Layer I neurons of rat neocortex. I. Action potential and repetitive firing properties

Journal of Neurophysiology

Volumn 76, Issue 2, 1996, Pages 651-667

  Zhou, Fu Ming ^a   Hablitz, John J ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; MEMBRANE STEADY POTENTIAL; NEOCORTEX; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SPIKE;

EID: 0029837281     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1996.76.2.651     Document Type: Article

References (80)

1. ALDRICH, R. W., GETTING, P. A., AND THOMPSON, S. H. Mechanism of frequency-dependent broadening of molluscan neurone soma spikes. J. Physiol. Lond. 291:531-544, 1979.
2. ANDERSON, J. C., MARTIN, K. A. C., AND PICANCO-DINIZ, C. W. The neurons in layer I of cat visual cortex. Proc. R. Soc. Lond. B Biol. Sci. 248: 27-33, 1992.
3. ANDREASEN, M. AND HABLITZ, J. J. Kinetic properties of a transient outward current in rat neocortical neurons. J. Neurophysiol. 68: 1133-1142, 1992.
4. ANDREASEN, M. AND HABLITZ, J. J. Paired-pulse facilitation in the dentate gyrus: a patch-clamp study rat hippocampus in vitro. J. Neurophysiol. 72: 326-336, 1994.
5. AUGUSTINE, G. Regulation of transmitter release at the squid giant synapse by presynaptic delayed rectifier potassium current. J. Physiol. Lond. 431: 343-364, 1990.
6. BARANYI, A., SZENTE, M. B., AND WOODY, C. D. Electrophysiological characterization of different types of neurons recorded in vivo in the motor cortex of the cat. II. membrane parameters, action potentials, current-induced voltage responses and electrotonic structures. J. Neurophysiol. 69: 1865-1879, 1993.
7. BARRETT, E. F., BARRETT, J. N., AND CRILL, W. E. Voltage sensitive outward currents in cat motoneurons. J. Physiol. Lond. 304: 252-276, 1980.
8. BURGARD, E. C. AND HABLITZ, J. J. Developmental changes in NMDA and non-NMDA receptor-mediated synaptic potentials in rat neocortex. J. Neurophysiol. 69: 230-240, 1993.
9. BUHL, E. H, HAN, Z.-S., LORINCZI, Z., STEZHKA, V. V., KARNUP, S. V., AND SOMOGYI, P. Physiological properties of anatomically identified axo-axonic cells in the rat hippocampus. J. Neurophysiol. 71: 1289-1307, 1994.
10. CALVIN, W. H. AND SYPERT, G. W. Fast and slow pyramidal tract neurons: an intracellular analysis of their contrasting repetitive firing properties in the cat. J. Neurophysiol. 39: 420-434, 1976.
11. CONNOR, J. A. AND STEVENS, C. F. Voltage clamp studies of a transient outward membrane current in gastropod neural somata. J. Physiol. Lond. 213: 21-30, 1971a.
12. CONNOR, J. A. AND STEVENS, C. F. Prediction of repetitive firing behavior from voltage clamp data on isolated neurone soma. J. Physiol. Lond. 213: 31-53, 1971b.
13. CONNORS, B. W. AND GUTNICK, M. J. Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci. 13: 99-104, 1990.
14. CONNORS, B. W., GUTNICK, M. J., AND PRINCE, D. A. Electrophysiological properties of neocortical neurons in vitro. J. Neurophysiol. 48: 1032-1320, 1982.
15. CONTI, F., MINELLI, A., AND BRECHA, N. C. Cellular localization and laminar distribution of AMPA glutamate receptor subunits mRNAs and proteins in the rat cerebral cortex. J. Comp. Neurol. 350: 241-259, 1994.
16. DEFELIPE, J. AND FARINAS, I. The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs. Prog. Neurobiol. 39: 563-607, 1992.
17. DEFELIPE, J. AND JONES, E. J. Cajal on the Cerebral Cortex. New York: Oxford University Press, 1988.
18. EDWARDS, F. A., KONNERTH, A., SAKMANN, B., AND TAKAHASHI, T. A thin slice preparation for patch clamp recordings from neurons of the mammalian central nervous system. Pfluegers Arch. 414:600-612, 1989.
