Characteristics and organization of discharge properties in rat hindlimb motoneurons

Journal of Neurophysiology

Volumn 104, Issue 3, 2010, Pages 1549-1565

  Turkin, Vladimir V ^a   O'Neill, Derek ^a   Jung, Ranu ^b   Iarkov, Alexandre ^b   Hamm, Thomas M ^a  

^a BARROW NEUROLOGICAL INSTITUTE   (United States)

^b Arizona State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KETAMINE; XYLAZINE;

AFTERHYPERPOLARIZATION; ANIMAL EXPERIMENT; ARTICLE; CELL MEMBRANE POTENTIAL; CELLULAR DISTRIBUTION; CONDUCTANCE; HINDLIMB; HYSTERESIS; MOTONEURON; NONHUMAN; PREVALENCE; PRIORITY JOURNAL; RAT;

ACTION POTENTIALS; ANIMALS; HINDLIMB; MOTOR NEURONS; RATS; RATS, LONG-EVANS; RECRUITMENT, NEUROPHYSIOLOGICAL;

EID: 77957200374     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00379.2010     Document Type: Article

References (73)

1. Bakels R, Kernell D. Average but not continuous speed match between motoneurons and muscle units of rat tibialis anterior. J Neurophysiol 70: 1300-1306, 1993a. (Pubitemid 23326368)
2. Bakels R, Kernell D. Matching between motoneurone and muscle unit properties in rat medial gastrocnemius. J Physiol 463: 307-324, 1993b. (Pubitemid 23120588)
3. Baldissera F, Campadelli P, Piccinelli L. Neural encoding of input transients investigated by intracellular injection of ramp currents in cat alpha-motoneurones. J Physiol 328: 73-86, 1982. (Pubitemid 12090155)
4. Beaumont E, Houle JD, Peterson CA, Gardiner PF. Passive exercise and fetal spinal cord transplant both help to restore motoneuronal properties after spinal cord transection in rats. Muscle Nerve 29: 234-242, 2004. (Pubitemid 38166845)
5. Beaumont E, Kaloustian S, Rousseau G, Cormery B. Training improves the electrophysiological properties of lumbar neurons and locomotion after thoracic spinal cord injury in rats. Neurosci Res 62: 147-154, 2008.
6. Bennett DJ, Li Y, Siu M. Plateau potentials in sacrocaudal motoneurons of chronic spinal rats, recorded in vitro. J Neurophysiol 86: 1955-1971, 2001.
7. Bennett DJ, Sanelli L, Cooke CL, Harvey PJ, Gorassini MA. Spastic long-lasting reflexes in the awake rat after sacral spinal cord injury. J Neurophysiol 91: 2247-2258, 2004. (Pubitemid 38500940)
8. Binder MD, Heckman CJ, Powers RK. The physiological control of motoneuron activity. In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems. Neural Control of Movement. Bethesda, MD: Am. Physiol. Soc., 1996, sect. 12, p. 3-53.
9. Brownstone RM, Jordan LM, Kriellaars DJ, Noga BR, Shefchyk SJ. On the regulation of repetitive firing in lumbar motoneurones during fictive locomotion in the cat. Exp Brain Res 90: 441-455, 1992.
10. Bui TV, Ter-Mikaelian M, Bedrossian D, Rose PK. Computational estimation of the distribution of L-type Ca(2+) channels in motoneurons based on variable threshold of activation of persistent inward currents. J Neurophysiol 95: 225-241, 2006. (Pubitemid 44698931)
11. Burke RE, Nelson PG. Accommodation to current ramps in motoneurons of fast and slow twitch motor units. Int J Neurosci 1: 347-356, 1971.
12. Button DC, Gardiner K, Marqueste T, Gardiner PF. Frequency-current relationships of rat hindlimb alpha-motoneurones. J Physiol 573: 663-677, 2006. (Pubitemid 43842509)
13. Button DC, Kalmar JM, Gardiner K, Cahill F, Gardiner PF. Spike frequency adaptation of rat hindlimb motoneurons. J Appl Physiol 102: 1041-1050, 2007. (Pubitemid 46377030)
