Fast kinetics, high-frequency oscillations, and subprimary firing range in adult mouse spinal motoneurons

Journal of Neuroscience

Volumn 29, Issue 36, 2009, Pages 11246-11256

  Manuel, Marin ^a,b   Iglesias, Caroline ^a   Donnet, Maud ^a   Leroy, Félix ^a   Heckman, C J ^b   Zytnicki, Daniel ^a  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; AFTERHYPERPOLARIZATION; ARTICLE; ELECTROPHYSIOLOGY; ELECTROSTIMULATION; FREQUENCY ANALYSIS; MOUSE; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; REPOLARIZATION; SPIKE; SPINAL CORD MOTONEURON;

ACTION POTENTIALS; AGE FACTORS; ANIMALS; BIOLOGICAL CLOCKS; CATS; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MOTOR NEURONS; RATS; SPECIES SPECIFICITY; SPINAL CORD; TIME FACTORS;

EID: 70349123549     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3260-09.2009     Document Type: Article

References (62)

1. Alonso A, Klink R (1993) Differential electroresponsiveness of stellate and pyramidal-like cells of medial entorhinal cortex layer II. J Neurophysiol 70:128-143. (Pubitemid 23220304)
2. Alstermark B, Ogawa J (2004) In vivo recordings of bulbospinal excitation in adult mouse forelimb motoneurons. J Neurophysiol 92:1958-1962.
3. Amendola J, Durand J (2008) Morphological differences between wild-type and transgenic superoxide dismutase 1 lumbar motoneurons in postnatal mice. J Comp Neurol 511:329-341.
4. Bakels R, Kernell D (1993) Matching between motoneurone and muscle unit properties in rat medial gastrocnemius. J Physiol 463:307-324. (Pubitemid 23120588)
5. Bateson DS, Parry DJ (1983) Motor units in a fast-twitch muscle of normal and dystrophic mice. J Physiol 345:515-523.
6. Beaumont E, Gardiner P (2002) Effects of daily spontaneous running on the electrophysiological properties of hindlimb motoneurones in rats. J Physiol 540:129-138. (Pubitemid 35174991)
7. Bories C, Amendola J, Lamotte d'Incamps B, Durand J (2007) Early electrophysiological abnormalities in lumbar motoneurons in a transgenic mouse model of amyotrophic lateral sclerosis. Eur J Neurosci 25:451-459.
8. Brizzi L, Meunier C, Zytnicki D, Donnet M, Hansel D, Lamotte d'Incamps B, Van Vreeswijk C (2004) How shunting inhibition affects the discharge of lumbar motoneurones: a dynamic clamp study in anaesthetized cats. J Physiol 558:671-683.
9. Burke RE (1967) Motor unit types of cat triceps surae muscle. J Physiol 193:141-160.
10. Burke RE, ten Bruggencate G (1971) Electrotonic characteristics of alpha motoneurones of varying size. J Physiol 212:120.
11. Burke RE, Strick PL, Kanda K, Kim CC, Walmsley B (1977) Anatomy of medial gastrocnemius and soleus motor nuclei in cat spinal cord. J Neurophysiol 40:667-680.
12. Button DC, Gardiner K, Marqueste T, Gardiner PF (2006) Frequency-current relationships of rat hindlimb alpha-motoneurones. J Physiol 573:663-677. (Pubitemid 43842509)
13. Chandler SH, Hsaio CF, Inoue T, Goldberg LJ (1994) Electrophysiological properties of guinea pig trigeminal motoneurons recorded in vitro. J Neurophysiol 71:129-145. (Pubitemid 24058846)
14. Chang Q, Gonzalez M, Pinter MJ, Balice-Gordon RJ (1999) Gap junctional coupling and patterns of connexin expression among neonatal rat lumbar spinal motor neurons. J Neurosci 19:10813-10828. (Pubitemid 30235727)
15. Cormery B, Beaumont E, Csukly K, Gardiner P (2005) Hindlimb unweighting for 2 weeks alters physiological properties of rat hindlimb motoneurones. J Physiol 568:841-850. (Pubitemid 41646025)
16. Engelhardt JK, Morales FR, Yamuy J, ChaseMH (1989) Cable properties of spinal cord motoneurons in adult and aged cats. J Neurophysiol 61:194-201.
17. Frugier T, Tiziano FD, Cifuentes-Diaz C, Miniou P, Roblot N, Dierich A, Le Meur M, Melki J (2000) Nuclear targeting defect of SMN lacking the C-terminus in a mouse model of spinal muscular atrophy. Hum Mol Genet 9:849-858. (Pubitemid 30162771)
18. Granit R, Kernell D, Shortess GK (1963) Quantitative aspects of repetitive firing of mammalian motoneurones, caused by injected currents. J Physiol 168:911-931.
