Comparison of the inhibition of Renshaw cells during subthreshold and suprathreshold conditions using anatomically and physiologically realistic models

Journal of Neurophysiology

Volumn 94, Issue 3, 2005, Pages 1688-1698

  Bui, Tuan V ^a   Dewey, Dianne E ^b   Fyffe, Robert E W ^b   Rose, P Ken ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b WRIGHT STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; GLYCINE RECEPTOR;

ARTICLE; COMPARTMENT MODEL; DENDRITE; MOTONEURON; NERVE CELL INHIBITION; NEUROANATOMY; PRIORITY JOURNAL; RENSHAW CELL; SYNAPSE; SYNAPTIC TRANSMISSION; VOLTAGE CLAMP;

ACETYLCHOLINE; ANIMALS; DIFFERENTIAL THRESHOLD; GAMMA-AMINOBUTYRIC ACID; GLYCINE; HUMANS; INTERNEURONS; MEMBRANE POTENTIALS; MODELS, NEUROLOGICAL; NEURAL INHIBITION; SYNAPSES;

EID: 23944441662     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00284.2005     Document Type: Article

References (56)

1. 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.
2. Alvarez FJ, Dewey DE, McMillin P, and Fyffe RE. Distribution of cholinergic contacts on Renshaw cells in the rat spinal cord: a light microscopic study. J Physiol 515: 787-797, 1999.
3. Baldiserra 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, vol. II.
4. Barrett JN and Crill WE. Specific membrane properties of cat motoneurones. J Physiol 239: 301-324, 1974.
5. 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.
6. Brizzi L, Meunier C, Zytnicki D, Donnet M, Hansel D, D'Incamps BL, and Van Vreeswijk C. How shunting inhibition affects the discharge of lumbar motoneurones: a dynamic clamp study in anaesthetized cats. J Physiol 558: 671-683, 2004.
7. Bui TV, Gushing S, Dewey D, Fyffe RE, and Rose PK. Comparison of the morphological and electrotonic properties of Renshaw cells, Ia inhibitory interneurons, and motoneurons in the cat. J Neurophysiol 90: 2900-2918, 2003.
8. Buisson B, Gopalakrishnan M, Arneric SP, Sullivan JP, and Bertrand D. Human alpha4beta2 neuronal nicotinic acetylcholine receptor in HEK 293 cells: a patch-clamp study. J Neurosci 16: 7880-7891, 1996.
9. Carnevale NT, Woolf TB, and Shepherd GM. Neuron simulations with SABER. J Neurosci Methods 33: 135-148, 1990.
10. Charnel P, Labarca C, Cohen BN, Davidson N, Lester HA, and Pilar G. Pharmacological and kinetic properties of alpha 4 beta 2 neuronal nicotinic acetylcholine receptors expressed in Xenopus oocytes. J Physiol 450: 375-394, 1992.
11. Covernton PJ, Kojima H, Sivilotti LG, Gibb AJ, and Colquhoun D. Comparison of neuronal nicotinic receptors in rat sympathetic neurones with subunit pairs expressed in Xenopus oocytes. J Physiol 481: 27-34, 1994.
12. 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.
13. Dourado M and Sargent PB. Properties of nicotinic receptors underlying Renshaw cell excitation by alpha-motor neurons in neonatal rat spinal cord. J Neurophysiol 87: 3117-3125, 2002.
14. Eccles JC, Eccles DM, and Fatt P. Pharmacological investigations on a central synapse operated by acetylcholine. J Physiol 131: 154-169, 1956.
15. 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.
16. Figl A, Viseshakul N, Shafaee N, Forsayeth J, and Cohen BN. Two mutations linked to nocturnal frontal lobe epilepsy cause use-dependent potentiation of the nicotinic ACh response. J Physiol 513: 655-670, 1998.
17. Gabbiani F, Midtgaard J, and Knopfel T. Synaptic integration in a model of cerebellar granule cells. J Neurophysiol 72: 999-1009, 1994.
18. Geiman EJ, Zheng W, Fritschy JM, and Alvarez FJ. Glycine and GABA(A) receptor subunits on Renshaw cells: relationship with presynaptic neurotransmitters and postsynaptic gephyrin clusters. J Comp Neurol 444: 275-289, 2002.
19. Gonzàlez-Forero D, Pastor AM, Geiman EJ, Benitez-Temino B, and Alvarez FJ. Regulation of gephyrin cluster size and inhibitory synaptic currents on Renshaw cells by motor axon excitatory inputs. J Neurosci 25: 417-429, 2005.
20. Haghighi AP and Cooper E. Neuronal nicotinic acetylcholine receptors are blocked by intracellular spermine in a voltage-dependent manner. J Neurosci 18: 4050-4062, 1998.
21. Hamm TM, Sasaki S, Stuart DG, Windhorst U, and Yuan CS. The measurement of single motor-axon recurrent inhibitory post-synaptic potentials in the cat. J Physiol 388: 631-651, 1987.
22. Heckman CJ and Binder MD. Analysis of effective synaptic currents generated by homonymous Ia afferent fibers in motoneurons of the cat. J Neurophysiol 60: 1946-1966, 1988.
23. Hille B. Ion Channels of Excitable Membranes. Sunderland, MA: Sinauer, 2001.
24. Holt GR and Koch C. Shunting inhibition does not have a divisive effect on firing rates. Neural Comput 9: 1001-1013, 1997.
