An ephaptic transmission model of CA3 pyramidal cells: an investigation into electric field effects

详细信息    查看全文

• 作者：Xile Wei (1)
  Yinhong Chen (1)
  Meili Lu (2)
  Bin Deng (1)
  Haitao Yu (1)
  Jiang Wang (1)
  Yanqiu Che (3)
  Chunxiao Han (3)
  
• 关键词：Field effect ; Ephaptic transmission ; Subthreshold ; Extracellular electric field ; Firing pattern
• 刊名：Cognitive Neurodynamics
• 出版年：2014
• 出版时间：June 2014
• 年：2014
• 卷：8
• 期：3
• 页码：177-197
• 全文大小：
• 参考文献：1. Anastassiou CA, Montgomery SM, Barahona M et al (2010) The effect of spatially inhomogeneous extracellular electric fields on neurons. J Neurosci 30(5):1925-936 CrossRef
  2. Anastassiou CA, Perin R, Markram H et al (2011) Ephaptic coupling of cortical neurons. Nat Neurosci 14(2):217-23 CrossRef
  3. Bawin SM, Sheppard AR, Mahoney MD et al (1984) Influences of sinusoidal electric fields on excitability in the rat hippocampal slice. Brain Res 323(2):227-37 CrossRef
  4. Bernhardt J (1979) The direct influence of electromagnetic fields on nerve- and muscle cells of man within the frequency range of 1?Hz to 30?MHz. Radiat Environ Biophys 16(4):309-23 CrossRef
  5. Bikson M, Inoue M, Akiyama H et al (2004) Effects of uniform extracellular dc electric fields on excitability in rat hippocampal slices in vitro. J Physiol 557(Pt 1):175-90 CrossRef
  6. Casarotto S, Romero LL, Bellina V et al (2010) EEg responses to TMS are sensitive to changes in the perturbation parameters and repeatable over time. PLoS One 5(4):e10281 CrossRef
  7. Chan CY, Nicholson C (1986) Modulation by applied electric fields of purkinje and stellate cell activity in the isolated turtle cerebellum. J Physiol 371:89-14
  8. 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 402:751-71
  9. Daskalakis ZJ, Levinson AJ, Fitzgerald PB (2008) Repetitive transcranial magnetic stimulation for major depressive disorder: a review. Can J Psychiatry 53(9):555-66
  10. de Ruyter VSR, Lewen GD, Strong SP et al (1997) Reproducibility and variability in neural spike trains. Science 275(5307):1805-808 CrossRef
  11. Deans JK, Powell AD, Jefferys JG (2007) Sensitivity of coherent oscillations in rat hippocampus to ac electric fields. J Physiol 583(Pt 2):555-65 CrossRef
  12. Du Y, Wang R, Han F, Lu Q, Qu J (2012) Firing pattern and synchronization property analysis in a network model of the olfactory bulb. Cogn Neurodyn 6(2):203-09 CrossRef
  13. Dudek FE, Yasumura T, Rash JE (1998) ‘Non-synaptic-mechanisms in seizures and epileptogenesis. Cell Biol Int 22(11-2):793-05 CrossRef
  14. Duong DH, Chang T (1998) The influence of electric fields on the epileptiform bursts induced by high potassium in ca3 region of rat hippocampal slice. Neurol Res 20(6):542-48
  15. Durand DM (2003) Electric field effects in hyperexcitable neural tissue: a review. Radiat Prot Dosimetry 106(4):325-31 CrossRef
  16. Durand DM, Bikson M (2001) Suppression and control of epileptiform activity by electrical stimulation: a review. Proc IEEE 89(7):1065-082 CrossRef
  17. Eichwald C, Kaiser F (1995) Model for external influences on cellular signal transduction pathways including cytosolic calcium oscillations. Bioelectromagnetics 16(2):75-5 CrossRef
  18. Ermentrout B (2002) Simulating, analyzing, and animating dynamical systems: a guide to XPPAUT for researchers and students. Society for Industrial Mathematics Press, Philadelphia, PA CrossRef
  19. Francis JT, Gluckman BJ, Schiff SJ (2003) Sensitivity of neurons to weak electric fields. J Neurosci 23(19):7255-261
  20. Fujisawa S, Matsuki N, Ikegaya Y (2004) Chronometric readout from a memory trace: gamma-frequency field stimulation recruits timed recurrent activity in the rat ca3 network. J Physiol 561(Pt 1):123-31 CrossRef
  21. Furukawa T, Furshpan EJ (1963) Two inhibitory mechanisms in the Mauthner neurons of goldfish. J Neurophysiol 26:140-76
  22. Gerstner W, Kistler WM (2002) Spiking neuron models: single neurons, populations, plasticity. Cambridge University Press, Cambridge CrossRef
  23. Ghai RS, Bikson M, Durand DM (2000) Effects of applied electric fields on low-calcium epileptiform activity in the ca1 region of rat hippocampal slices. J Neurophysiol 84(1):274-80
  24. Gildenberg PL (2005) Evolution of neuromodulation. Stereotact Funct Neurosurg 83(2-):71-9 CrossRef
  25. Gluckman BJ, Neel EJ, Netoff TI et al (1996) Electric field suppression of epileptiform activity in hippocampal slices. J Neurophysiol 76(6):4202-205
  26. Holt GR, Koch C (1999) Electrical interactions via the extracellular potential near cell bodies. J Comput Neurosci 6(2):169-84 CrossRef
  27. Jefferys JG (1981) Influence of electric fields on the excitability of granule cells in guinea-pig hippocampal slices. J Physiol 319:143-52
  28. Jefferys JG (1995) Nonsynaptic modulation of neuronal activity in the brain: electric currents and extracellular ions. Physiol Rev 75(4):689-23
  29. Jefferys JG, Deans J, Bikson M et al (2003) Effects of weak electric fields on the activity of neurons and neuronal networks. Radiat Prot Dosimetry 106(4):321-23 CrossRef
  30. Klimesch W, Sauseng P, Gerloff C (2003) Enhancing cognitive performance with repetitive transcranial magnetic stimulation at human individual alpha frequency. Eur J Neurosci 17(5):1129-133 CrossRef
  31. Korn H, Faber DS (1975) An electrically mediated inhibition in goldfish medulla. J Neurophysiol 38(2):452-71
  32. Korn H, Faber DS (2005) The Mauthner cell half a century later: a neurobiological model for decision-making? Neuron 47(1):13-8 CrossRef
  33. Kringelbach ML, Jenkinson N, Owen SL et al (2007) Translational principles of deep brain stimulation. Nat Rev Neurosci 8(8):623-35 CrossRef