19. FRANKENHAEUSER, B. AND HODOKIN, A. L. The action of calcium on the electrical properties of squid axons. J. Physiol. Lond. 137: 218-244, 1957.
20. GABBOTT, P. L. A. AND SOMOGYI, P. Quantitative distribution of GABA-immunoreactive neurons in the visual cortex (area 17) of the cat. Exp. Brain Res. 61: 323-331, 1986.
21. GIUFFRIDA, R. AND RUSTIONI, A. Glutamate and aspartate immunoreactivity in cortico-cortical neurons of the sensorimotor cortex of rats. Exp. Brain Res. 74: 41-46, 1989.
22. GILLETTE, R., GILLETTE, M. U., AND DAVIS, W. J. Action potential broadening and endogenously sustained bursting are substrates of command ability in a feeding neuron of pleurobranchaea. J. Neurophysiol. 43: 669-685, 1980.
23. GOLDSTEIN, S. A. N. AND MILLER, C. Mechanism of charybdotoxin block of a voltage-gated K+ channel. Biophys. J. 565: 1613-1619, 1993.
24. HAMILL, O. P., HUGUENARD, J. R., AND PRINCE, D. A. Patch-clamp studies of voltage-gated currents in identified neurons of the rat cerebral cortex. Cereb. Cortex 1: 48-61, 1991.
25. HILLE, B. Ionic Channels in Excitable Membrane (2nd ed.). Sunderland, MA: Sinauer, 1992.
26. HODGKIN, A. L. AND HUXLEY, A. F. A quantitative description of membrane current and its application to conduction and excitation in nerve. J. Physiol. Lond. 117: 500-544, 1952.
27. HORIKAWA, K. AND ARMSTRONG, W. E. A versatile means of intracellular labeling: injection of biocylin and its detection with avidin conjugates. J. Neurosci. Methods 25: 1-11, 1988.
28. HUBEL, D. H. Cortical neurobiology: a slanted historical perspective. Annu. Rev. Neurosci. 5: 363-370, 1982.
29. + channels in hippocampal neurons of the rat. Biophys. J. 56: 207-212, 1989.
30. IMAMOTO, K., KARASAWA, N., ISOMURA, G., AND NAGATSU, I. Cajal-Retzius neurons identified by GABA immunohistochemistry in layer I of the rat cerebral cortex. Neurosci. Res. 20: 101-105, 1994.
31. ISTVAN, P. AND ZARZECKI, P. Intrinsic discharge patterns and somatosensory inputs for neurons in raccoon somatosensory cortex. J. Neurophysiol. 72: 2827-2839, 1994.
32. JAHNSEN, H. AND LLINAS, R. Electrophysiological properties of guinea-pig thalamic neurons: an in vitro study. J. Physiol. Lond. 349: 205-226, 1984a.
33. JAHNSEN, H. AND LLINAS, R. Ionic basis for the electroresponsiveness and oscillatory properties of guinea-pig thalamic neurons in vitro. J. Physiol. Lond. 349: 227-247, 1984b.
34. KAWAGUCHI, Y. Groupings of nonpyramidal and pyramidal cells with specific physiological and morphological characteristics in rat frontal cortex. J. Neurophysiol. 69: 416-431, 1993.
35. KNOPFEL, T. AND GAHWILER, B. H. Activity-induced elevations of intracellular calcium concentration in pyramidal and nonpyramidal cells of the CA3 region of rat hippocampal slice cultures. J. Neurophysiol. 68: 961-963, 1992.
36. KOESTER, J. AND ALEVIZOS, A. Innervation of the kidney of aplysia by L10, the LUQ cells, and an identified peripheral motoneuron. J. Neurosci. 9: 4078-4088, 1989.
37. LACAILLE, J.-C., MUELLER, A. L., KUNKEL, D. D., AND SCHWARTZKROIN, P. A. Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology. J. Neurosci. 1: 1979-1993, 1987.
38. LACAILLE, J.-C. AND WILLAMS, S. Membrane properties of interneurons in stratum oriens-alveus of the CAl region of rat hippocampus in vitro. Neuroscience 36: 349-359, 1990.