25. Hultborn H, Denton ME, Wienecke J, and Nielsen JB. Variable amplification of synaptic input to cat spinal motoneurones by dendritic persistent inward current. J Physiol 552: 945-952, 2003.
26. Hultborn H and Pierrot-Deseilligny E. Input-output relations in the pathway of recurrent inhibition to motoneurones in the cat. J Physiol 297: 267-287, 1979.
27. Jonas P, Bischofberger J, and Sandkuhler J. Corelease of two fast neurotransmitters at a central synapse. Science 281: 419-424, 1998.
28. Katz R and Pierrot-Deseilligny E. Recurrent inhibition in humans. Prog Neurobiol 5T: 325-355, 1999.
29. Keller AF, Coull JA, Chery N, Poisbeau P, and De Koninck Y. Region-specific developmental specialization of GABA-glycine cosynapses in laminas I-II of the rat spinal dorsal horn. J Neurosci 21: 7871-7880, 2001.
30. Koch C. Biophysics of Computation: Information Processing in Single Neurons. New York: Oxford Univ. Press, 1999.
31. 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.
32. 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.
33. Koos T, Tepper JM, and Wilson CJ. Comparison of IPSCs evoked by spiny and fast-spiking neurons in the neostriatum. J Neurosci 24: 7916-7922, 2004.
34. Lagerback PA. An ultrastructural study of serially sectioned Renshaw cells. III. Quantitative distribution of synaptic boutons. Brain Res 264: 215-223, 1983.
35. Lee RH and Heckman CJ. Adjustable amplification of synaptic input in the dendrites of spinal motoneurons in vivo. J Neurosci 20: 6734-6740, 2000.
36. Lindsay AD and Binder MD. Distribution of effective synaptic currents underlying recurrent inhibition in cat triceps surae motoneurons. J Neurophysiol 65: 168-177, 1991.
37. Maltenfort MG, Heckman CJ, and Rymer WZ. Decorrelating actions of Renshaw interneurons on the firing of spinal motoneurons within a motor nucleus: a simulation study, J Nearophysiol 80: 309-323, 1998.
38. Maltenfort MG, McCurdy ML, Phillips CA, Turkin VV, and Hamm TM. Location and magnitude of conductance changes produced by Renshaw recurrent inhibition in spinal motoneurons. J Neurophysiol 92: 1417-1432, 2004.
39. Megias M, Emri Z, Freund TF, and Gulyas AI. Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102: 527-540, 2001.
40. Nelson ME and Lindstrom J. Single channel properties of human alpha3 AChRs: impact of beta2, beta4 and alphas subunits. J Physiol 516: 657-678, 1999.
41. Oleskevich S, Alvarez FJ, and Walmsley B. Glycinergic miniature synaptic currents and receptor cluster sizes differ between spinal cord interneurons. J Neurophysiol 82: 312-319, 1999.
42. Powers RK and Binder MD. Summation of effective synaptic currents and firing rate modulation in cat spinal motoneurons. J Neurophysiol 83: 483-500, 2000.
43. 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, vol. 1, pt. 1.
44. Renshaw B. Central effects of centripetal impulses in axons of spinal ventral roots. J Neurophysiol 9: 191-204, 1946.
45. Ross HG, Cleveland S, and Haase J. Quantitative relation between discharge frequencies of a Renshaw cell and an intracellularly depolarized motoneuron. Neurosci Lett 3: 129-132, 1976.
46. Ryall RW. Renshaw cell mediated inhibition of Renshaw cells: patterns of excitation and inhibition from impulses in motor axon collaterals. J Neurophysiol 33: 257-270, 1970.
47. Sacchi O, Rossi ML, Canella R, and Fesce R. Synaptic current at the rat ganglionic synapse and its interactions with the neuronal voltage-dependent currents. J Neurophysiol 79: 727-742, 1998.
48. Schmitt B, Knaus P, Becker CM, and Betz H. The Mr 93,000 polypeptide of the postsynaptic glycine receptor is a peripheral protein. Biochemistry 26: 805-811, 1987.
49. Schneider SP and Fyffe RE. Involvement of GABA and glycine in recurrent inhibition of spinal motoneurons. J Neurophysiol 68: 397-406, 1992.
50. Stuart GJ and Redman SJ. Voltage dependence of Ia reciprocal inhibitory currents in cat spinal motoneurones. J Physiol 420: 111-125, 1990.
51. Trevelyan AJ and Watkinson O. Does inhibition balance excitation in neocortex? Prog Biophys Mol Biol 87: 109-143, 2005.
52. Ulrich D. Differential arithmetic of shunting inhibition for voltage and spike rate in neocortical pyramidal cells. Eur J Neurosci 18: 2159-2165, 2003.
53. Van Keulen L. Autogenetic recurrent inhibition of individual spinal motoneurones of the cat. Neurosci Lett 21: 297-300, 1981.
54. Walmsley B and Tracey DJ. An intracellular study of Renshaw cells. Brain Res 223: 170-175, 1981.
55. Windhorst U. On the role of recurrent inhibitory feedback in motor control. Prog Neurobiol 49: 517-587, 1996.
56. Yang KH, Franaszczuk PJ, and Bergey GK. The influences of somatic and dendritic inhibition on bursting patterns in a neuronal circuit model. Biol Cybern 89: 242-253, 2003.