  34. Krishnamurthi N, Mulligan S, Mahant P, Samanta J, Abbas JJ (2012) Deep brain stimulation amplitude alters posture shift velocity in Parkinson’s disease. Cogn Neurodyn 6(4):325-32 CrossRef
  35. Macvicar BA, Dudek FE (1981) Electrotonic coupling between pyramidal cells: a direct demonstration in rat hippocampal slices. Science 213(4509):782-85 CrossRef
  36. Marshall L, Helgadottir H, Molle M et al (2006) Boosting slow oscillations during sleep potentiates memory. Nature 444(7119):610-13 CrossRef
  37. Martin PI, Naeser MA, Ho M et al (2009) Research with transcranial magnetic stimulation in the treatment of aphasia. Curr Neurol Neurosci Rep 9(6):451-58 CrossRef
  38. Mcbain CJ, Traynelis SF, Dingledine R (1990) Regional variation of extracellular space in the hippocampus. Science 249(4969):674-77 CrossRef
  39. Meng P, Wang Q, Lu Q (2013) Bursting synchronization dynamics of pancreatic β-cells with electrical and chemical coupling. Cogn Neurodyn 7(3):197-12 CrossRef
  40. Netoff TI, Schiff SJ (2002) Decreased neuronal synchronization during experimental seizures. J Neurosci 22(16):7297-307
  41. Njap F, Clausssen JC, Moser A, Hofmann UG (2012) Modeling effect of GABAergic current in a basal ganglia computational model. Cogn Neurodyn 6(4):333-41 CrossRef
  42. Park EH, Barreto E, Gluckman BJ et al (2005) A model of the effects of applied electric fields on neuronal synchronization. J Comput Neurosci 19(1):53-0 CrossRef
  43. Partsvania B, Sulaberidze T, Modebadze Z et al (2008) Extremely low-frequency magnetic fields effects on the snail single neurons. Electromagn Biol Med 27(4):409-17 CrossRef
  44. Pinsky PF, Rinzel J (1994) Intrinsic and network rhythmogenesis in a reduced traub model for ca3 neurons. J Comput Neurosci 1(1-):39-0 CrossRef
  45. Purpura DP, Mcmurtry JG (1965) Intracellular activities and evoked potential changes during polarization of motor cortex. J Neurophysiol 28:166-85
  46. Radman T, Su Y, An JH et al (2007) Spike timing amplifies the effect of electric fields on neurons: implications for endogenous field effects. J Neurosci 27(11):3030-036 CrossRef
  47. Reato D, Rahman A, Bikson M et al (2010) Low-intensity electrical stimulation affects network dynamics by modulating population rate and spike timing. J Neurosci 30(45):15067-5079 CrossRef
  48. Rubin JE, Terman D (2004) High frequency stimulation of the subthalamic nucleus eliminates pathological thalamic rhythmicity in a computational model. J Comput Neurosci 16(3):211-35 CrossRef
  49. Sandrini M, Umilta C, Rusconi E (2011) The use of transcranial magnetic stimulation in cognitive neuroscience: a new synthesis of methodological issues. Neurosci Biobehav Rev 35(3):516-36 CrossRef
  50. Schaefer AT, Angelo K, Spors H et al (2006) Neuronal oscillations enhance stimulus discrimination by ensuring action potential precision. PLoS Biol 4(6):e163 CrossRef
  51. Schutt M, Claussen JC (2012) Desynchronizing effect of high-frequency stimulation in a generic cortical network model. Cogn Neurodyn 6(4):343-51 CrossRef
  52. Schweitzer JS, Patrylo PR, Dudek FE (1992) Prolonged field bursts in the dentate gyrus: dependence on low calcium, high potassium, and nonsynaptic mechanisms. J Neurophysiol 68(6):2016-025
  53. Shoji FF, Lee HH (2000) On a response characteristics in the Hodgkin–Huxley model of nerve and muscle fiber to a periodic stimulation. Ind Electron Soc (IECON 2000) 3:2035-041
  54. Shuai J, Bikson M, Hahn PJ et al (2003) Ionic mechanisms underlying spontaneous ca1 neuronal firing in ca2+-free solution. Biophys J 84(3):2099-111 CrossRef
  55. Tranchina D, Nicholson C (1986) A model for the polarization of neurons by extrinsically applied electric fields. Biophys J 50(6):1139-156 CrossRef
  56. Traub RD, Dudek FE, Taylor CP et al (1985) Simulation of hippocampal afterdischarges synchronized by electrical interactions. Neuroscience 14(4):1033-038 CrossRef
  57. Traynelis SF, Dingledine R (1988) Potassium-induced spontaneous electrographic seizures in the rat hippocampal slice. J Neurophysiol 59(1):259-76
  58. Ullah G, Schiff SJ (2009) Tracking and control of neuronal Hodgkin–Huxley dynamics. Phys Rev E Stat Nonlin Soft Matter Phys 79(4 Pt 1):40901 CrossRef
  59. Wang R, Zhang Z (2007) Energy coding in biological neural networks. Cogn Neurodyn 1(3):203-12 CrossRef
  60. Weiss SA, Faber DS (2010) Field effects in the CNS play functional roles. Front Neural Circuits 4:15
  61. Weiss SA, Preuss T, Faber DS (2008) A role of electrical inhibition in sensorimotor integration. Proc Natl Acad Sci USA 105(46):18047-8052 CrossRef
  62. Xie Y, Xu JX, Hu SJ, Kang YM, Yang HJ, Duan YB (2004) Dynamical mechanisms for sensitive response of aperiodic firing cells to external stimulation. Chaos, Solitons Fractals 22(1):151-60 CrossRef
  63. Yaari Y, Konnerth A, Heinemann U (1983) Spontaneous epileptiform activity of ca1 hippocampal neurons in low extracellular calcium solutions. Exp Brain Res 51(1):153-56
  64. Yang L, Liu W, Ming Y, Wang C et al (2012) Vibrational resonance induced by transition of phase-locking modes in excitable systems. Phys Rev E 86:016209 CrossRef
  65. Yi G, Wang J, Bian H, Han C, Deng B, Wei X, Li H (2013) Multi-scale order recurrence quantification analysis of EEG signals evoked by manual acupuncture in healthy subjects. Cogn Neurodyn 7(1):79-8 CrossRef
  66. Yu K, Wang J, Deng B, Wei X (2013) Synchronization of neuron population subject to steady DC electric field induced by magnetic stimulation. Cogn Neurodyn 7(3):237-52 CrossRef
  