14. Button DC, Kalmar JM, Gardiner K, Marqueste T, Zhong H, Roy RR, Edgerton VR, Gardiner PF. Does elimination of afferent input modify the changes in rat motoneurone properties that occur following chronic spinal cord transection? J Physiol 586: 529-544, 2008.
15. Cormery B, Beaumont E, Csukly K, Gardiner P. Hindlimb unweighting for 2 weeks alters physiological properties of rat hindlimb motoneurones. J Physiol 568: 841-850, 2005. (Pubitemid 41646025)
16. V1.3 channels in cat lumbar motoneurons: spatial distribution. J Neurophysiol 94: 3961-3974, 2005.
17. 2+ persistent inward currents in spinal motoneurones: mode of activation and integration of synaptic inputs. J Physiol 570: 355-374, 2006.
18. Ermentrout GB. Linearization of f-I curves by adaptation. Neural Comput 10: 1721-1729, 1998.
19. Gardiner PF. Physiological properties of motoneurons innervating different muscle unit types in rat gastrocnemius. J Neurophysiol 69: 1160-1170, 1993.
20. Gorassini M, Eken T, Bennett DJ, Kiehn O, Hultborn H. Activity of hindlimb motor units during locomotion in the conscious rat. J Neurophysiol 83: 2002-2011, 2000.
21. Granit R, Kernell D, Shortess GK. Quantitative aspects of repetitive firing of mammalian motoneurones, caused by injected currents. J Physiol 168: 911-931, 1963.
22. Hamm TM, Turkin VV, Bandekar N, O'Neill D, Jung R. Persistent currents and discharge patterns of rat hindlimb motoneurons. J Neurophysiol 104: 1566-1577, 2010.
23. Heckman CJ, Binder MD. Computer simulations of motoneuron firing rate modulation. J Neurophysiol 69: 1005-1008, 1993.
24. Heckman CJ, Gorassini MA, Bennett DJ. Persistent inward currents in motoneuron dendrites: implications for motor output. Muscle Nerve 31: 135-156, 2005.
25. Heckman CJ, Johnson M, Mottram C, Schuster J. Persistent inward currents in spinal motoneurons and their influence on human motoneuron firing patterns. Neuroscientist 14: 264-275, 2008. (Pubitemid 351624860)
26. Hennig R, Lomo T. Firing patterns of motor units in normal rats. Nature 314: 164-166, 1985. (Pubitemid 15137124)
27. Hounsgaard J, Hultborn H, Jespersen B, Kiehn O. Bistability of alpha-motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5-hydroxytryptophan. J Physiol 405: 345-367, 1988.
28. Hounsgaard J, Kiehn O. Serotonin-induced bistability of turtle motoneurons caused by a nifedipine-sensitive calcium plateau potential. J Physiol 414: 265-282, 1989. (Pubitemid 19177302)
29. Kanosue K, Yoshida M, Akazawa K, Fujii K. The number of active motor units and their firing rates in voluntary contraction of human brachialis muscle. Jpn J Physiol 29: 427-443, 1979. (Pubitemid 10208910)
30. Kernell D. High-frequency repetitive firing of cat lumbosacral motoneurones stimulated by long-lasting injected currents. Acta Physiol Scand 65: 74-86, 1965a.
31. Kernell D. The limits of firing frequency in cat lumbosacral motoneurones possessing different time course of afterhyperpolarization. Acta Physiol Scand 65: 87-100, 1965b.
32. Kernell D. Input resistance, electrical excitability, and size of ventral horn cells in cat spinal cord. Science 152: 1637-1640, 1966.
33. Kernell D. Rhythmic properties of motoneurones innervating muscle fibers of different speed in m. gastrocnemius medialis of the cat. Brain Res 160: 159-162, 1979. (Pubitemid 9064110)
34. Kernell D. Repetitive impulse firing in motoneurons: facts and perspectives. Prog Brain Res 123: 31-37, 1999. (Pubitemid 30014544)
35. Kernell D. The Motoneurone and its Muscle Fibres Oxford, UK: Oxford Univ. Press, 2006.