39. LANCASTER, B. AND NICOLL, R. A. Properties of two calcium-activated hyperpolarizations in rat hippocampal neurons. J. Physiol. Lond. 389: 187-203, 1987.
40. LI, J. Y. AND SCHWARK, H. D. Distribution and proportions of GABA-immunopositive neurons in cat primary somatosensory cortex. J. Comp. Neurol. 343: 353-361, 1994.
41. LLINAS, R. R. AND ALONSO, A. Electrophysiology of the mammillary complex in vitro I. tuberomammilary and lateral mammillary neurons. J. Neurophysiol. 68: 1307-1320, 1992.
42. LYNCH, J. W. AND BARRY, P. H. Properties of transient K+ currents and underlying single K+ channels in rat olfactory receptor neurons. J. Gen. Physiol. 97: 1043-1072, 1991.
43. A-Depol in frequency-dependent spike broadening of R20 cells in Aplysia californica. Soc. Neurosci. Abstr. 626. 11, 1994.
44. MADISON, D. V. AND NICOLL, R. A. Control of the repetitive discharge of rat CA1 pyramidal neurons in vitro. J. Physiol. Lond. 354: 319-331, 1984.
45. MARIN-PADILLA, R. M. Ontogenesis of the pyramidal cell of the mammalian neocortex cytoarchitectonics: a unifying theory. J Comp. Neurol. 321: 223-240, 1992.
46. MAYER, M. L. AND SUGIYAMA, K. A modulatory action of divalent cations on transient outward current in cultured rat sensory neurons. J. Physiol. Lond. 396: 417-433, 1988.
47. MCBAIN, C. J. AND DINGELDINE, R. Heterogeneity of synaptic glutamate receptors on CA3 stratum radiatum interneurones of rat hippocampus. J. Physiol. Lond. 462: 373-392, 1993.
48. MCCORMICK, D. A. Functional properties of a slowly inactivating potassium current in guinea pig dorsal lateral geniculate relay neurons. J. Neurophysiol. 66: 1176-1189, 1991.
49. MCCORMICK, D. A., CONNORS, B. W., LIGHTHALL, J. W., AND PRINCE, D. A. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J. Neurophysiol. 54: 782-806, 1985.
50. MCCORMICK, D. A. AND PRINCE, D. A. Postnatal development of electrophysiological properties of rat cerebral cortical pyramidal neurons. J. Physiol. Lond. 393: 743-762, 1987.
51. MIDTGAARD, J. Membrane properties and synaptic responses of Golgi cells and stellate cells in the turtle cerebellum in vitro. J. Physiol. Lond. 457: 329-354, 1992.
52. NUMANN, R. E., WADMAN, W. J., AND WONG, R. K. S. Outward currents of single hippocampal cells obtained from the adult guinea-pig. J. Physiol. Lond. 393: 331-353, 1987.
53. + current. J. Physiol. Lond. 478: 403-422, 1994.
54. PERREAULT, P. AND AVOLI, M. Effects of low concentrations of 4-aminopyridine on CA1 pyramidal cells of the hippocampus. J. Neurophysiol. 61: 953-970, 1989.
55. PETERS, A. AND JONES, E. G. (Editors). Cerebral Cortex, Cellular Components of the Cerebral Cortex, vol. 1, New York: Plenum Press, 1984.
56. PONGS, O. Molecular biology of voltage-dependent potassium channels. Physiol. Rev. 72: S69-S88, 1992.
57. RALL, W. Core conductor theory and cable properties of neurons. In: Handbook of Physiology. The Nervous System. Washington, DC: Am. Physiol. Soc., 1977, sect. 1, vol. I., p. 39-97.
58. SCHWARTZKROIN, P. A. AND MATHERS, L. H. Physiological and morphological identification of a nonpyramidal hippocampal cell type. Brain Res. 157: 1-10, 1978.
59. SCHWINDT, P. C., SPAIN, W. J., FOEHRING, R. C., STAFSTORM, C. E., CHUBB, M. C., AND CRILL, W. E. Multiple potassium conductances and their function in neurons from cat sensorimotor cortex in vitro. J. Neurophysiol. 59: 424-449, 1988.
60. SPAIN, W. J., SCHWINDT, P. C., AND CRILL, W. E. Two transient potassium currents in layer V pyramidal neurons from cat sensorimotor cortex. J. Physiol. Lond. 434: 591-607, 1991.
