Comparison of the Morphological and Electrotonic Properties of Renshaw Cells, Ia Inhibitory Interneurons, and Motoneurons in the Cat

Journal of Neurophysiology

Volumn 90, Issue 5, 2003, Pages 2900-2918

  Bui, T V ^b   Cushing, S ^b   Dewey, D ^a   Fyffe, R E ^a   Rose, P K ^b  

^a WRIGHT STATE UNIVERSITY   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

AMPLITUDE MODULATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CAT; CELL FUNCTION; CELL STRUCTURE; COMPARATIVE STUDY; COMPARTMENT MODEL; CONTROLLED STUDY; DENDRITE; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; INTERNEURON; ION TRANSPORT; MOTONEURON; NONHUMAN; PRIORITY JOURNAL; RENSHAW CELL; THREE DIMENSIONAL IMAGING;

ANIMALS; CATS; ELECTRIC CONDUCTIVITY; EXCITATORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; MOTOR NEURONS; NEURAL INHIBITION;

EID: 0242509065     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00533.2003     Document Type: Article

References (93)

1. Agmon-Snir and Segev I. Signal delay and input synchronization in passive dendritic structures. J Neurophysiol 70: 2066-2085, 1993.
2. Alvarez FJ, Dewey DE, Harrington DA, and Fyffe RE. Cell-type specific organization of glycine receptor clusters in the mammalian spinal cord. J Comp Neurol 379: 150-170, 1997.
3. Ascoli GA. Progress and perspectives in computational neuroanatomy. Anat Rec 257: 195-207, 1999.
4. Baldissera F, Hultborn H, and Illert M. Integration in spinal neuronal systems. In: Handbook of Physiology. The Nervous System. Motor Control. Bethesda, MD: Am. Physiol. Soc., 1981, sect. 1, vol. II, p. 509-595.
5. Barrett JN and Crill WE. Specific membrane properties of cat motoneurones. J Physiol 239: 301-324, 1974.
6. Bennett DJ, Hultborn H, Fedirchuk B, and Gorassini M. Synaptic activation of plateaus in hindlimb motoneurons of decerebrate cats. J Neurophysiol 80: 2023-2037, 1998.
7. Bernander O, Douglas RJ, Martin KA, and Koch C. Synaptic background activity influences spatiotemporal integration in single pyramidal cells. Proc Natl Acad Sci USA 88: 11569-11573, 1991.
8. Bernander O, Koch C, and Douglas RJ. Amplification and linearization of distal synaptic input to cortical pyramidal cells. J Neurophysiol 72: 2743-2753, 1994.
9. Bras H, Gogan P, and Tyc-Dumont S. The dendrites of single brain-stem motoneurons intracellularly labelled with horseradish peroxidase in the cat. Morphological and electrical differences. Neuroscience 22: 947-970, 1987.
10. Bui T, Cushing S, Dewey D, Fyffe REW, Richmond FJR, and Rose PK. A comparison of the morphoelectrotonic characteristics of spinal motoneurons, Ia inhibitory interneurons and Renshaw cells. Soc Neurosci Abstr 26: 257.15, 2000.
11. Burke RE, Dum RP, Fleshman JW, Glenn LL, Lev-Tov A, O'Donovan MJ, and Pinter MJ. A HRP study of the relation between cell size and motor unit type in cat ankle extensor motoneurons. J Comp Neurol 209: 17-28, 1982.
12. Burke RE, Fyffe RE, and Moschovakis AK. Electrotonic architecture of cat gamma motoneurons. J Neurophysiol 72: 2302-2316, 1994.
13. Carlin KP, Jones KE, Jiang Z, Jordan LM, and Brownstone RM. Dendritic L-type calcium currents in mouse spinal motoneurons: implications for bistability. Eur J Neurosci 12: 1635-1646, 2000.
14. Carnevale NT, Tsai KY, Claiborne BJ, and Brown TH. Comparative electrotonic analysis of three classes of rat hippocampal neurons. J Neurophysiol 78: 703-720, 1997.
15. Carnevale NT, Woolf TB, and Shepherd GM. Neuron simulations with SABER. J Neurosci Methods 33: 135-148, 1990.
16. Carr PA, Pearson JC, and Fyffe RE. Distribution of 5-hydroxytryptamine-immunoreactive boutons on immunohistochemically-identified Renshaw cells in cat and rat lumbar spinal cord. Brain Res 823: 198-201, 1999.
17. Chance FS, Abbott LF, and Reyes AD. Gain modulation from background synaptic input. Neuron 35: 773-782, 2002.
18. Chitwood RA, Hubbard A, and Jaffe DB. Passive electrotonic properties of rat hippocampal CA3 interneurones. J Physiol 515: 743-756, 1999.
