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. 1991 Mar;434:609–626. doi: 10.1113/jphysiol.1991.sp018489

Post-inhibitory excitation and inhibition in layer V pyramidal neurones from cat sensorimotor cortex.

W J Spain 1, P C Schwindt 1, W E Crill 1
PMCID: PMC1181437  PMID: 2023133

Abstract

1. The effect of conditioning pre-pulses on repetitive firing evoked by intracellular current injection was studied in layer V pyramidal neurones in a brain slice preparation of cat sensorimotor cortex. Most cells displayed spike frequency adaptation (monotonic decline of firing rate to a tonic value) for several hundred milliseconds when depolarized from resting potential, but the cells differed in their response when pre-pulses to other potentials were employed. In one group of cells, the initial firing rate increased as the pre-pulse potential was made more negative (post-hyperpolarization excitation). Adaptation was abolished by depolarizing prepulses. In a second group, the initial firing rate decreased as the pre-pulse potential was made more negative (post-hyperpolarization inhibition). Hyperpolarizing pre-pulses caused the initial firing to fall below and accelerate to the tonic rate over a period of several seconds. A third group displayed a mixture of these two responses: the first three to seven interspike intervals became progressively shorter and subsequent intervals became progressively longer as the conditioning pre-pulse was made more negative (post-hyperpolarization mixed response). 2. Cells were filled with horseradish peroxidase or biocytin after the effect of pre-pulses was determined. All cells whose firing patterns were altered by pre-pulses were large layer V pyramidal neurones. Cells showing post-hyperpolarization excitation or a mixed response had tap root dendrites, fewer spines on the apical dendrite and larger soma diameters than cells showing post-hyperpolarization inhibition. 3. Other electrophysiological parameters varied systematically with the response to conditioning pre-pulses. Both the mean action potential duration and the input resistance of cells showing post-hyperpolarization excitation were about half the values measured in cells showing post-hyperpolarization inhibition. Values were intermediate in cells showing a post-hyperpolarization mixed response. The after-hyperpolarization following a single evoked action potential was 20% briefer in cells showing post-hyperpolarization excitation compared to those showing inhibition. 4. Membrane current measured during voltage clamp suggested that two ionic mechanisms accounted for the three response patterns. Post-hyperpolarization excitation was caused by deactivation of the inward rectifier current (Ih). Selective reduction of Ih with extracellular caesium diminished post-hyperpolarization excitation, whereas blockade of calcium influx had no effect. Post-hyperpolarization inhibition was caused by enhanced activation of a slowly inactivating potassium current. Selective reduction of this current with 4-aminopyridine diminished the post-hyperpolarization inhibition. 5. Chord conductances underlying both Ih and the slow-transient potassium current were measured and divided by leakage conductance to control for differences in cell size.(ABSTRACT TRUNCATED AT 400 WORDS)

