Journal of Computational Neuroscience

, Volume 6, Issue 2, pp 169–184 | Cite as

Electrical Interactions via the Extracellular Potential Near Cell Bodies

Article

Abstract

Ephaptic interactions between a neuron and axons or dendrites passing by its cell body can be, in principle, more significant than ephaptic interactions among axons in a fiber tract. Extracellular action potentials outside axons are small in amplitude and spatially spread out, while they are larger in amplitude and much more spatially confined near cell bodies. We estimated the extracellular potentials associated with an action potential in a cortical pyramidal cell using standard one-dimensional cable theory and volume conductor theory. Their spatial and temporal pattern reveal much about the location and timing of currents in the cell, especially in combination with a known morphology, and simple experiments could resolve questions about spike initiation. From the extracellular potential we compute the ephaptically induced polarization in a nearby passive cable. The magnitude of this induced voltage can be several mV, does not spread electrotonically, and depends only weakly on the passive properties of the cable. We discuss their possible functional relevance.

extracellular field potential volume conduction branch point failure axon hillock/initial segment 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Arvanitaki A (1942) Effects evoked in an axon by the activity of a contiguous one. J. Neurophysiol 5:89–108.Google Scholar
  2. Barr RC, Plonsey R (1992) Electrophysiological interaction through the interstitial space between adjacent unmyelinated parallel fibers. Biophys. J. 61:1164–1175.Google Scholar
  3. Bernander Ö, Douglas R, Martin K, Koch C. (1991) Synaptic background activity determines spatio-temporal integration in single pyramidal cells. Proc. Natl. Acad. Sci. USA 88:1569–1573.Google Scholar
  4. Bishop GH, O'Leary JL (1942) The polarity of potentials recorded from the superior colliculus. J. Cell. Comp. Physiol. 19:289–300.Google Scholar
  5. Bullock TH (1965) Comparative neurology of transmission. In: TH Bullock, GA Horridge, eds. Structure and Function in the Nervous Systems of Invertebrates. Vol. I. WH Freeman, San Francisco. pp. 181–251.Google Scholar
  6. Bullock TH (1997) Signals and signs in the nervous system: The dynamic anatomy of electrical activity is probably informationrich. Proc. Natl. Acad. Sci. USA 94:1–6.Google Scholar
  7. Buzsáki G, Penttonen M, Nádasdy Z, Bragin A (1996) Pattern and inhibition-dependent invasion of pyramidal cell dendrites by fast spikes in the hippocampus in vitro. Proc. Natl. Acad. Sci. USA 93:9921–9925.Google Scholar
  8. Chan CY, Nicholson C (1986) Modulation by applied electric fields of purkinje and stellate cell activity in the isolated turtle cerebellum. J. Physiol. 371:89–114.Google Scholar
  9. Clark J, Plonsey R (1968) The extracellular potential field of the single active nerve fiber in a volume conductor. Biophys. J. 8:842–864.Google Scholar
  10. Clark JW, Plonsey R (1970) A mathematical study of nerve fiber interaction. Biophys. J. 10:937–957.Google Scholar
  11. Clark JW, Plonsey R (1971) Fiber interaction in a nerve trunk. Biophys. J. 11:281–294.Google Scholar
  12. Colbert CM, Johnston D (1996) Axonal action-potential initiation and Na+ channel densities in the soma and axon initial segment of subicular neurons. J. Neurosci. 16:6676–6686.Google Scholar
  13. Coombs JS, Curtis DR, Eccles JC (1957a) The generation of impulses in motoneurons. J. Physiol. 139:232–249.Google Scholar
  14. Coombs JS, Curtis DR, Eccles JC (1957b) The interpretation of spike potentials of motoneurons. J. Physiol. 139:198–231.Google Scholar
  15. Dalkara T, Krnjević K, Ropert N, Yim CY (1986) Chemical modulation of ephaptic activation of CA3 hippocampal pyramids. Neurosci. 17:361–370.Google Scholar
  16. Debanne D, Guérineau NC, Gähwiler BH, Thompson SM (1997) Action-potential propagaion gated by an axonal I A-like K+ conductance in hippocampus. Nature 389:286–289.Google Scholar
  17. Douglas RJ, Martin KAC, Whitteridge D (1991) An intracellular analysis of the visual responses of neurones in cat visual cortex. J. Physiol. 440:659–696.Google Scholar
  18. Eccles JC (1964) The physiology of synapses. Academic Press, New York.Google Scholar
  19. Faber DS, Korn H (1989) Electrical field effects: Their relevance in central neural networks. Physiol. Rev. 69:821–863.Google Scholar
  20. Fatt P (1957) Electric potentials occuring around a neurone during its antidromic activation. J. Neurophysiol. 20:27–60.Google Scholar