19. Guertin PA, Hounsgaard J (1999) Non-volatile general anaesthetics reduce spinal activity by suppressing plateau potentials. Neuroscience 88:353-358.
20. Gurney ME, Pu H, Chiu AY, Dal Canto MC, Polchow CY, Alexander DD, Caliendo J, Hentati A, Kwon YW, Deng HX, Chen W, Zhai P, Sufit RL, Siddique T (1994) Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 264:1772-1775. (Pubitemid 24227760)
21. Gustafsson B, Pinter MJ (1984) Relations among passive electrical properties of lumbar alpha-motoneurones of the cat. J Physiol 356:401-431. (Pubitemid 14011556)
22. Gutfreund Y, Yarom Y, Segev I (1995) Subthreshold oscillations and resonant frequency in guinea-pig cortical neurons: physiology and modelling. J Physiol 483:621-640.
23. Hashizume K, Kanda K, Burke RE (1988) Medial gastrocnemius motor nucleus in the rat: age-related changes in the number and size of motoneurons. J Comp Neurol 269:425-430. (Pubitemid 18090008)
24. Holmes WR, Rall W (1992) Electrotonic length estimates in neurons with dendritic tapering or somatic shunt. J Neurophysiol 68:1421-1437.
25. Horcholle-Bossavit G, Jami L, Thiesson D, Zytnicki D (1988) Motor nuclei of peroneal muscles in the cat spinal cord. J Comp Neurol 277:430-440. (Pubitemid 18268918)
26. Hounsgaard J, Hultborn H, Jespersen B, Kiehn O (1988) Bistability of alpha-motoneurones in the decerebrate cat and in the acute spinal cat after intravenous 5-hydroxytryptophan. J Physiol 405:345-367. (Pubitemid 18250343)
27. Hsieh-Li HM, Chang JG, Jong YJ, Wu MH, Wang NM, Tsai CH, LiH (2000) A mouse model for spinal muscular atrophy. Nat Genet 24:66-70. (Pubitemid 30041423)
28. Huizar P, Kuno M, Miyata Y (1975) Electrophysiological properties of spinal motoneurones of normal and dystrophic mice. J Physiol 248:231-246.
29. Hutcheon B, Yarom Y (2000) Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci 23:216-222. (Pubitemid 30236181)
30. Ishihara A, Ohira Y, Tanaka M, Nishikawa W, Ishioka N, Higashibata A, Izumi R, Shimazu T, Ibata Y (2001) Cell body size and succinate dehydrogenase activity of spinal motoneurons innervating the soleus muscle in mice, rats, and cats. Neurochem Res 26:1301-1304. (Pubitemid 34184029)
31. Kernell D (1965) The limits of firing frequency in cat lumbosacral motoneurones possessing different time course of afterhyperpolarization. Acta Physiol Scand 56:87-100.
32. Kernell D (2006) The motoneurone and its muscle fibers. Oxford: Oxford UP.
33. Kiehn O, Kjaerulff O, Tresch MC, Harris-Warrick RM (2000) Contributions of intrinsic motor neuron properties to the production of rhythmic motor output in the mammalian spinal cord. Brain Res Bull 53:649-659.
34. Krnjevic K, Puil E, Werman R (1978) EGTA and motoneuronal afterpotentials. J Physiol 275:199-223.
35. Kudina LP (1999) Analysis of firing behaviour of human motoneurones within "subprimary range." J Physiol Paris 93:115-123.
36. Kuo JJ, Siddique T, Fu R, Heckman CJ (2005) Increased persistent Na(+) current and its effect on excitability in motoneurones cultured from mutant SOD1 mice. J Physiol 563:843-854. (Pubitemid 40425599)
37. Lee RH, Heckman CJ (2000) Adjustable amplification of synaptic input in the dendrites of spinal motoneurons in vivo. J Neurosci 20:6734-6740.
38. Lewis DM, Parry DJ, Rowlerson A (1982) Isometric contractions of motor units and immunohistochemistry of mouse soleus muscle. J Physiol 325:393-401.
39. Llinas RR, Grace AA, Yarom Y (1991) In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10-to 50-Hz frequency range. Proc Natl Acad Sci U S A 88:897-901.
40. Logan SD, Pickering AE, Gibson IC, Nolan MF, Spanswick D (1996) Electrotonic coupling between rat sympathetic preganglionic neurones in vitro. J Physiol 495:491-502. (Pubitemid 26331829)
41. Manuel M, Meunier C, Donnet M, Zytnicki D (2005) How much afterhyperpolarization conductance is recruited by an action potential? A dynamic-clamp study in cat lumbar motoneurons. J Neurosci 25:8917-8923. (Pubitemid 41384460)