36. Kernell D, Eerbeek O, Verhey BA. Relation between isometric force and stimulus rate in cat's hindlimb motor units of different twitch contraction time. Exp Brain Res 50: 220-227, 1983. (Pubitemid 14183342)
37. Kernell D, Monster AW. Time course and properties of late adaptation in spinal motoneurones of the cat. Exp Brain Res 46: 191-196, 1982. (Pubitemid 12092916)
38. Kernell D, Sjöholm H. Repetitive impulse firing: comparisons between neurone models based on "voltage clamp equations" and spinal motoneurones. Acta Physiol Scand 87: 40-56, 1973.
39. Lee RH, Heckman CJ. Bistability in spinal motoneurons in vivo: systematic variations in persistent inward currents. J Neurophysiol 80: 583-593, 1998a. (Pubitemid 28387643)
40. Lee RH, Heckman CJ. Bistability in spinal motoneurons in vivo: systematic variations in rhythmic firing patterns. J Neurophysiol 80: 572-582, 1998b. (Pubitemid 28387642)
41. Lee RH, Heckman CJ. Paradoxical effect of QX-314 on persistent inward currents and bistable behavior in spinal motoneurons in vivo. J Neurophysiol 82: 2518-2527, 1999.
42. Lee RH, Heckman CJ. Adjustable amplification of synaptic input in the dendrites of spinal motoneurons in vivo. J Neurosci 20: 6734-6740, 2000.
43. Lee RH, Kuo JJ, Jiang MC, Heckman CJ. Influence of active dendritic currents on input-output processing in spinal motoneurons in vivo. J Neurophysiol 89: 27-39, 2003.
44. Li X, Bennett DJ. Apamin-sensitive calcium-activated potassium currents (SK) are activated by persistent calcium currents in rat motoneurons. J Neurophysiol 97: 3314-3330, 2007. (Pubitemid 47084748)
45. Li X, Murray K, Harvey PJ, Ballou EW, Bennett DJ. Serotonin facilitates a persistent calcium current in motoneurons of rats with and without chronic spinal cord injury. J Neurophysiol 97: 1236-1246, 2007. (Pubitemid 46239501)
46. Li Y, Bennett DJ. Persistent sodium and calcium currents cause plateau potentials in motoneurons of chronic spinal rats. J Neurophysiol 90: 857-869, 2003. (Pubitemid 37092571)
47. Li Y, Gorassini MA, Bennett DJ. Role of persistent sodium and calcium currents in motoneuron firing and spasticity in chronic spinal rats. J Neurophysiol 91: 767-783, 2004. (Pubitemid 38168850)
48. MacKenzie ET, McCulloch J, O'Kean M, Pickard JD, Harper AM. Cerebral circulation and norepinephrine: relevance of the blood-brain barrier. Am J Physiol 231: 483-488, 1976.
49. Maltenfort MG, Hamm TM. Estimation of the electrical parameters of spinal motoneurons using impedance measurements. J Neurophysiol 92: 1433-1444, 2004.
50. Manuel M, Iglesias C, Donnet M, Leroy F, Heckman CJ, Zytnicki D. Fast kinetics, high-frequency oscillations, and subprimary firing range in adult mouse spinal motoneurons. J Neurosci 29: 11246-11256, 2009.
51. Manuel M, Meunier C, Donnet M, Zytnicki D. The afterhyperpolarization conductance exerts the same control over the gain and variability of motoneurone firing in anaesthetized cats. J Physiol 576: 873-886, 2006. (Pubitemid 44637890)
52. Manuel M, Meunier C, Donnet M, Zytnicki D. Resonant or not, two amplification modes of proprioceptive inputs by persistent inward currents in spinal motoneurons. J Neurosci 27: 12977-12988, 2007. (Pubitemid 350159590)
53. Matthews PB. Relationship of firing intervals of human motor units to the trajectory of post-spike after-hyperpolarization and synaptic noise. J Physiol 492: 597-628, 1996.
54. McDonagh JC, Hornby TG, Reinking RM, Stuart DG. Associations between the morphology and physiology of ventral-horn neurons in the adult turtle. J Comp Neurol 454: 177-191, 2002.
