Recovery of cable properties through active and passive modeling of subthreshold membrane responses from laterodorsal tegmental neurons

Journal of Neurophysiology

Volumn 80, Issue 5, 1998, Pages 2593-2607

  Surkis, A ^a   Peskin, C S ^a   Tranchina, D ^a   Leonard, C S ^b  

^a NEW YORK UNIVERSITY   (United States)

^b NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TETRODOTOXIN;

ANIMAL CELL; ARTICLE; CHOLINERGIC NERVE; CONTROLLED STUDY; FEMALE; GUINEA PIG; HYPERPOLARIZATION; MEMBRANE CONDUCTANCE; MEMBRANE STEADY POTENTIAL; NONHUMAN; PONS RETICULAR FORMATION; POTASSIUM CURRENT; PRIORITY JOURNAL; REM SLEEP; TEGMENTUM; WAKEFULNESS;

EID: 0031761847     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1998.80.5.2593     Document Type: Article

References (59)

1. BAGHDOYAN, H. A., RODRIGO-ANGULO, M. L., MCCARLEY, R. W., AND HOBSON, J. A. A neuroanatomical gradient in the pontine tegmentum for the cholinoceptive induction of desynchronized sleep signs. Brain Res. 414: 245-261, 1987.
2. BROWN, T. H., PERKEL, D. H., NORRIS, J. C., AND PEACOCK, J. H. Electrotonic structure and specific membrane properties of mouse dorsal root ganglion neurons. J. Neurophysiol. 45: 1-15, 1981.
3. BURKE, R. E., FYFFE, R.E.W., AND MOSCHOVAKIS, A. K. Electrotonic architecture of cat gamma motoneurons. J. Neurophysiol. 72: 2302-2316, 1994.
4. CAPOWSKI, J. J. The reconstruction, display, and analysis of neuronal structure using a computer. In: The Microcomputer in Cell and Neurobiology Research, edited by R. R. Mize. New York: Elsevier, 1985, p. 85-109.
5. CLEMENTS, J. D. AND REDMAN, S. J. Cable properties of cat spinal motoneurones measured by combining voltage clamp, current clamp and intracellular staining. J. Physiol. (Lond.) 409: 63-87, 1989.
6. COLE, K. S. Membrane, Ions and Impulses. Berkeley, CA: University of California Press, 1968.
7. EL MANSARI, M., SAKAI, K., AND JOUVET, M. Unitary characteristics of presumptive cholinergic tegmental neurons during the sleep-waking cycle in freely moving cats. Exp. Brain Res. 76: 519-529, 1989.
8. HALLANGER, A., LEVEY, A., LEE, H., RYE, D., AND WAINER, B. The origins of cholinergic and other subcortical afferents to the thalamus in the rat. J. Comp. Neural 262: 105-124, 1987.
9. HINES, M. A program for simulation of nerve equations with branching geometries. Int. J. Biomed. Comput. 24: 55-68, 1989.
10. 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.
11. HUGUIENARD, J. R., COULTER, D. A., AND PRINCE, D. A. A fast transient potassium current in thalamic relay neurons: kinetics of activation and inactivation. J. Neurophysiol. 66: 1304-1315, 1991.
12. HUGUENARD, J. R. AND MCCORMICK, D. A. Simulations of the currents involved in rhythmic oscillations in thalamic relay neurons. J. Neurophysiol. 68: 1992.
13. JOHNSTON, D., MAGEE, J., COLBERT, C. M., AND CHRISTIE. B. R. Active properties of neuronal dendrites. Anna. Rev. Neurosci. 19: 165-186, 1996.
14. JONES, B. E. Immunohistochemical study of choline acetyltransferase-immunoreactive processes and cells innervating the pontomedullary reticular formation in the rat. J. Comp. Neural. 295: 485-514, 1990.
15. JONES, B. E. Paradoxical sleep and its chemical substrates in the brain. Neuroscience 40: 637-656, 1991.
16. KAYAMA, Y., OHTA, M., AND JODO, E. Firing of "possibly" cholinergic neurons in the rat laterodorsal tegmental nucleus during sleep and wakefulness. Brain Res. 569: 210-220, 1992.
17. LEONARD, C. S., KERMAN, I., BLAHA, G., TAVERAS, E., AND TAYLOR, B. Interdigitation of nitric oxide synthase-, tyrosine hydroxylase- and serotonin-containing neurons in and around the laterodorsal and pedunculopontine tegmental nuclei of the guinea pig. J. Comp. Neural. 362: 411-432, 1995.
