Spike-frequency adaptation of a two-compartment neuron modulated by extracellular electric fields

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• 作者：Guosheng Yi ; Jiang Wang ; Kai-Ming Tsang ; Xile Wei ; Bin Deng…
• 关键词：Extracellular electric field ; Spike ; frequency adaptation ; Two ; compartment neuron ; Spike initiation dynamic ; Bifurcation ; Morphological parameter
• 刊名：Biological Cybernetics
• 出版年：2015
• 出版时间：June 2015
• 年：2015
• 卷：109
• 期：3
• 页码：287-306
• 全文大小：6,393 KB
• 参考文献：Benda J, Herz AV (2003) A universal model for spike-frequency adaptation. Neural Comput 15(11):2523鈥?564View Article PubMed
  Benda J, Longtin A, Maler L (2005) Spike-frequency adaptation separates transient communication signals from background oscillations. J Neurosci 25(9):2312鈥?321View Article PubMed
  Benda J, Maler L, Longtin A (2010) Linear versus nonlinear signal transmission in neuron models with adaptation currents or dynamic thresholds. J Neurophysiol 104(5):2806鈥?820View Article PubMed
  Bikson M, Inoue M, Akiyama H, Deans JK, Fox JE, Miyakawa H, Jefferys GR (2004) Effects of uniform extracellular DC electric fields on excitability in rat hippocampal slices in vitro. J Physiol 557(Pt 1):175鈥?0View Article PubMed Central PubMed
  Br酶ns M, Krupa M, Wechselberger M (2006) Mixed mode oscillations due to the generalized canard phenomenon. Fields Inst Commun 49:39鈥?3
  Brown DA, Adams PR (1980) Muscarinic suppression of a novel voltage-sensitive K\(^{+}\) current in a vertebrate neurone. Nature 283(5748):673鈥?76View Article PubMed
  Carnevale NT, Hines M (2005) The NEURON Book. Cambridge University Press, Cambridge
  Chan CY, Hounsgaard J, Nicholson C (1988) Effects of electric fields on transmembrane potential and excitability of turtle cerebellar Purkinje cells in vitro. J Physiol 402:751鈥?1View Article PubMed Central PubMed
  Chan CY, Nicholson C (1986) Modulation by applied electric fields of Purkinje and stellate cell activity in the isolated turtle cerebellum. J Physiol 371:89鈥?14View Article PubMed Central PubMed
  Desroches M, Guckenheimer J, Krauskop B, Kuehn C, Osinga HM, Wechselberger M (2012) Mixed-mode oscillations with multiple time scales. SIAM Rev 54(2):211鈥?88View Article
  Drion G, Franci A, Seutin V, Sepulchre R (2012) A novel phase portrait for neuronal excitability. PLoS One 7(8):e41806View Article PubMed Central PubMed
  Durand DM (2003) Electric field effects in hyperexcitable neural tissue: a review. Radiat Prot Dosimetry 106(4):325鈥?1View Article PubMed
  Ermentrout B (1998) Linearization of F-I curves by adaptation. Neural Comput 10(7):1721鈥?729View Article PubMed
  Ermentrout B (2002) Simulating, analyzing, and animating dynamical systems: a guide to XPPAUT for researchers and students. SIAM, PhiladelphiaView Article
  Goodman D, Brette R (2008) Brian: a simulator for spiking neural networks in python. Front Neuroinform 2:5View Article PubMed Central PubMed
  Hu H, Vervaeke K, Storm JF (2002) Two forms of electrical resonance at theta frequencies, generated by M-current, h-current and persistent Na\(^{+}\) current in rat hippocampal pyramidal cells. J Physiol 545(Pt 3):783鈥?05View Article PubMed Central PubMed
  Izhikevich EM (2005) Dynamical systems in neuroscience: the geometry of excitability and bursting. The MIT Press, London
  Kimiskidis VK, Kugiumtzis D, Papagiannopoulos S, Vlaikidis N (2013) Transcranial magnetic stimulation (TMS) modulates epileptiform discharges in patients with frontal lobe epilepsy: a preliminary EEG-TMS study. Int J Neural Syste 23(1):1250035View Article
  Liu YH, Wang XJ (2001) Spike-frequency adaptation of a generalized leaky integrate-and-fire model neuron. J Comput Neurosci 10(1):25鈥?5View Article PubMed
  Madison DV, Nicoll RA (1984) Control of the repetitive discharge of rat CA1 pyramidal neurones in vitro. J Physiol 354:319鈥?1View Article PubMed Central PubMed
  Marino F, Marin F, Balle S, Piro O (2007) Chaotically spiking canards in an excitable system with 2D inertial fast manifolds. Phys Rev Lett 98(7):074104View Article PubMed
  Mclntyre CC, Grill WM (1999) Excitation of central nervous system neurons by nonuniform electric fields. Biophys J 76(2):878鈥?8View Article
  Milik A, Szmolyan P, Loeffelmann H, Groeller E (1998) Geometry of mixed-mode oscillations in the 3-D autocatalator. Int J Bifurc Chaos 8(3):505鈥?19View Article
  Moehlis J (2006) Canards for a reduction of the Hodgkin鈥揌uxley equation. J Math Biol 52:141鈥?53View Article PubMed