42. Manuel M, Meunier C, Donnet M, Zytnicki D (2006) The afterhyperpolarization conductance exerts the same control over the gain and variability of motoneurone firing in anaesthetized cats. J Physiol 576:873-886. (Pubitemid 44637890)
43. Manuel M, Meunier C, Donnet M, Zytnicki D (2007) Resonant or not, two amplification modes of proprioceptive inputs by persistent inward currents in spinal motoneurons. J Neurosci 27:12977-12988. (Pubitemid 350159590)
44. Matthews PB (1999) Properties of human motoneurones and their synaptic noise deduced from motor unit recordings with the aid of computer modelling. J Physiol Paris 93:135-145.
45. McHanwell S, Biscoe TJ (1981) The sizes of motoneurons supplying hindlimb muscles in the mouse. Proc R Soc Lond B Biol Sci 213:201-216. (Pubitemid 12199650)
46. McLarnon JG (1995) Potassium currents in motoneurones. Prog Neurobiol 47:513-531.
47. Meehan CF, Sukiasyan N, Chakrabarty S, Hulton H, Nielsen JB (2008) Intracellular recording from identified lumbar motoneurones of the adult mouse recorded in vivo. Soc Neurosci Abstr 34:758/MM31.
48. Meunier C, Borejsza K (2005) How membrane properties shape the discharge of motoneurons: a detailed analytical study. Neural Comput 17:2383-2420. (Pubitemid 41337040)
49. Monani UR, Sendtner M, Coovert DD, Parsons DW, Andreassi C, Le TT, Jablonka S, Schrank B, Rossoll W, Prior TW, Morris GE, Burghes AH (2000) The human centromeric survival motor neuron gene (SMN2) rescues embryonic lethality in Smn(-/-) mice and results in a mouse with spinal muscular atrophy. Hum Mol Genet 9:333-339. (Pubitemid 30098725)
50. Pape HC (1996) Queer current and pacemaker: the hyperpolarization- activated cation current in neurons. Annu Rev Physiol 58:299-327. (Pubitemid 26106723)
51. Placantonakis DG, Bukovsky AA, Aicher SA, Kiem HP, Welsh JP (2006) Continuous electrical oscillations emerge from a coupled network: a study of the inferior olive using lentiviral knockdown of connexin36. J Neurosci 26:5008-5016.
52. Powers RK, Binder MD (2001) Input-output functions of mammalian motoneurons. Rev Physiol Biochem Pharmacol 143:137-263.
53. Rall W (1969) Time constants and electrotonic length of membrane cylinders and neurons. Biophys J 9:1483-1508.
54. Rall W, Burke RE, Holmes WR, Jack JJ, Redman SJ, Segev I (1992) Matching dendritic neuron models to experimental data. Physiol Rev 72:S159-S186.
55. Roy RR, Matsumoto A, Zhong H, Ishihara A, Edgerton VR (2007) Rat alpha-and gamma-motoneuron soma size and succinate dehydrogenase activity are independent of neuromuscular activity level. Muscle Nerve 36:234-241. (Pubitemid 47221861)
56. Safronov BV, Vogel W (1995) Single voltage-activated Na+ and K+ channels in the somata of rat motoneurones. J Physiol 487:91-106.
57. Swett JE, Wikholm RP, Blanks RH, Swett AL, Conley LC (1986) Motoneurons of the rat sciatic nerve. Exp Neurol 93:227-252.
58. Ulfhake B, Kellerth JO (1984) Electrophysiological and morphological measurements in cat gastrocnemius and soleus alpha-motoneurones. Brain Res 307:167-179. (Pubitemid 14094574)
59. van Zundert B, Peuscher MH, Hynynen M, Chen A, Neve RL, Brown RH, Jr., Constantine-Paton M, Bellingham MC (2008) Neonatal neuronal circuitry shows hyperexcitable disturbance in a mouse model of the adultonset neurodegenerative disease amyotrophic lateral sclerosis. J Neurosci 28:10864-10874.
60. Walton KD, Navarrete R (1991) Postnatal changes in motoneurone electrotonic coupling studied in the in vitro rat lumbar spinal cord. J Physiol 433:283-305.
61. Zengel JE, Reid SA, Sypert GW, Munson JB (1985) Membrane electrical properties and prediction of motor-unit type of medial gastrocnemius motoneurons in the cat. J Neurophysiol 53:1323-1344.
62. Zhang L, Krnjevic K (1987) Apamin depresses selectively the afterhyperpolarization of cat spinal motoneurons. Neurosci Lett 74:58-62. (Pubitemid 17229026)