Abstract
Although the bursting patterns with spike undershoot are involved with the achievement of physiological or cognitive functions of brain with synaptic noise, noise induced-coherence resonance (CR) from resting state or subthreshold oscillations instead of bursting has been widely identified to play positive roles in information process. Instead, in the present paper, CR characterized by the increase firstly and then decease of peak value of power spectrum of spike trains is evoked from a bursting pattern with spike undershoot, which means that the minimal membrane potential within burst is lower than that of the subthreshold oscillations between bursts, while CR cannot be evoked from the bursting pattern without spike undershoot. With bifurcations and fast-slow variable dissection method, the bursting patterns with and without spike undershoot are classified into “Sub-Hopf/Fold” bursting and “Fold/Homoclinic” bursting, respectively. For the bursting with spike undershoot, the trajectory of the subthreshold oscillations is very close to that of the spikes within burst. Therefore, noise can induce more spikes from the subthreshold oscillations and modulate the bursting regularity, which leads to the appearance of CR. For the bursting pattern without spike undershoot, the trajectory of the quiescent state is not close to that of the spikes within burst, and noise cannot induce spikes from the quiescent state between bursts, which is cause for non-CR. The result provides a novel case of CR phenomenon and extends the scopes of CR concept, presents that noise can enhance rather than suppress information of the bursting patterns with spike undershoot, which are helpful for understanding the dynamics and the potential physiological or cognitive functions of the nerve fiber or brain neurons with such bursting patterns.
Similar content being viewed by others
References
Benzi R, Sutera A, Vulpiani A (1981) Stochastic resonance in climatic change. J Phys A 14:L453–L457. https://doi.org/10.1111/j.2153-3490.1982.tb01787.x
Braun HA, Wissing H, Schäfer K, Hirsch MC (1994) Oscillation and noise determine signal transduction in shark multimodal sensory cells. Nature 367:270–273. https://doi.org/10.1038/367270a0
Cagnan H, Mallet N, Moll CKE, Gulberti A, Holt AB, Westphal M, Gerloff C, Engel AK, Hamel W, Magill PJ, Brown P, Sharott A (2019) Temporal evolution of beta bursts in the parkinsonian cortical and basal ganglia network. Proc Natl Acad Sci USA 116:16095–16104. https://doi.org/10.1073/pnas.1819975116
Cao B, Guan LN, Gu HG (2018) Bifurcation mechanism of not increase but decrease of spike numbers within a neural burst induced by excitatory effect. Acta Phys Sin 67(24):240502. https://doi.org/10.7498/aps.67.20181675(in Chinese)
Del Negro CA, Hsiao CF, Chandler SH, Garfinkel A (1998) Evidence for a novel bursting mechanism in rodent trigeminal neurons. Biophys J 75:174–182. https://doi.org/10.1016/S0006-3495(98)77504-6
Douglass JK, Wilkens L, Pantazelou E, Moss F (1993) Noise enhancement of information transfer in crayfish mechanoreceptors by stochastic resonance. Nature 365:337–340. https://doi.org/10.1038/365337a0
Ermentrout B (2002) Simulating, analyzing, and animating dynamical systems: a guide to XPPAUT for researchers and students. SIAM, Philadelphia
Faisal AA, Selen LP, Wolpert DM (2008) Noise in the nervous system. Nat Rev Neurosci 9(4):292–303. https://doi.org/10.1038/nrn2258
Gammaitoni L, Hanggi P, Jung P, Marchesoni F (1998) Stochastic resonance. Rev Mod Phys 70:223–287. https://doi.org/10.1103/RevModPhys.70.223