61. SPENCER, A. N., PRZYSIEZNIAK, J., ACOSTA-URQUIDI, J., AND BASARSKY, T. A. Presynaptic spike broadening reduces junctional potential amplitude. Nature Lond. 340: 636-638, 1989.
62. + currents. J. Neurophysiol. 68: 55-69, 1992.
63. SPRUTSON, N. AND JOHNSTON, D. Perforated patch clamp analysis of the passive membrane properties of three classes of hippocampal neurons. J. Neurophysiol. 67: 508-529, 1992.
64. STALEY, K. J., OTIS, T. S., AND MODY, I. Membrane properties of dentate gyrus granule cells: comparison of sharp microelectrode and whole-cell recordings. J. Neurophysiol. 67: 1346-1358, 1992.
65. STORM, J. Action potential repolarization and a fast after-hyperpolarization in rat hippocampal pyramidal cells. J. Physiol. Lond. 385: 733-759, 1987.
66. STORM, J. An after-hyperpolarization of medium duration in rat hippocampal pyramidal cells. J. Physiol. Lond. 409: 171-190, 1989.
67. SUTOR, B. AND HABLITZ, J. J. EPSPs in rat neocortical neurons in vitro. I. Electrophysiological evidence for two distinct EPSPs. J. Neurophysiol. 61: 607-620, 1989.
68. TAKAHASI, K. Slow and fast groups of pyramidal tract neurons and their respective membrane properties. J. Neurophysiol. 29: 908-924, 1965.
69. TANOUYE, M. A., FERRUS, A., AND FUJITA, S. Abnormal action potentials associated with the Shaker complex locus of Drosophila. Proc. Natl. Acad. Sci. USA 78: 6548-6552, 1981.
70. TAYLOR, C. P. Na+ currents that fail to inactivate. Trends Neurosci. 16: 455-460, 1993.
71. THURBON, D., FIELD, A., AND REDMAN, S. Electrotonic profiles of interneurons in stratum pyramidale of the CA1 region of rat hippocampus. J. Neurophysiol. 71: 1948-1958, 1994.
72. THOMPSON, S. M., MASUKAWA, L. M., AND PRINCE, D. A. Temperature dependence of intrinsic membrane properties and synaptic potentials in hippocampal CAl neurons in vitro. J. Neurosci. 5: 817-824, 1985.
73. VIANA, F., BAYLISS, D. A., AND BERGER, A. L. Multiple potassium conductances and their roles in action potential repolarization and repetitive firing behavior of neonatal rat hypoglossal motoneurons. J. Neurophysiol. 69: 2150-2163, 1993.
74. WILLIAMS, S., SAMULACK, D. D., BEAULIEU, C., AND LACAILLE, J.-C. Membrane properties and synaptic responses of interneurons located near the stratum lacunosum-moleculare/radiatum border of area CA1 in whole-cell recordings from rat hippocampal slices. J. Neurophysiol. 71: 2217-2235, 1994.
75. WARMAN, E. D., DURAND, D. M., AND YUEN, G. L. F. Reconstruction of hippocampal pyramidal cell electrophysiology by computer simulation. J. Neurophysiol. 71: 2033-2045, 1994.
76. 2+ does not affect spike repolarization in cat spinal motoneurons. Brain Res. 462: 174-180, 1988.
77. ZHOU, F.-M. AND HABLITZ, J. J. Bicuculline unmasks a fast EPSP resistant to glutamatergic antagonists in rat neocortex. Soc. Neurosci. Abstr. 19: 469, 1993a.
78. ZHOU, F.-M. AND HABLITZ, J. J. Zinc enhances GABAergic transmission in rat neocortex. J. Neurophysiol. 70: 1264-1269, 1993b.
79. ZHOU, F.-M. AND HABLITZ, J. J. Morphological and electrophysiological properties of layer I neurons in rat neocortex. Soc. Neurosci. Abstr. 20: 1414, 1994.
80. ZHOU, F.-M. AND HABLITZ, J. J. Layer I neurons of rat neocortex. II. Voltage-dependent outward currents. J. Neurophysiol. 76: 668-682, 1996.