18. LEONARD, C. S. AND KUMAR, A.K.P. A persistent sodium current underlying subthreshold membrane potential oscillations in mesopontine cholinergic neurons in vitro. Soc. Neurosci. Abstr. 19: 1761, 1993.
19. LEONARD, C. S. AND LLINÁS, R. Electrophysiology of mammalian pedunculopontine and laterodorsal tegmental neurons in vitro: implications for the control of REM sleep. In: Brain Cholinergic Systems, edited by M. Steriade and D. Biesold. New York: Oxford Univ. Press, 1990, p. 205-223,
20. LEONARD, C. S. AND LLINÁS, R. Serotonergic and cholinergic inhibition of mesopontine cholinergic neurons controlling REM sleep: an in vitro electrophysiological study. Neuroscience 59: 309-330, 1994.
21. MAJOR, G. The Physiology, Morphology and Modelling of Cortical Pyramidal Neurones (PhD thesis). Oxford, UK: Oxford University, 1992.
22. MAJOR, G., LARKMAN, A. U., JONAS, P., SAKMANN, B., AND JACK, J.J.B. Detailed passive cable models of whole-cell recorded CA3 pyramidal neurons in rat hippocampal slices. J. Neurosci. 14: 4613-4638, 1994.
23. MASCAGNI, M. V. Numerical methods for neuronal modeling. In: Methods in Neuronal Modeling, edited by C. Koch and I. Segev. Cambridge, MA: MIT Press, 1989, p. 439-484.
24. MCCORMICK, D. A. AND PAPE, H.-C. Properties of a hyperpolarization-activated cation current and its role in rhythmic oscillation in thalamic relay neurones. J. Physiol. (Lond.) 431: 291-318, 1990.
25. MEL, B. W. Information processing in dendritic trees. Neural Comput. 6: 1031-1085, 1994.
26. MESULAM, M.-M., MUFSON, E. J., WAINER, B. H., AND LEVEY, A. I. Central cholinergic pathways in the rat: an overview based on an alternative nomenclature. Neuroscience 10: 1185-1201, 1983.
27. MITANI, A., ITO, K., HALLANGER, A. E., WAINER, B. H., KATAOKA, K., AND MCCARLEY, R. W. Cholinergic projections from the laterodorsal and pedunculopontine tegmental nuclei to the pontine gigantocellular tegmental field in the cat. Brain Res. 451: 397-402, 1988.
28. NELDER, J. A. AND MEAD, R. A geometric technique for optimisation. Comput. J. 7: 308-327, 1965.
29. O'BOYLE, M. P., CARNEVALE, N. T., CLAIBORNE, B. J., AND BROWN, T. H. A new graphical approach for visualizing the relationship between anatomical and electrotonic structure. In: Computational Neuroscience: Trends in Research 1995, edited by J. M. Bower. San Diego, CA: Academic, 1996, p. 423-428.
30. O'BOYLE, M., RAHIMI, O., BROWN, T. H., AND CLAIBORNE, B. J. Improved dendritic diameter measurements yield higher input resistances in modeled dentate granule neurons. Soc. Neurosci. Abstr. 19: 799, 1993.
31. ORNUNG, G. AND ULFHAKE, B. Changes in size and shape during histochemical preparation for light and electron microscopy of neurons intracellularly labelled with horseradish peroxidase. Acta Physiol. Scand. 140: 501-506, 1990.
32. PONGRACZ, F., FIRESTEIN. S., AND SHEPHERD, G. M. Electrotonic structure of olfactory sensory neurons analyzed by intracellular and whole cell patch techniques. J Neurophysiol. 65: 747-759. 1991.
33. PRESS, W. H., FLANNERY, B. P., TEUKOLSKY, S. A., AND VETTERLING, W. T. Numerical Recipes in C: The Art of Scientific Computing. Cambridge, UK: Cambridge Univ. Press, 1988.
34. QUATTROCHI, J. J., MAMELAK, A. N., MADISON, R. D., MACKLIS, J. D., AND HOBSON, J. A. Mapping neuronal inputs to REM sleep induction sites with carbachol-fluorescent microspheres. Science 245: 984-986, 1989.
35. RAINNIE, D. G., GRUNZE, H.C.R., MCCARLEY, R. W., AND GREENE, R. W. Adenosine inhibition of mesopontine cholinergic neurons: implications for EEG arousal. Science 263: 689-692, 1994.
36. RALL, W. Theory of physiological properties of dendrites. Ann. NY Acad. Sci. 96: 1071-1092, 1962.
37. RALL, W. Core conductor theory and cable properties of neurons. In: Handbook of Physiology. The Nervous System. Cellular Biology of Neurons. Bethesda, MD: Am. Physiol. Soc., 1977, sect. 1, vol. I, p. 39-97.