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Selected References

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  1. Adams J. C. Heavy metal intensification of DAB-based HRP reaction product. J Histochem Cytochem. 1981 Jun;29(6):775–775. doi: 10.1177/29.6.7252134. [DOI] [PubMed] [Google Scholar]
  2. Avoli M. Inhibitory potentials in neurons of the deep layers of the in vitro neocortical slice. Brain Res. 1986 Apr 2;370(1):165–170. doi: 10.1016/0006-8993(86)91118-2. [DOI] [PubMed] [Google Scholar]
  3. Bargas J., Galarraga E., Aceves J. An early outward conductance modulates the firing latency and frequency of neostriatal neurons of the rat brain. Exp Brain Res. 1989;75(1):146–156. doi: 10.1007/BF00248538. [DOI] [PubMed] [Google Scholar]
  4. Biedenbach M. A., De Vito J. L., Brown A. C. Pyramidal tract of the cat: axon size and morphology. Exp Brain Res. 1986;61(2):303–310. doi: 10.1007/BF00239520. [DOI] [PubMed] [Google Scholar]
  5. Cheney P. D., Fetz E. E. Functional classes of primate corticomotoneuronal cells and their relation to active force. J Neurophysiol. 1980 Oct;44(4):773–791. doi: 10.1152/jn.1980.44.4.773. [DOI] [PubMed] [Google Scholar]
  6. Connor J. A., Stevens C. F. Prediction of repetitive firing behaviour from voltage clamp data on an isolated neurone soma. J Physiol. 1971 Feb;213(1):31–53. doi: 10.1113/jphysiol.1971.sp009366. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dekin M. S., Getting P. A., Johnson S. M. In vitro characterization of neurons in the ventral part of the nucleus tractus solitarius. I. Identification of neuronal types and repetitive firing properties. J Neurophysiol. 1987 Jul;58(1):195–214. doi: 10.1152/jn.1987.58.1.195. [DOI] [PubMed] [Google Scholar]
  8. Deschênes M., Labelle A., Landry P. Morphological characterization of slow and fast pyramidal tract cells in the cat. Brain Res. 1979 Dec 14;178(2-3):251–274. doi: 10.1016/0006-8993(79)90693-0. [DOI] [PubMed] [Google Scholar]
  9. Evarts E. V. Relation of pyramidal tract activity to force exerted during voluntary movement. J Neurophysiol. 1968 Jan;31(1):14–27. doi: 10.1152/jn.1968.31.1.14. [DOI] [PubMed] [Google Scholar]
  10. Foehring R. C., Schwindt P. C., Crill W. E. Norepinephrine selectively reduces slow Ca2+- and Na+-mediated K+ currents in cat neocortical neurons. J Neurophysiol. 1989 Feb;61(2):245–256. doi: 10.1152/jn.1989.61.2.245. [DOI] [PubMed] [Google Scholar]
  11. Friedman A., Gutnick M. J. Low-threshold calcium electrogenesis in neocortical neurons. Neurosci Lett. 1987 Oct 16;81(1-2):117–122. doi: 10.1016/0304-3940(87)90350-8. [DOI] [PubMed] [Google Scholar]
  12. Horikawa K., Armstrong W. E. A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates. J Neurosci Methods. 1988 Aug;25(1):1–11. doi: 10.1016/0165-0270(88)90114-8. [DOI] [PubMed] [Google Scholar]
  13. Hoshi T., Aldrich R. W. Voltage-dependent K+ currents and underlying single K+ channels in pheochromocytoma cells. J Gen Physiol. 1988 Jan;91(1):73–106. doi: 10.1085/jgp.91.1.73. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Landry P., Wilson C. J., Kitai S. T. Morphological and electrophysiological characteristics of pyramidal tract neurons in the rat. Exp Brain Res. 1984;57(1):177–190. doi: 10.1007/BF00231144. [DOI] [PubMed] [Google Scholar]
  15. Lemon R. N., Mantel G. W. The influence of changes in discharge frequency of corticospinal neurones on hand muscles in the monkey. J Physiol. 1989 Jun;413:351–378. doi: 10.1113/jphysiol.1989.sp017658. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Llinás R., Jahnsen H. Electrophysiology of mammalian thalamic neurones in vitro. Nature. 1982 Jun 3;297(5865):406–408. doi: 10.1038/297406a0. [DOI] [PubMed] [Google Scholar]