  Nagarajan SS, Durand DM, Warman EN (1993) Effects of induced electric fields on finite neuronal structures: a simulation study. IEEE Trans Biomed Eng 40(11):1175鈥?8View Article PubMed
  Park EH, Barreto E, Gluckman BJ, Schiff SJ, So P (2005) A model of the effects of applied electric fields on neuronal synchronization. J Comput Neurosci 19(1):53鈥?0View Article PubMed Central PubMed
  Park EH, So P, Barreto E, Gluckman BJ, Schiff SJ (2003) Electric field modulation of synchronization in neuronal networks. Neurocomputing 52鈥?4:169鈥?75View Article
  Pashut T, Wolfus S, Friedman A, Lavidor M, Bar-Gad I, Yeshurun Y, Korngreen A (2011) Mechanisms of magnetic stimulation of central nervous system neurons. PLoS Comput Biol 7(3):e1002022View Article PubMed Central PubMed
  Peron S, Gabbiani F (2009) Spike frequency adaptation mediates looming stimulus selectivity in a collision-detecting neuron. Nat Neurosci 12(3):318鈥?26View Article PubMed Central PubMed
  Peterchev AV, Wagner TA, Miranda PC, Nitsche MA, Paulus W, Lisanby SH, Pascual-Leone A, Bikson M (2012) Fundamentals of transcranial electric and magnetic stimulation dose: definition, selection, and reporting practices. Brain Stimul 5(4):435鈥?53View Article PubMed Central PubMed
  Pineda JC, Galarraga E, Foehring RC (1999) Different Ca\(^{2+}\) source for slow AHP in completely adapting and repetitive firing pyramidal neurons. Neuroreport 10(9):1951鈥?956View Article PubMed
  Prescott SA, De Koninck Y, Sejnowski TJ (2008a) Biophysical basis for three distinct dynamical mechanisms of action potential initiation. PLoS Comput Biol 4(10):e1000198View Article PubMed Central PubMed
  Prescott SA, Ratt茅 S, De Koninck Y, Sejnowski TJ (2006) Nonlinear interaction between shunting and adaptation controls a switch between integration and coincidence detection in pyramidal neurons. J Neurosci 26(36):9084鈥?097View Article PubMed Central PubMed
  Prescott SA, Ratt茅 S, De Koninck Y, Sejnowski TJ (2008b) Pyramidal neurons switch from integrators in vitro to resonators under in vivo-like conditions. J Neurophysiol 100(6):3030鈥?042View Article PubMed Central PubMed
  Prescott SA, Sejnowski TJ (2008) Spike-rate coding and spike-time coding are affected oppositely by different adaptation mechanisms. J Neurosci 28(50):13649鈥?3661View Article PubMed Central PubMed
  Radman T, Ramos RL, Brumberg JC, Bikson M (2009) Role of cortical cell type and morphology in sub- and suprathreshold uniform electric field stimulation. Brain Stimul 2(4):215鈥?28View Article PubMed Central PubMed
  Rubin J, Wechselberger M (2007) Giant squid-hidden canard: the 3D geometry of the Hodgkin鈥揌uxley model. Biol Cybern 97(1):5鈥?2View Article PubMed
  Sharpee TO, Sugihara H, Kurgansky AV, Rebrik SP, Stryker MP, Miller KD (2006) Adaptive filtering enhances information transmission in visual cortex. Nature 439:936鈥?42View Article PubMed Central PubMed
  Svirskis G, Baginskas A, Hounsgaard J, Gutman A (1997) Electrotonic measurements by electric field-induced polarization in neurons: theory and experimental estimation. Biophys J 73(6):3004鈥?5View Article PubMed Central PubMed
  Tranchina D, Nicholson C (1986) A model for the polarization of neurons by extrinsically applied electric fields. Biophys J 50(6):1139鈥?6View Article PubMed Central PubMed
  Wagner T, Valero-Cabre A, Pascual-Leone A (2007) Noninvasive human brain stimulation. Annu Rev Biomed Eng 9:527鈥?65View Article PubMed
  Walsh V, Cowey A (2000) Transcranial magnetic stimulation and cognitive neuroscience. Nat Rev Neurosci 1(1):73鈥?9View Article PubMed
  Wang XJ (1998) Calcium coding and adaptive temporal computation in cortical pyramidal neurons. J Neurophysiol 79(3): 1549鈥?566
  Wark B, Lundstrom BN, Fairhall A (2007) Sensory adaptation. Curr Opin Neurobiol 17(4):423鈥?29View Article PubMed Central PubMed
  Xie Y, Chen L, Kang YM, Aihara K (2008) Controlling the onset of Hopf bifurcation in the Hodgkin鈥揌uxley model. Phys Rev E 77(6 Pt 1):061921View Article
  Yi GS, Wang J, Deng B, Wei XL (2015) Spike initiating dynamics of the neuron with different adaptation mechanisms to extracellular electric fields. Commun Nonlinear Sci Numer Simul 22(1鈥?):574鈥?86
  Yi GS, Wang J, Wei XL, Tsang KM, Chan WL, Deng B (2014a) Neuronal spike initiation modulated by extracellular electric fields. PLoS ONE 9(5):e97481
  Yi GS, Wang J, Wei XL, Tsang KM, Chan WL, Deng B, Han CX (2014b) Exploring how extracellular electric field modulates neuron activity through dynamical analysis of a two-compartment neuron model. J Comput Neurosci 36(3):383鈥?99View Article PubMed
  