Gireesh E, Plenz D (2008) Neuronal avalanches organize as nested theta- and beta/gamma-oscillations during development of cortical layer 2/3. Proc Natl Acad Sci USA 105:7576–7581. https://doi.org/10.1073/pnas.0800537105
Gu HG, Ren W, Lu QS, Wu SG, Yang MH, Chen WJ (2001) Integer multiple spiking in neural pacemakers without external periodic stimulation. Phys Lett A 285:63–68. https://doi.org/10.1016/S0375-9601(01)00278-X
Gu HG, Yang MH, Li L, Liu ZQ, Ren W (2002) Experimental observation of the stochastic bursting caused by coherence resonance in a neural pacemaker. NeuroReport 13(13):1657–1660. https://doi.org/10.1097/00001756-200209160-00018
Gu HG, Zhao ZG, Jia B, Chen SG (2015) Dynamics of on-off neural firing patterns and stochastic effects near a sub-critical Hopf bifurcation. PloS One 10(4):e0121028. https://doi.org/10.1371/journal.pone.0121028
Guttman R, Barnhill R (1970) Oscillation and repetitive firing in squid axons: comparison of experiments with computations. J Gen Physiol 55:104–118. https://doi.org/10.1085/jgp.55.1.104
Guttman R, Lewis S, Rinzel J (1980) Control of repetitive firing in squid axon membrane as a model for a neuroneoscillator. J Physiol 305:377–395. https://doi.org/10.1113/jphysiol.1980.sp013370
Izhikevich EM (2000a) Subcritical elliptic bursting of Bautin type. SIAM J Appl Math 60(2):503–535. https://doi.org/10.1137/S003613999833263X
Izhikevich EM (2000b) Neural excitability, spiking and bursting. Int J Bifurc Chaos 10(6):1171–1266. https://doi.org/10.1142/S0218127400000840
Izhikevich EM (2007) Dynamical systems in neuroscience: the geometry of excitability and bursting. MIT Press, London
Jia B, Gu HG (2012) Identifying type I excitability using dynamics of stochastic neural firing patterns. Cogn Neurodyn 6(6):485–497. https://doi.org/10.1007/s11571-012-9209-x
Jia B, Gu HG (2017) Dynamics and physiological roles of stochastic neural firing patterns near bifurcation points. Int J Bifurc Chaos 27(7):1750113. https://doi.org/10.1142/S0218127417501139
Jia B, Gu HG, Xue L (2017) A basic bifurcation structure from bursting to spiking of the injured nerve fibers in a two-dimensional parameter space. Cogn Neurodyn 11(2):189–200. https://doi.org/10.1007/s11571-017-9422-8
Kim JH, Lee HJ, Min CH, Lee KJ (2015) Coherence resonance in bursting neural networks. Phys Rev E 92(4):042701. https://doi.org/10.1103/PhysRevE.92.042701
Kim JH, Lee HJ, Choi W, Lee KJ (2019) Encoding information into autonomously bursting neural network with pairs of time-delayed pulses. Sci Rep 9:1394. https://doi.org/10.1038/s41598-018-37915-7
Levin JE, Miller JP (1996) Broadband neural encoding in the cricket cereal sensory system enhanced by stochastic resonance. Nature 380:165–168. https://doi.org/10.1038/380165a0
Li YY, Gu HG (2017) The distinct stochastic and deterministic dynamics between period-adding and period-doubling bifurcations of neural bursting patterns. Nonlinear Dyn 87(4):2541–2562. https://doi.org/10.1007/s11071-016-3210-6
Li YY, Gu HG, Ding XL (2019) Bifurcations of enhanced neuronal bursting activities induced by the negative current mediated by inhibitory autapse. Nonlinear Dyn 97(4):2091–2105. https://doi.org/10.1007/s11071-019-05106-2
Lindnera B, García-Ojalvob J, Neiman A, Schimansky-Geiere L (2004) Effects of noise in excitable systems. Phys Rep 392:321–424. https://doi.org/10.1016/j.physrep.2003.10.015
Lisman JE (1997) Bursts as a unit of neural information: making unreliable synapses reliable. Trends Neurosci 20(1):38–43. https://doi.org/10.1016/S0166-2236(96)10070-9
Longtin A (1997) Autonomous stochastic resonance in bursting neurons. Phys Rev E 55(1):868–876. https://doi.org/10.1103/PhysRevE.55.868
