Computational analysis of action potential initiation in mitral cell soma and dendrites based on dual patch recordings

Journal of Neurophysiology

Volumn 82, Issue 6, 1999, Pages 3006-3020

  Shen, Gongyu Y ^a   Chen, Wei R ^a   Midtgaard, Jens ^c   Shepherd, Gordon M ^a   Hines, Michael L ^a,b,d  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Yale University   (United States)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d YALE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

POTASSIUM; POTASSIUM CHANNEL; SODIUM; SODIUM CHANNEL;

ACTION POTENTIAL; ALGORITHM; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; DENSITY; HODGKIN HUXLEY EQUATION; KINETICS; MATHEMATICAL COMPUTING; MITRAL CELL; MODEL; NERVE FIBER; NERVE POTENTIAL; NONHUMAN; OLFACTORY BULB; PERIKARYON; POTASSIUM CURRENT; PRIORITY JOURNAL; RAT; SODIUM CURRENT;

EID: 0033376680     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1999.82.6.3006     Document Type: Article

References (50)

1. ANDERSEN, P. Interhippocampal impulses. II. Apical dendritic activation of CA1 neurons. Acta Physiol. Scand. 48: 178-208, 1960.
2. BENARDO, L. S., MASUKAWA, L. M., AND PRINCE, D. A. Electrophysiology of isolated hippocampal pyramidal dendrites. J. Neurosci. 2: 1614-1622, 1982.
3. BENARDO, L. S. AND PRINCE, D. A. Ionic mechanisms of cholinergic excitation in mammalian hippocampal pyramidal cells. Brain Res. 249: 333-344, 1982.
4. BERTHOLD, C. H. Ultrastructure of postnatally developing feline peripheral nodes of Ranvier. Acta Soc. Med. Ups. 73: 145-168, 1968a.
5. BERTHOLD, C. H. Ultrastructure of the node-paranode region of mature feline ventral lumbar spinal-root fibres. Acta Soc. Med. Ups. 73, Suppl.: 37-70, 1968b.
6. BHALLA, U. S. AND BOWER, J. M. Exploring parameter space in detailed single neuron models: simulations of the mitral and granule cells of the olfactory bulb. J. Neurophysiol. 69: 1948-1965, 1993.
7. BISCHOFBERGER, J. AND JONAS, P. Action potential propagation into the pre-synaptic dendrites of rat mitral cells. J. Physiol. (Lond.) 504: 359-365, 1997.
8. BLACK, J. A., KOCSIS, J. D., AND WAXMAN, S. G. Ion channel organization of the myelinated fiber. Trends Neurosci. 13: 48-54, 1990.
9. BRENT, R. A new algorithm for minimizing a function of several variables without calculating derivatives. In: Algorithms for Minimization without Derivatives. Englewood Cliffs, NJ: Prentice Hall, 1976, p. 200-248.
10. CHEN, W. R., MIDTGAARD, J., AND SHEPHERD, G. M. Forward and backward propagation of dendritic impulses and their synaptic control in mitral cells. Science 278: 463-467, 1997.
11. COLBERT, C. M. AND JOHNSTON, D. Axonal action-potential initiation and Na+ channel densities in the soma and axon initial segment of subicular pyramidal neurons. J. Neurosci. 16: 6676-6686, 1996.
12. CONRADI, S. Observations on the ultrastructure of the axon hillock and initial axon segment of lumbosacral motoneurons in the cat. Acta Physiol. Scand. Suppl. 332: 65-84, 1969.
13. COOLEY, J. W. AND DODGE, F. A., JR. Digital computer solutions for excitation and propagation of the nerve impulse. Biophys. J. 6: 583-599, 1966.
14. CULLHEIM, S. AND KELLERTH, J. O. A morphological study of the axons and recurrent axon collaterals of cat sciatic alpha-motoneurons after intracellular staining with horseradish peroxidase. J. Comp. Neurol. 178: 537-557, 1978.
15. ECCLES, J. The Physiology of Nerve Cells. Baltimore: Johns Hopkins Press, 1957.
16. EDWARDS, C. AND OTTOSON, D. The site of impulse initiation in a nerve cell of a crustacean stretch receptor. J. Physiol. (Lond.) 143: 138-148, 1958.
17. FARINAS, I. AND DEFELIPE, J. Patterns of synaptic input on corticocortical and corticothalamic cells in the cat visual cortex. II. The axon initial segment. J. Comp. Neurol. 304: 70-77, 1991.
18. FITZGIBBON, T., FUNKE, K., AND EYSEL, U. T. Anatomical correlations between soma size, axon diameter, and intraretinal length for the alpha ganglion cells of the cat retina. Vis. Neurosci. 6: 159-174, 1991.
19. FUORTES, M., FRANK, K., AND BECKER, M. Steps in the production of motoneuron spikes. J. Gen. Physiol. 40: 735-750, 1957.
20. GOLDING, N. L. AND SPRUSTON, N. Dendritic sodium spikes are variable triggers of axonal action potentials in hippocampal CA1 pyramidal neurons. Neuron 21: 1189-1200, 1998.
21. HERRERAS, O., MENENDEZ, N., HERRANZ, A. S., SOLIS, J. M., AND MARTIN DEL RIO, R. Synaptic transmission at the Schaffer-CA1 synapse is blocked by 6,7-dinitro-quinoxaline-2,3-dione. An in vivo brain dialysis study in the rat. Neurosci. Lett. 99: 119-124, 1989.
22. HILDEBRAND, C. Ultrastructural and light-microscopic studies of the nodal region in large myelinated fibres of the adult feline spinal cord white matter. Acta Physiol. Scand Suppl. 364: 43-79, 1971.