  17. Llinás R., Yarom Y. Electrophysiology of mammalian inferior olivary neurones in vitro. Different types of voltage-dependent ionic conductances. J Physiol. 1981 Jun;315:549–567. doi: 10.1113/jphysiol.1981.sp013763. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Matsumura M., Cope T., Fetz E. E. Sustained excitatory synaptic input to motor cortex neurons in awake animals revealed by intracellular recording of membrane potentials. Exp Brain Res. 1988;70(3):463–469. doi: 10.1007/BF00247594. [DOI] [PubMed] [Google Scholar]
  19. McCormick D. A., Connors B. W., Lighthall J. W., Prince D. A. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol. 1985 Oct;54(4):782–806. doi: 10.1152/jn.1985.54.4.782. [DOI] [PubMed] [Google Scholar]
  20. Samejima A., Yamamoto T., Ito J., Oka H. Two groups of corticofugal neurons identified with the pontine stimulation in the cat parietal association cortex: an intracellular HRP study. Brain Res. 1985 Nov 11;347(1):117–120. doi: 10.1016/0006-8993(85)90895-9. [DOI] [PubMed] [Google Scholar]
  21. Schwindt P. C., Spain W. J., Crill W. E. Long-lasting reduction of excitability by a sodium-dependent potassium current in cat neocortical neurons. J Neurophysiol. 1989 Feb;61(2):233–244. doi: 10.1152/jn.1989.61.2.233. [DOI] [PubMed] [Google Scholar]
  22. Schwindt P. C., Spain W. J., Foehring R. C., Chubb M. C., Crill W. E. Slow conductances in neurons from cat sensorimotor cortex in vitro and their role in slow excitability changes. J Neurophysiol. 1988 Feb;59(2):450–467. doi: 10.1152/jn.1988.59.2.450. [DOI] [PubMed] [Google Scholar]
  23. Schwindt P. C., Spain W. J., Foehring R. C., Stafstrom C. E., Chubb M. C., Crill W. E. Multiple potassium conductances and their functions in neurons from cat sensorimotor cortex in vitro. J Neurophysiol. 1988 Feb;59(2):424–449. doi: 10.1152/jn.1988.59.2.424. [DOI] [PubMed] [Google Scholar]
  24. Segal M. A potent transient outward current regulates excitability of dorsal raphe neurons. Brain Res. 1985 Dec 16;359(1-2):347–350. doi: 10.1016/0006-8993(85)91448-9. [DOI] [PubMed] [Google Scholar]
  25. Spain W. J., Schwindt P. C., Crill W. E. Anomalous rectification in neurons from cat sensorimotor cortex in vitro. J Neurophysiol. 1987 May;57(5):1555–1576. doi: 10.1152/jn.1987.57.5.1555. [DOI] [PubMed] [Google Scholar]
  26. Spain W. J., Schwindt P. C., Crill W. E. Two transient potassium currents in layer V pyramidal neurones from cat sensorimotor cortex. J Physiol. 1991 Mar;434:591–607. doi: 10.1113/jphysiol.1991.sp018488. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Stafstrom C. E., Schwindt P. C., Chubb M. C., Crill W. E. Properties of persistent sodium conductance and calcium conductance of layer V neurons from cat sensorimotor cortex in vitro. J Neurophysiol. 1985 Jan;53(1):153–170. doi: 10.1152/jn.1985.53.1.153. [DOI] [PubMed] [Google Scholar]
  28. Stafstrom C. E., Schwindt P. C., Crill W. E. Repetitive firing in layer V neurons from cat neocortex in vitro. J Neurophysiol. 1984 Aug;52(2):264–277. doi: 10.1152/jn.1984.52.2.264. [DOI] [PubMed] [Google Scholar]
  29. Storm J. F. Temporal integration by a slowly inactivating K+ current in hippocampal neurons. Nature. 1988 Nov 24;336(6197):379–381. doi: 10.1038/336379a0. [DOI] [PubMed] [Google Scholar]
  30. Stühmer W., Ruppersberg J. P., Schröter K. H., Sakmann B., Stocker M., Giese K. P., Perschke A., Baumann A., Pongs O. Molecular basis of functional diversity of voltage-gated potassium channels in mammalian brain. EMBO J. 1989 Nov;8(11):3235–3244. doi: 10.1002/j.1460-2075.1989.tb08483.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Yamamoto T., Samejima A., Oka H. Morphology of layer V pyramidal neurons in the cat somatosensory cortex: an intracellular HRP study. Brain Res. 1987 Dec 29;437(2):369–374. doi: 10.1016/0006-8993(87)91654-4. [DOI] [PubMed] [Google Scholar]

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