 (1-2) pp 39– (1994) · doi:10.1007/BF00962717
[47] Platkiewicz, A Threshold Equation For Action Potential Initiation, Plos Comput.Biol. 6 (7) pp E1000850– (2010) · doi:10.1371/journal.pcbi.1000850
[48] Prescott, Pyramidal Neurons Switch From Integrators In Vitro To Resonators Under In Vivo-Like Conditions, J. Neurophysiol. 100 (6) pp 3030– (2008) · doi:10.1152/jn.90634.2008
[49] Rinzel, Excitation Dynamics: Insights From Simplified Membrane Models, Fed. Proc. 44 (15) pp 2944– (1985)
[50] Rinzel, A Formal Classification Of Bursting Mechanisms In Excitable Systems pp 1578– (1987) · Zbl 0665.92003
[51] Rinzel, Methods In Neuronal Modelling: From Synapses To Networks pp 251– (1998)
[52] Rinzel, Hopf Bifurcation To Repetitive Activity In Nerve, Siam J. Appl. Math. 43 (4) pp 907– (1983) · Zbl 0534.92015 · doi:10.1137/0143058
[53] Rothman, The Roles Potassium Currents Play In Regulating The Electrical Activity Of Ventral Cochlear Nucleus Neurons, J. Neurophysiol. 89 (6) pp 3097– (2003) · doi:10.1152/jn.00127.2002
[54] Schultheiss, Phase Response Curve Analysis Of A Full Morphological Globus Pallidus Neuron Model Reveals Distinct Perisomatic And Dendritic Modes Of Synaptic Integration, J. Neurosci. 30 (7) pp 2767– (2010) · doi:10.1523/JNEUROSCI.3959-09.2010
[55] Scott, Perisomatic Voltage-Gated Sodium Channels Actively Maintain Linear Synaptic Integration In Principal Neurons Of The Medial Superior Olive, J. Neurosci. 30 (6) pp 2039– (2010) · doi:10.1523/JNEUROSCI.2385-09.2010
[56] Svirskis, Enhancement Of Signal-To-Noise Ratio And Phase Locking For Small Inputs By A Low-Threshold Outward Current In Auditory Neurons, J. Neurosci. 22 (24) pp 11019– (2002)
[57] Svirskis, Sodium Along With Low-Threshold Potassium Currents Enhance Coincidence Detection Of Subthreshold Noisy Signals In Mso Neurons, J. Neurophysiol. 91 (6) pp 2465– (2004) · doi:10.1152/jn.00717.2003
[58] Tabak, Quantifying The Relative Contributions Of Divisive And Subtractive Feedback To Rhythm Generation, Plos Comput. Biol. 7 (4) (2011) · doi:10.1371/journal.pcbi.1001124
[59] Tabak, The Role Of Activity-Dependent Network Depression In The Expression And Self-Regulation Of Spontaneous Activity In The Developing Spinal Cord, J. Neurosci. 21 (22) pp 8966– (2001)
[60] Tabak, Modeling Of Spontaneous Activity In Developing Spinal Cord Using Activity-Dependent Depression In An Excitatory Network, J. Neurosci. 20 (8) pp 3041– (2000)
[61] Tateno, Threshold Firing Frequency-Current Relationships Of Neurons In Rat Somatosensory Cortex: Type 1 And Type 2 Dynamics, J. Neurophysiol. 92 (4) pp 2283– (2004) · doi:10.1152/jn.00109.2004
[62] Van Der Pol , B On Relaxation Oscillations 2 1926 11 978 992
[63] Wilent, Stimulus-Dependent Changes In Spike Threshold Enhance Feature Selectivity In Rat Barrel Cortex Neurons, J. Neurosci. 25 (11) pp 2983– (2005) · doi:10.1523/JNEUROSCI.4906-04.2005
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.