  21. Freygang WH (1958) An analysis of extracellular potentials from single neurons in the lateral geniculate nucleus of the cat. J. Gen. Physiol. 41:543–564.Google Scholar
  22. Freygang WH, Frank K (1959) Extracellular potentials from single spinal motoneurons. J. Gen. Physiol. 42:749–760.Google Scholar
  23. Fuortes MGF, Frank K, Becker MC (1957) Steps in the production of motoneuron spikes. J. Gen. Physiol. 40:735–752.Google Scholar
  24. Hoffman DA, Magee JC, Colbert CM, Johnston D (1997) K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387:869–875.Google Scholar
  25. Holt GR (1998) A critical reexamination of some assumptions and implications of cable theory in neurobiology. Ph.D. Thesis, California Institute of Technology. Available from http://www. klab.caltech.edu/~holt/papers/thesis/.Google Scholar
  26. Hubbard JI, Llinás R, Quastel DMJ (1969) Electrophysiological Analysis of Synaptic Transmission. Williams & Wilkins, Baltimore.Google Scholar
  27. Jefferys JGR (1995) Nonsynaptic modulation of neuronal activity in the brain: Electric current and extracellular ions. Physiol. Rev. 75:689–723.Google Scholar
  28. Katz B, Schmitt OH (1942) A note on interaction between nerve fibers. J. Physiol. 100:369–371.Google Scholar
  29. Kocsis JD, Ruiz JA, Cummins KL (1982) Modulation of axonal excitability mediated by surround electrical activity: An intraaxonal study. Exp. Brain Res. 47:151–153.Google Scholar
  30. Korn H, Axelrad H(1980) Electrical inhibition of Purkinje cells in the cerebellum of the rat. Proc. Natl. Acad. Sci. USA 77:6244–6247.Google Scholar
  31. Korn H, Faber DS (1980) Electrical field effect interactions in the vertebrate brain. Trends Neurosci. 3:6–9.Google Scholar
  32. Lorente de Nó R (1947) Action potential of the motoneurons of the hypoglossus nucleus. J. Cell. Comp. Physiol. 29:207–287.Google Scholar
  33. MacNeal DR(1976) Analysis of a model for excitation of myelinated nerve. IEEE Trans. Biomed. Eng. BME-33:329–337.Google Scholar
  34. Mainen ZF, Joerges J, Huguenard JR, Sejnowski TJ (1995) A model of spike initiation in neocortical pyramidal neurons. Neuron 15:1427–1439.Google Scholar
  35. Mainen ZF, Sejnowski TJ (1996) Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382:363–366.Google Scholar
  36. Malmivuo J, Plonsey R (1995) Bioelectromagnetism: Principles and Applications of Bioelectric and Biomagnetic Fields. Oxford University Press, Oxford.Google Scholar
  37. Manor Y, Koch C, Segev I (1991) The effect of geometrical irregularities on propagation delay in axonal trees. Biophys. J. 60:1424–1437.Google Scholar
  38. Markin VS (1970a) Electrical interaction of parallel non-myelinated nerve fibers. I. Change in excitability of the adjacent fiber. Biofizika 15:120–128.Google Scholar
  39. Markin VS (1970b) Electrical interaction of parallel non-myelinated nerve fibers. II. Collective conduction of impulses. Biofizika 15:681–689.Google Scholar
  40. Markin VS (1973a) Electrical interaction of parallel non-myelinated nerve fibers. III. Interaction in bundles. Biofizika 18:314–321. Translated.Google Scholar
  41. Markin VS (1973b) Electrical interaction of parallel non-myelinated nerve fibers. IV. Role of anatomical inhomogeneities of nerve trunks. Biofizika 18:512–518. Translated.Google Scholar
  42. McCaig CD (1988) Nerve guidance: A role for bio-electric fields? Prog. Neurobiol. 30:449–468.Google Scholar
  43. McCaig CD, Zhao M (1997) Physiological electrical fields modify cell behaviour. Bioessays 19:819–826.Google Scholar
  44. Mitzdorf U (1985) Current source-density method and application in cat cerebral cortex: Investigation of evoked potentials and EEG phenomena. Physiol. Rev. 65:37–100.Google Scholar
  45. Nelson PG (1966) Interaction between spinal motoneurons of the cat. J. Neurophysiol. 29:275–287.Google Scholar
  46. Nelson PG, Frank K (1964) Extracellular potential fields of single spinal motoneurons. J. Neurophysiol. 27:913–927.Google Scholar
  47. Nicholson C (1995) Extracellular space as the pathway for neuronglial cell interaction. In: H Kettenmann, BR Ransom, eds. Neuroglia. Oxford University Press, Oxford, pp. 387–397.Google Scholar
  48. Patel NB, Poo MM (1984) Perturbation of the direction of neurite growth by pulsed and focal electric fields. J. Neurosci. 4:2939–2947.Google Scholar
  49. Peters A, Palay SL, deFWebster H (1991) The Fine Structure of the Nervous System: The Neurons and Supporting Cells. Saunders, Philadelphia.Google Scholar