19. Clements JD and Redman SJ. Cable properties of cat spinal motoneurones measured by combining voltage clamp, current clamp and intracellular staining. J Physiol 409: 63-87, 1989.
20. Cullheim S, Fleshman JW, Glenn LL, and Burke RE. Membrane area and dendritic structure in type-identified triceps surae alpha motoneurons. J Comp Neurol 255: 68-81, 1987.
21. Derjean D, Bertrand S, Le Masson G, Landry M, Morisset V, and Nagy F. Dynamic balance of metabotropic inputs causes dorsal horn neurons to switch functional states. Nat Neurosci 6: 274-281, 2003.
22. Durand D. The somatic shunt cable model for neurons. Biophys J 46: 645-653, 1984.
23. Eccles JC, Fatt P, and Koketsu K. Cholinergic and inhibitory synapses in a pathway from motor-axon collaterals to motoneurones. J Physiol 126: 524-562, 1954.
24. Edwards DH Jr and Mulloney B. Compartmental models of electrotonic structure and synaptic integration in an identified neurone. J Physiol 348: 89-113, 1984.
25. Efron B. Ann Stat 7: Bootstrap Methods: Another Look at the Jacknife. Ann Stat 7: 1-26, 1979.
26. Finkel AS and Redman SJ. The synaptic current evoked in cat spinal motoneurones by impulses in single group Ia axons. J Physiol 342: 615-632, 1983.
27. Fleshman JW, Segev I, and Burke RB. Electrotonic architecture of type-identified alpha-motoneurons in the cat spinal cord. J Neurophysiol 60: 60-85, 1988.
28. Fyffe RE. Evidence for separate morphological classes of Renshaw cells in the cat's spinal cord. Brain Res 536: 301-304, 1990.
29. Fyffe RE. Glycine-like immunoreactivity in synaptic boutons of identified inhibitory interneurons in the mammalian spinal cord. Brain Res 547: 175-179, 1991a.
30. Fyffe RE. Spatial distribution of recurrent inhibitory synapses on spinal motoneurons in the cat. J Neurophysiol 65: 1134-1149, 1991b.
31. Helmchen F. Dendrites as biochemical compartments. In: Dendrites, edited by Stuart G, Spruston N, and Hausser M. Oxford, UK: Oxford Univ. Press, 1999, p. 161-192.
32. Hille B. Ion Channels of Excitable Membranes. Sunderland, MA: Sinauer Associates, 2001.
33. Ho N and Destexhe A. Synaptic background activity enhances the responsiveness of neocortical pyramidal neurons. J Neurophysiol 84: 1488-1496, 2000.
34. Hoffman DA, Magee JC, Colbert CM, and Johnston D. K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387: 869-875, 1997.
35. Holmes WR and Rall W. Electrotonic length estimates in neurons with dendritic tapering or somatic shunt. J Neurophysiol 68: 1421-1437, 1992.
36. Horcholle-Bossavit G, Gogan P, Ivanov Y, Korogod S, and Tyc-Dumont S. The problem of the morphological noise in reconstructed dendritic arborizations. J Neurosci Methods 95: 83-93, 2000.
37. 2+-mediated plateau potentials in a subpopulation of interneurons in the ventral horn of the turtle spinal cord. Eur J Neurosci 4: 183-188, 1992.
38. Hsiao CF, del Negro CA, Trueblood PR, and Chandler SH. Ionic basis for serotonin-induced bistable membrane properties in guinea pig trigeminal motoneurons. J Neurophysiol 79: 2847-2856, 1998.
39. Hultborn H, Jankowska E, and Lindstrom S. Recurrent inhibition of interneurones monosynaptically activated from group Ia afferents. J Physiol 215: 613-636, 1971.
40. Jack JJ, Noble D, and Tsien RW. Electric Current Flow in Excitable Cells. London: Oxford Univ. Press, 1975.
41. Jaffe DB and Carnevale NT. Passive normalization of synaptic integration influenced by dendritic architecture. J Neurophysiol 82: 3268-3285, 1999.
42. Jankowska E. Interneuronal relay in spinal pathways from proprioceptors. Prog Neurobiol 38: 335-378, 1992.
43. Jordan LM and McCrea DA. Analysis of the effects of p-methoxy-phenyl-ethylamine on spinal cord neurones. Br J Pharmacol 57: 191-199, 1976.
44. Kernell D and Zwaagstra B. Size and remoteness: two relatively independent parameters of dendrites, as studied for spinal motoneurones of the cat. J Physiol 413: 233-254, 1989.