• 作者单位：Xile Wei (1)
  Yinhong Chen (1)
  Meili Lu (2)
  Bin Deng (1)
  Haitao Yu (1)
  Jiang Wang (1)
  Yanqiu Che (3)
  Chunxiao Han (3)
  
  1. School of Electrical Engineering and Automation, Tianjin University, Tianjin, 300072, China
  2. School of Informational Technology and Engineering, Tianjin University of Technology and Education, Tianjin, 300222, China
  3. School of Automation and Electrical Engineering, Tianjin University of Technology and Education, Tianjin, 300222, China
  
• ISSN：1871-4099

文摘

Extracellular electric fields existing throughout the living brain affect the neural coding and information processing via ephaptic transmission, independent of synapses. A two-compartment whole field effect model (WFEM) of pyramidal neurons embedded within a resistive array which simulates the extracellular medium i.e. ephapse is developed to study the effects of electric field on neuronal behaviors. We derive the two linearized filed effect models (LFEM-1 and LFEM-2) from WFEM at the stable resting state. Through matching these simplified models to the subthreshold membrane response in experiments of the resting pyramidal cells exposed to applied electric fields, we not only verify our proposed model’s validity but also found the key parameters which dominate subthreshold frequency response characteristic. Moreover, we find and give its underlying biophysical mechanism that the unsymmetrical properties of active ion channels results in the very different low-frequency response of somatic and dendritic compartments. Following, WFEM is used to investigate both direct-current (DC) and alternating-current field effect on the neural firing patterns by bifurcation analyses. We present that DC electric field could modulate neuronal excitability, with the positive field improving the excitability, the modest negative field suppressing the excitability, but interestingly, the larger negative field re-exciting the neuron back into spiking behavior. The neuron exposed to the sinusoidal electric field exhibits abundant firing patterns sensitive to the input frequency and intensity. In addition, the electrical properties of ephapse can modulate the efficacy of field effect. Our simulated results are qualitatively in line with the relevant experimental results and can explain some experimental phenomena. Furthermore, they are helpful to provide the predictions which can be tested in future experiments.