  50. Plonsey R (1969) Bioelectric phenomena. McGraw-Hill, New York.Google Scholar
  51. Plonsey R, Barr RC (1995) Electric field stimulation of excitable tissue. IEEE Trans. Biomed. Eng. 42:329–336.Google Scholar
  52. Rall W (1962) Electrophysiology of a dendritic neuron model. Biophys. J. 2:145–167.Google Scholar
  53. Rall W(1977) Core conductor theory and cable properties of neurons. In: ER Kandel ed. The Nervous System, Vol. I: Cellular Biology of Neurons, Part 1. American Physiological Society, Bethesda, pp. 39–97.Google Scholar
  54. Ranck JB (1963) Specific impedance of rabbit cerebral cortex. Exp. Neurol. 7:144–152.Google Scholar
  55. Ranck JB (1975) Which elements are excited in electrical stimulation of mammalian central nervous system: A review. Brain Res. 98:417–440.Google Scholar
  56. Rapp M, Yarom Y, Segev I (1996) Modeling back propagating action potential in weakly excitable dendrites of neocortical pyramidal cells. Proc. Natl. Acad. Sci. USA 93:11985–11990.Google Scholar
  57. Roney KJ, Scheibel AB, Shaw GL (1979) Dendritic bundles: Survey of anatomical experiments and physiological theories. Brain Res. Rev. 1:225–271.Google Scholar
  58. Rosenfalck P (1969) Intra-and extra-cellular potential fields of active nerve and muscle fibers. Acta Physiol. Scand. Suppl. 321:1–168.Google Scholar
  59. Rosenthal F (1972) Extracellular fields of single PT-neurons. Brain Res. 36:251–263.Google Scholar
  60. Scott AC, Luzader SD (1979) Coupled solitary waves in neurophysics. Physica Scripta 20:395–401.Google Scholar
  61. Snow RW, Dudek FE (1984) Electrical fields directly contribute to action potential synchronization during convulsant-induced epileptiform bursts. Brain Res. 323:114–118.Google Scholar
  62. Sperti L, Gessi T, Volta F (1967) Extracellular potential field of antidromically activated CA1 neurons. Brain Res. 3:343–361.Google Scholar
  63. Stein RB, Pearson KG(1971) Predicted amplitude and form of action potentials recorded from unmyelinated nerve fibres. J. Theor. Biol. 32:539–558.Google Scholar
  64. Stevens CF (1966) Neurophysiology: A primer. JWiley, New York.Google Scholar
  65. Stuart G, Sakmann B (1994) Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367:69–72.Google Scholar
  66. Swadlow HA, Kocsis JD, Waxman SG (1980) Modulation of impulse conduction along the axonal tree. Ann. Rev. Biophys. Bioeng. 9:143–179.Google Scholar
  67. Syková E (1997) The extracellular space in the CNS: Its regulation, volume and geomtry in normal and pathological neuronal function. The Neuroscientist 3:28–41.Google Scholar
  68. Tabata T (1990) Ephaptic transmission and conduction velocity of an action potential in Chara internodal cells placed in parallel and in contact with one another. Plant Cell Physiol. 31:575–579.Google Scholar
  69. Terzuolo CA, Araki T (1961) An analysis of intra-versus extracellular potential changes associated with activity of single spinal motoneurons. Ann. NY Acad. Sci. 94:547–558.Google Scholar
  70. Tranchina D, Nicholson C (1986) Amodel for the polarization of neurons by extrinsically applied electric fields. Biophys. J. 50:1139–1156.Google Scholar
  71. Traub RD, Dudek FE, Snow RW, Knowles WD (1985a) Computer simulations indicate that electrical field effects contribute to the shape of the epileptiform field potential. Neurosci. 15:947–958.Google Scholar
  72. Traub RD, Dudek FE, Taylor CP, Knowles WD (1985b) Simulation of hippocampal afterdischarges synchronized by electrical interaction. Neurosci. 14:1033–1038.Google Scholar
  73. Trayanova N, Henriquez CS (1991) Examination of the choice of models for computing the extracellular potential of a single fibre in a restricted volume conductor. Med. & Biol. Eng. & Comput. 29:580–584.Google Scholar
  74. Trayanova NA, Henriquez CS, Plonsey R (1990) Limitations of approximate solutions for computing the extracellular potential of single fibers and bundle equivalents. IEEE Trans. Biomed. Eng. 37:22–35.Google Scholar
  75. Turner RW, Richardson TL (1991) Apical dendritic depolarizations and field interactions evoked by stimulation of afferent inputs to rat hippocampal CA1 pyramidal cells. Neurosci. 42:125–135.Google Scholar
  76. Van Harreveld A (1972) The extracellular space in the vertebrate central nervous system. In: GH Bourne, ed. The Structure and Function of Nervous Tissue. Academic Press, New York, pp. 447–511.Google Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  1. 1.Computation and Neural Systems ProgramCalifornia Institute of TechnologyPasadena

Personalised recommendations