45. Kiehn O, Kjaerulff O, Tresch MC, and Harris-Warrick RM. Contributions of intrinsic motor neuron properties to the production of rhythmic motor output in the mammalian spinal cord. Brain Res Bull 53: 649-659, 2000.
46. Koch C, Bernander O, and Douglas RJ. Do neurons have a voltage or a current threshold for action potential initiation? J Comput Neurosci 2: 63-82, 1995.
47. Koch C, Poggio T, and Torre V. Nonlinear interactions in a dendritic tree: localization, timing, and role in information processing. Proc Natl Acad Sci USA 80: 2799-2802, 1983.
48. Korogod SM, Kulagina IB, Horcholle-Bossavit G, Gogan P, and Tyc-Dumont S. Activity-dependent reconfiguration of the effective dendritic field of motoneurons. J Comp Neurol 422: 18-34, 2000.
49. Lagerback PA and Kellerth JO. Light microscopic observations on cat Renshaw cells after intracellular staining with horseradish peroxidase. II. The cell bodies and dendrites. J Comp Neurol 240: 368-376, 1985.
50. Larkum ME, Launey T, Dityatev A, and Luscher HR. Integration of excitatory postsynaptic potentials in dendrites of motoneurons of rat spinal cord slice cultures. J Neurophysiol 80: 924-935, 1998.
51. Lee RH and Heckman CJ. Adjustable amplification of synaptic input in the dendrites of spinal motoneurons in vivo. J Neurosci 20: 6734-6740, 2000.
52. Lee RH and Heckman CJ. Essential role of a fast persistent inward current in action potential initiation and control of rhythmic firing. J Neurophysiol 85: 472-475, 2001.
53. Lee RH, Kuo JJ, Jiang MC, and Heckman CJ. Influence of active dendritic currents on input-output processing in spinal motoneurons in vivo. J Neurophysiol 89: 27-39, 2003.
54. London M, Meunier C, and Segev I. Signal transfer in passive dendrites with nonuniform membrane conductance. J Neurosci 19: 8219-8233, 1999.
55. London M and Segev I. Synaptic scaling in vitro and in vivo. Nat Neurosci 4: 853-855, 2001.
56. Magee JC. Dendritic integration of excitatory synaptic input. Nat Rev Neurosci 1: 181-190, 2000.
57. Magee JC and Cook EP. Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons. Nat Neurosci 3: 895-903, 2000.
58. Mainen ZF, Carnevale NT, Zador AM, Claiborne BJ, and Brown TH. Electrotonic architecture of hippocampal CA1 pyramidal neurons based on three-dimensional reconstructions. J Neurophysiol 76: 1904-1923, 1996.
59. Mainen ZF and Sejnowski TJ. Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382: 363-366, 1996.
60. Major G. Passive cable modeling - a practical introduction. In: Computational Neuroscience: Realistic Modeling for Experimentalists, edited by De Schutter E. New York: CRC Press, 2000, p. 209-232.
61. Major G, Larkman AU, Jonas P, Sakmann B, and Jack JJ. Detailed passive cable models of whole-cell recorded CA3 pyramidal neurons in rat hippocampal slices. J Neurosci 14: 4613-4638, 1994.
62. McCrea DA, Pratt CA, and Jordan LM. Renshaw cell activity and recurrent effects on motoneurons during fictive locomotion. J Neurophysiol 44: 475-488, 1980.
63. Migliore M and Shepherd GM. Emerging rules for the distributions of active dendritic conductances. Nat Rev Neurosci 3: 362-370, 2002.
64. Nitzan R, Segev I, and Yarom Y. Voltage behavior along the irregular dendritic structure of morphologically and physiologically characterized vagal motoneurons in the guinea pig. J Neurophysiol 63: 333-346, 1990.
65. Powers RK and Binder MD. Persistent sodium and calcium currents in rat hypoglossal motoneurons. J Neurophysiol 89: 615-624, 2003.
66. Prescott SA and De Koninck Y. Gain control of firing rate by shunting inhibition: roles of synaptic noise and dendritic saturation. Proc Natl Acad Sci USA 100: 2076-2081, 2003.
67. Raastad M, Enriquez-Denton M, and Kiehn O. Synaptic signaling in an active central network only moderately changes passive membrane properties. Proc Natl Acad Sci USA 95: 10251-10256, 1998.
68. Rall W. Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. J Neurophysiol 30: 1138-1168, 1967.
69. Rail 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.