• 作者单位：Guosheng Yi (1)
  Jiang Wang (1)
  Kai-Ming Tsang (2)
  Xile Wei (1)
  Bin Deng (1)
  Chunxiao Han (3)
  
  1. School of Electrical Engineering and Automation, Tianjin University, Tianjin, 300072, China
  2. Department of Electrical Engineering, The Hong Kong Polytechnic University, Hong Kong, China
  3. School of Automation and Electrical Engineering, Tianjin University of Technology and Education, Tianjin, 300222, China
  
• 刊物类别：Biomedical and Life Sciences
• 刊物主题：Biomedicine
  Neurosciences
  Computer Application in Life Sciences
  Neurobiology
  Bioinformatics
  
• 出版者：Springer Berlin / Heidelberg
• ISSN：1432-0770

文摘

Spike-frequency adaptation has been shown to play an important role in neural coding. Based on a reduced two-compartment model, here we investigate how two common adaptation currents, i.e., voltage-sensitive potassium current (\(I_{\mathrm{M}}\)) and calcium-sensitive potassium current (\(I_{\mathrm{AHP}}\)), modulate neuronal responses to extracellular electric fields. It is shown that two adaptation mechanisms lead to distinct effects on the dynamical behavior of the neuron to electric fields. These effects depend on a neuronal morphological parameter that characterizes the ratio of soma area to total membrane area and internal coupling conductance. In the case of \(I_{\mathrm{AHP}}\) current, changing the morphological parameter switches spike initiation dynamics between saddle-node on invariant cycle bifurcation and supercritical Hopf bifurcation, whereas it only switches between subcritical and supercritical Hopf bifurcations for \(I_{\mathrm{M}}\) current. Unlike the morphological parameter, internal coupling conductance is unable to alter the bifurcation scenario for both adaptation currents. We also find that the electric field threshold for triggering neuronal steady-state firing is determined by two parameters, especially by the morphological parameter. Furthermore, the neuron with \(I_{\mathrm{AHP}}\) current generates mixed-mode oscillations through the canard phenomenon for some small values of the morphological parameter. All these results suggest that morphological properties play a critical role in field-induced effects on neuronal dynamics, which could qualitatively alter the outcome of adaptation by modulating internal current between soma and dendrite. The findings are readily testable in experiments, which could help to reveal the mechanisms underlying how the neuron responds to electric field stimulus.