55. Meunier C, Borejsza K. How membrane properties shape the discharge of motoneurons: a detailed analytical study. Neural Comput 17: 2383-2420, 2005. (Pubitemid 41337040)
56. Monster AW, Chan H. Isometric force production by motor units of extensor digitorum communis muscle in man. J Neurophysiol 40: 1432-1443, 1977. (Pubitemid 8233151)
57. Moore J, Appenteng K. The membrane properties and firing characteristics of rat jaw-elevator motoneurones. J Physiol 423: 137-153, 1990. (Pubitemid 20137751)
58. Moritz AT, Newkirk G, Powers RK, Binder MD. Facilitation of somatic calcium channels can evoke prolonged tail currents in rat hypoglossal motoneurons. J Neurophysiol 98: 1042-1047, 2007. (Pubitemid 47236052)
59. Moritz CT, Barry BK, Pascoe MA, Enoka RM. Discharge rate variability influences the variation in force fluctuations across the working range of a hand muscle. J Neurophysiol 93: 2449-2459, 2005. (Pubitemid 40570830)
60. Mrówczynski W, Celichowski J, Krutki P. Interspecies differences in the force-frequency relationship of the medial gastrocnemius motor units. J Physiol Pharmacol 57: 491-502, 2006.
61. Nicolopoulos-Stournaras S, Iles JF. Motor neuron columns in the lumbar spinal cord of the rat. J Comp Neurol 217: 75-85, 1983.
62. Powers RK, Binder MD. Persistent sodium and calcium currents in rat hypoglossal motoneurons. J Neurophysiol 89: 615-624, 2003. (Pubitemid 36134048)
63. Rekling JC, Funk GD, Bayliss DA, Dong XW, Feldman JL. Synaptic control of motoneuronal excitability. Physiol Rev 80: 767-852, 2000.
64. Schwindt PC, Calvin WH. Membrane-potential trajectories between spikes underlying motoneuron firing rates. J Neurophysiol 35: 311-325, 1972.
65. Schwindt PC, Crill WE. Factors influencing motoneuron rhythmic firing: results from a voltage-clamp study. J Neurophysiol 48: 875-890, 1982. (Pubitemid 12037634)
66. Sekerli M, Del Negro CA, Lee RH, Butera RJ. Estimating action potential thresholds from neuronal time-series: new metrics and evaluation of methodologies. IEEE Trans Biomed Eng 51: 1665-1672, 2004. (Pubitemid 39100239)
67. Stafstrom CE, Schwindt PC, Crill WE. Repetitive firing in layer V neurons from cat neocortex in vitro. J Neurophysiol 52: 264-277, 1984. (Pubitemid 14058391)
68. Stein RB. The frequency of nerve action potentials generated by applied currents. Proc R Soc Lond B Biol Sci 167: 64-86, 1967.
69. Turkin VV, O'Neill D, Jung R, Hamm TM. Comparison of frequency - current relations and persistent inward currents in rat motoneurons measured in situ. Soc Neurosci Abstr 35: 860.12, 2009.
70. Viana F, Bayliss DA, Berger AJ. Multiple potassium conductances and their role in action potential repolarization and repetitive firing behavior of neonatal rat hypoglossal motoneurons. J Neurophysiol 69: 2150-2163, 1993. (Pubitemid 23195680)
71. Wienecke J, Zhang M, Hultborn H. A prolongation of the postspike afterhyperpolarization following spike trains can partly explain the lower firing rates at derecruitment than those at recruitment. J Neurophysiol 102: 3698-3710, 2009.
72. Wilson CJ, Weyrick A, Terman D, Hallworth NE, Bevan MD. A model of reverse spike frequency adaptation and repetitive firing of subthalamic nucleus neurons. J Neurophysiol 91: 1963-1980, 2004.
73. Zengel JE, Reid SA, Sypert GW, Munson JB. Membrane electrical properties and prediction of motor-unit type of medial gastrocnemius motoneurons in the cat. J Neurophysiol 53: 1323-1344, 1985.