Longtin A, Bulsara A, Moss F (1991) Time-interval sequences in bistable systems and the noise-induced transmission of information by sensory neurons. Phys Rev Lett 67(5):656–659. https://doi.org/10.1103/PhysRevLett.67.656
Mannella R, Palleschi V (1989) Fast and precise algorithm for compute simulation of stochastic differential equations. Phys Rev A 40:3381–3386. https://doi.org/10.1103/PhysRevA.40.3381
McDonnell MD, Abbott D (2009) What is stochastic resonance? Definitions, misconceptions, debates, and its relevance to biology. PLoS Comput Biol 5(5):e1000348. https://doi.org/10.1371/journal.pcbi.1000348
McDonnell MD, Iannella N, To MS, Tuckwell HC, Jost J, Gutkin BS, Ward LM (2015) A review of methods for identifying stochastic resonance in simulations of single neuron models. Network 26(2):35–71. https://doi.org/10.3109/0954898X.2014.990064
Pikovsky AS, Kurths J (1997) Coherence resonance in a noise-driven excitable system. Phys Rev Lett 78:775–778. https://doi.org/10.1103/PhysRevLett.78.775
Serafin M, Williams S, Khateb A, Fort P, Muhlethaler M (1996) Rhythmic firing of medial septum non-cholinergic neurons. Neuroscience 75:671–675. https://doi.org/10.1016/0306-4522(96)00349-1
Simakov DS, Pérez-Mercader J (2013) Noise induced oscillations and coherence resonance in a generic model of the nonisothermal chemical oscillator. Sci Rep 3:2404. https://doi.org/10.1038/srep02404
Sun GQ, Jusup M, Jin Z, Wang Y, Wang Z (2016) Pattern transitions in spatial epidemics: mechanisms and emergent properties. Phys Life Rev 19:43–73. https://doi.org/10.1016/j.plrev.2016.08.002
Wang XJ (2002) Pacemaker neurons for the theta rhythm and their synchronization in the septohippocampal reciprocal loop. J Neurophysiol 87:889–900. https://doi.org/10.1152/jn.00135.2001
Wang XJ (2010) Neurophysiological and computational principles of cortical rhythms in cognition. Physiol Rev 90:1195–1268. https://doi.org/10.1152/physrev.00035.2008
Wu FQ, Gu HG (2020) Bifurcations of negative responses to positive feedback current mediated by memristor in neuron model with bursting patterns. Int J Bifurc Chaos 30(4):2030009. https://doi.org/10.1142/S0218127420300098
Wu J, Ma SJ (2019) Coherence resonance of the spiking regularity in a neuron under electromagnetic radiation. Nonlinear Dyn 96:1895–1908. https://doi.org/10.1007/s11071-019-04892-z
Wu SG, Ren W, He KF, Huang ZQ (2001) Burst and coherence resonance in Rose–Hindmarsh model induced by additive noise. Phys Lett A 279(5–6):347–354. https://doi.org/10.1016/S0375-9601(01)00020-2
Wu FQ, Gu HG, Li YY (2019) Inhibitory electromagnetic induction current induced enhancement instead of reduction of neural bursting activities. Commun Nonlinear Sci Numer Simul 79:104924. https://doi.org/10.1016/j.cnsns.2019.104924
Zhang XJ, Gu HG, Guan LN (2019) Stochastic dynamics of conduction failure of action potential along nerve fiber with Hopf bifurcation. Sci China Technol Sci 62(9):1502–1511. https://doi.org/10.1007/s11431-018-9515-4
Acknowledgements
This work was supported by the National Natural Science Foundation of China under Grant Nos. 11872276 and 11572225, and 11762001.
Author information
Authors and Affiliations
Contributions
HG conceived the experiments, BC, RW, HG, and YL conducted the experiments, HG, BC, RW, and YL analyzed the results, BC and HG written the paper. All authors reviewed the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing financial interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Cao, B., Wang, R., Gu, H. et al. Coherence resonance for neuronal bursting with spike undershoot. Cogn Neurodyn 15, 77–90 (2021). https://doi.org/10.1007/s11571-020-09595-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11571-020-09595-5