70. Rail W and Agmon-Snir H. Cable theory for dendritic neurons. In: Methods in Neuronal Modeling: From Ions to Networks, edited by Koch C and Segev I. Cambridge, MA: MIT Press, 1999, p. 27-92.
71. Rastad J, Gad P, Jankowska E, McCrea D, and Westman J. Light microscopical study of dendrites and perikarya of interneurones mediating Ia reciprocal inhibition of cat lumbar alpha-motoneurones. Anat Embryol (Berl) 181: 381-388, 1990.
72. Reyes A. Influence of dendritic conductances on the input-output properties of neurons. Annu Rev Neurosci 24: 653-675, 2001.
73. Rose PK and Cushing S. Non-linear summation of synaptic currents on spinal motoneurons: lessons from simulations of the behaviour of anatomically realistic models. Prog Brain Res 123: 99-107, 1999.
74. Rose PK, Jones T, Nirula R, and Corneil T. Innervation of motoneurons based on dendritic orientation. J Neurophysiol 73: 1319-1322, 1995.
75. Rose PK, Keirstead SA, and Vanner SJ. A quantitative analysis of the geometry of cat motoneurons innervating neck and shoulder muscles. J Comp Neurol 239: 89-107, 1985.
76. Rose PK and Neuber-Hess M. Morphology and frequency of axon terminals on the somata, proximal dendrites, and distal dendrites of dorsal neck motoneurons in the cat. J Comp Neurol 307: 259-280, 1991.
77. Rose PK and Vanner SJ. Differences in somatic and dendritic specific membrane resistivity of spinal motoneurons: an electrophysiological study of neck and shoulder motoneurons in the cat. J Neurophysiol 60: 149-166, 1988.
78. Roth A and Hausser M. Compartmental models of rat cerebellar Purkinje cells based on simultaneous somatic and dendritic patch-clamp recordings. J Physiol 535: 445-472, 2001.
79. Russo RE and Hounsgaard J. Plateau-generating neurones in the dorsal horn in an in vitro preparation of the turtle spinal cord. J Physiol 493 (Pt 1): 39-54, 1996.
80. Schwindt P and Crill W. Mechanisms underlying burst and regular spiking evoked by dendritic depolarization in layer 5 cortical pyramidal neurons. J Neurophysiol 81: 1341-1354, 1999.
81. Segev I and London M. Untangling dendrites with quantitative models. Science 290: 744-750, 2000.
82. Sherrington CS. Integrative Action of the Nervous System. New Haven, CT: Yale Univ. Press, 1947.
83. Stacey WC and Durand DM. Stochastic resonance improves signal detection in hippocampal CA1 neurons. J Neurophysiol 83: 1394-1402, 2000.
84. Stuart G and Spruston N. Determinants of voltage attenuation in neocortical pyramidal neuron dendrites. J Neurosci 18: 3501-3510, 1998.
85. Svirskis G, Gutman A, and Hounsgaard J. Electrotonic structure of motoneurons in the spinal cord of the turtle: inferences for the mechanisms of bistability. J Neurophysiol 85: 391-398, 2001.
86. Thurbon D, Luscher HR, Hofstetter T, and Redman SJ. Passive electrical properties of ventral horn neurons in rat spinal cord slices. J Neurophysiol 79: 2485-2502, 1998.
87. Ulfhake B and Kellerth JO. A quantitative light microscopic study of the dendrites of cat spinal alpha-motoneurons after intracellular staining with horseradish peroxidase. J Comp Neurol 202: 571-583, 1981.
88. Ulrich D, Quadroni R, and Luscher HR. Electronic structure of motoneurons in spinal cord slice cultures: a comparison of compartmental and equivalent cylinder models. J Neurophysiol 72: 861-871, 1994,
89. Williams SR and Stuart GJ. Mechanisms and consequences of action potential burst firing in rat neocortical pyramidal neurons. J Physiol 521: 467-482, 1999.
90. Williams SR and Stuart GJ. Role of dendritic synapse location in the control of action potential output. Trends Neurosci 26: 147-154, 2003.
91. Windhorst U. Activation of Renshaw cells. Prog Neurobiol 35: 135-179, 1990.
92. Zador AM, Agmon-Snir H, and Segev I. The morphoelectrotonic transform: a graphical approach to dendritic function. J Neurosci 15: 1669-1682, 1995.
93. Zar JH. Biostatistical Analysis. Upper Saddle River, NJ: Prentice-Hall, 1996.