38. RALL, W., BURKE, R. E., HOLMES, W. R., JACK, J.J.B., REDMAN, S. J., AND SEGEV, I. Matching dendritic neuron models to experimental data. Physiol. Rev. 72, Suppl. 4: S159-S186, 1992.
39. RAPP, M., SEGEV, I, AND YAROM, Y. Physiology, morphology and detailed passive models of guinea-pig cerebellar Purkinje cells. J. Physiol. (Lond.) 474: 101-118, 1994.
40. SANCHEZ, R., SURKIS, A., AND LEONARD, C. S. Voltage-clamp analysis and computer simulation of a novel cesium-resistant A-current in guinea pig laterodorsal tegmental neurons. J. Neurophysiol. 79: 3111-3126, 1998.
41. SATOH, K. AND FIBIGER, H. C. Cholinergic neurons of the laterodorsal tegmental nucleus: efferent and afferent connections. J. Comp. Neurol. 253: 277-302, 1986.
42. SEMBA, K. Aminergic and cholinergic afferents to REM sleep induction regions of the pontine reticular formation in the rat. J. Comp. Neural. 330: 543-556, 1993.
43. SHELTON, D. P. Membrane resistivity estimated for the Purkinje neuron by means of a passive computer model. Neuroscience 14: 111-131, 1985.
44. SHUTE, C.C.D. AND LEWIS, P. R. The ascending cholinergic reticular system: neocortical, olfactory and subcortical projections. Brain 90: 497-520, 1967.
45. SOFRONIEW, M. V., PRIESTLEY, J. V., CONSOLAZIONE, A., ECKENSTEIN, F., AND CUELLO, A. C. Cholinergic projections from the midbrain and pons to the thalamus in the rat, identified by combined retrograde tracing and choline acetyltransferase immunohistochemistry. Brain Res. 329: 213-223, 1985.
46. SPRUSTON, 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.
47. 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.
48. STERIADE, M., DATTA, S., PARE, D., OAKSON, G., AND CURRO DOSSI, R. Neuronal activities in the brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical system. J. Neurosci. 10: 2541-2559, 1990a.
49. STERIADE, M. AND MCCARLEY, R. W. Brainstem Control of Wakefulness and Sleep. New York: Plenum, 1990.
50. STERIADE, M., PARE, D., DATTA, S., OAKSON, G., AND CURRO DOSSI, R. Different cellular types in mesopontine cholinergic nuclei related to ponto-geniculo-occipital waves. J. Neurosci. 10: 2560-2579, 1990b.
51. SURKIS, A., TAYLOR, B., PESKIN, C. S., AND LEONARD, C. S. Quantitative morphology of physiologically identified and intracellularly labeled neurons from the guina pig laterodorsal tegmental nucleus in vitro. Neuroscience 74: 375-392, 1996.
52. TAKAKUSAKI, K., SHIROYAMA, T., AND KITAI, S. T. Two types of cholinergic neurons in the rat tegmental pedunculopontine nucleus: electrophysiological and morphological characterization. Neuroscience 79: 1089-1109, 1997.
53. 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.
54. ULRICH, D., QUADRONI, R., AND LUSCHER, H. Electrotonic structure of motoneurons in spinal cord slice cultures: a comparison of compartmental and equivalent cylinder models. J. Neurophysiol. 72: 861-871, 1994.
55. VANNI-MERCIER, G., SAKAI, G., LIN, J. S., AND JOUVET, M. Mapping of cholinoceptive brainstem structures responsible for the generation of paradoxical sleep in the cat. Arch. Ital. Biol. 127: 133-164, 1989.
56. VINCENT, S. R. AND KIMURA, H. Histochemical mapping of nitric oxide synthase in the rat brain. Neuroscience 46: 755-784, 1992.
57. WAINER, B. H. AND MESULAM, M.-M. Ascending cholinergic pathways in the rat brain. In: Brain Cholinergic Systems, edited by M. Steriade and D. Biesold. New York: Oxford Univ. Press, 1990, p. 65-119.
58. WOOLF, N. Cholinergic systems in mammalian brain and spinal cord. Prog. Neurobiol 37: 475-524, 1991.
59. WOOLF, N. J. AND BUTCHER, L. L. Cholinergic systems in the rat brain. III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia and basal forebrain. Brain Res. Bull. 16: 603-637, 1986.