23. HILDEBRAND, C. AND WAXMAN, S. G. Postnatal differentiation of rat optic nerve fibers: electron microscopic observations on the development of nodes of Ranvier and axoglial relations. J. Comp. Neurol. 224: 25-37, 1984.
24. HINES, M. L. AND CARNEVALE, N. T. The NEURON simulation environment. Neural Comput. 9: 1179-1209, 1997.
25. HOFFMAN, D. A., MAGEE, J. C., COLBERT, C. M., AND JOHNSTON, D. K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387: 869-875, 1997.
26. HODGKIN, A. L. AND HUXLEY, A. F. A quantitive description of membrane current and its application to conduction and excitation in nerve. J. Physiol. (Lond.) 117: 500-544, 1952
27. KATO, T. AND HIRANO, A. A Golgi study of the proximal portion of the human Purkinje cell axon. Acta Neuropathol. (Berl.). 68: 191-195, 1985.
28. LUSCHER, H. R. AND LARKUM, M. E. Modeling action potential initiation and back-propagation in dendrites of cultured rat motoneurons. J. Neurophysiol. 80: 715-729, 1998.
29. MAINEN, Z. F., JOERGES, J., HUGUENARD, J. R., AND SEINOWSKI, T. J. A model of spike initiation in neocortical pyramidal neurons. Neuron 15: 1427-1439, 1995.
30. MORI, K. Membrane and synaptic properties of identified neurons in the olfactory bulb. Prog. Neurobiol. 29: 275-320, 1987.
31. PANNESE, E. Neurocytology: Fine Structure of Neurons, Nerve Processes, and Neuroglial Cells. New York: Thieme Medical Publishers, 1994.
32. PETERS, A., PROSKAUER, C. C., AND KAISERMAN-ABRAMOF, I. R. The small pyramidal neuron of the rat cerebral cortex. The axon hillock and initial segment. J. Cell Biol. 39: 604-619, 1968.
33. PRESS, W. H., TEUKOLSKY, S. A., VETTERLING, W. T., AND FLANNERY, B. P. Minimization or maximization of functions. In: Numerical Recipes in C: The Art of Scientific Computing, Cambridge: Cambridge, 1993, p. 394-455.
34. RALL, W. AND SHEPHERD, G. M. Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in olfactory bulb. J. Neurophysiol. 31: 884-915, 1968.
35. RAPP, M., YAROM, Y., AND SEGEV, I. Modeling back propagating action potential in weakly excitable dendrites of neocortical pyramidal cells. Proc. Natl. Acad. Sci. USA 93: 11985-11990, 1996.
36. RYDMARK, M. AND BERTHOLD, C. H. Electron microscopic serial section analysis of nodes of Ranvier in lumbar spinal roots of the cat: a morphometric study of nodal compartments in fibres of different sizes. J. Neurocytol. 12: 537-565, 1983.
37. SHEN, G. Y., SHEPHERD, G. M., AND HINES, M. L. Tightly constrained model of the olfactory mitral cell based on dual patch electrode data. Soc. Neurosci. Abstr. 24: 1814, 1998.
38. SHEPHERD, G. M. AND BRAYTON, R. K. Computer simulation of a dendrodendritic synaptic circuit for self- and lateral-inhibition in the olfactory bulb. Brain Res. 175: 377-382, 1979.
39. SHEPHERD, G. M. AND GREER, C. A. Olfactory bulb. In: Synaptic Organization of the Brain, edited by G. M. Shepherd. New York: Oxford, 1998, p. 159-178.
40. SHEPHERD, G. M., MIRSKY, J. S., HEALY, M. D., SINGER, M. S., SKOUFOS, E., HINES, M. S., NADKARNI, P. M., AND MILLER, P. L. The Human Brain Project: neuroinformatics tools for integrating, searching and modeling multidisciplinary neuroscience data. Trends Neurosci. 21: 460-468, 1998.
41. SPENCER, W. A. AND KANDEL, E. R. Electrophysiology of hippocampal neurons. IV. Fast prepotentials. J. Neurophysiol. 24: 272-285, 1961.
42. STUART, G., SCHILLER, J., AND SAKMANN, B. Action potential initiation and propagation in rat neocortical pyramidal neurons. J. Physiol. (Lond.) 505: 617-632, 1997a.
43. STUART, G. AND SPRUSTON, N. Determinants of voltage attenuation in neocortical pyramidal neuron dendrites. J. Neurosci. 18: 3501-3510, 1998.
44. STUART, G., SPRUSTON, N., SAKMANN, B., AND HAUSSER, M. Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci. 20: 125-131, 1997b.
45. STUART, G. J. AND SAKMANN, B. Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature 367: 69-72, 1994.
46. TRAUB, R. D. AND LLINAS, R. Hippocampal pyramidal cells: significance of dendritic ionic conductances for neuronal function and epileptogenesis. J. Neurophysiol. 42: 476-496, 1979.
47. TUCZINSKI, H. J. AND FRIEDE, R. L. Internodal length in ventral roots of bovine spinal nerves varies independently of fibre calibre. J. Anat. 138: 423-433, 1984.
48. TURNER, R. W., MEYERS, D. E., AND BARKER, J. L. Localization of tetrodotoxin-sensitive field potentials of CA1 pyramidal cells in the rat hippocampus. J. Neurophysiol. 62: 1375-1387, 1989.
49. TURNER, R. W., MEYERS, D. E., RICHARDSON, T. L., AND BARKER, J. L. The site for initiation of action potential discharge over the somatodendritic axis of rat hippocampal CA1 pyramidal neurons. J. Neurosci. 11: 2270-2280, 1991.
50. WESTRUM, L. E. Observations on initial segments of axons in the prepyriform cortex of the rat. J. Comp. Neurol. 139: 337-356, 1970.