Evidence from computer simulations for alterations in the membrane biophysical properties and dendritic processing of synaptic inputs in mutant superoxide dismutase-1 motoneurons

Journal of Neuroscience

Volumn 30, Issue 16, 2010, Pages 5544-5558

  ElBasiouny, Sherif M ^a   Amendola, Julien ^b   Durand, Jacques ^b   Heckman, C J ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; ION CHANNEL;

ANIMAL EXPERIMENT; ARTICLE; BIOPHYSICS; CELL STRUCTURE; COMPUTER SIMULATION; DENDRITIC CELL; ELECTROPHYSIOLOGY; MEMBRANE BIOLOGY; MEMBRANE RESISTANCE; MOTONEURON; MOUSE; MUTANT; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD MOTONEURON; SYNAPTIC POTENTIAL; TRANSGENIC MOUSE;

ANIMALS; CELL MEMBRANE; COMPUTER SIMULATION; DENDRITES; EXCITATORY POSTSYNAPTIC POTENTIALS; MICE; MICE, TRANSGENIC; MOTOR NEURONS; MUTATION; NEURAL INHIBITION; SUPEROXIDE DISMUTASE; SYNAPSES;

EID: 77951615746     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0434-10.2010     Document Type: Article

References (60)

1. 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.
2. Amendola J, Verrier B, Roubertoux P, Durand J (2004) Altered sensorimotor development in a transgenic mouse model of amyotrophic lateral sclerosis. Eur J Neurosci 20:2822-2826. (Pubitemid 39573798)
3. Berger AJ, Bayliss DA, Viana F (1992) Modulation of neonatal rat hypoglossal motoneuron excitability by serotonin. Neurosci Lett 143:164-168.
4. 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 25:45-459.
5. Bruijn LI, Becher MW, Lee MK, Anderson KL, Jenkins NA, Copeland NG, Sisodia SS, Rothstein JD, Borchelt DR, Price DL, Cleveland DW (1997) ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron 18:327-338.
6. Bruijn LI, Houseweart MK, Kato S, Anderson KL, Anderson SD, Ohama E, Reaume AG, Scott RW, Cleveland DW (1998) Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1. Science 281:1851-1854. (Pubitemid 28450505)
7. Carlin KP, Jiang Z, Brownstone RM (2000a) Characterization of calcium currents in functionally mature mouse spinal motoneurons. Eur J Neurosci 12:1624-1634. (Pubitemid 30258871)
8. Carlin KP, Jones KE, Jiang Z, Jordan LM, Brownstone RM (2000b) Dendritic L-type calcium currents in mouse spinal motoneurons: implications for bistability. Eur J Neurosci 12:1635-1646. (Pubitemid 30258872)
9. Carlin KP, Bui TV, Dai Y, Brownstone RM (2009) Staircase currents in motoneurons: insight into the spatial arrangement of calcium channels in the dendritic tree. J Neurosci 29:5343-5353.
10. Clements JD, Redman SJ (1989) Cable properties of cat spinal motoneurones measured by combining voltage clamp, current clamp and intracellular staining. J Physiol 409:63-87.
11. Cushing S, Bui T, Rose PK (2005) Effect of nonlinear summation of synaptic currents on the input-output properties of spinal motoneurons. J Neurophysiol 94:3465-3478. (Pubitemid 41504782)
12. Deforges S, Branchu J, Biondi O, Grondard C, Pariset C, Lécolle S, Lopes P, Vidal PP, Chanoine C, Charbonnier F (2009) Motoneuron survival is promoted by specific exercise in a mouse model of amyotrophic lateral sclerosis. J Physiol 587:3561-3572.
13. ElBasiouny SM, Heckman CJ (2008) Upregulation of active conductances and persistent inward currents in mutant SOD1 motoneurons: insights from computer simulations. In 2008 Abstract Viewer/Itinerary Planner, Washington, DC: Society for Neuroscience, Online Program number: 445.19.
14. ElBasiouny SM, Bennett DJ, Mushahwar VK (2005) Simulation of dendritic Cav1.3 channels in cat lumbar motoneurons: spatial distribution. J Neurophysiol 94:3961-3974.
15. Elliott P, Wallis DI (1992) Serotonin and l-norepinephrine as mediators of altered excitability in neonatal rat motoneurons studied in vitro. Neuroscience 47:533-544.
16. Fedirchuk B, Dai Y (2004) Monoamines increase the excitability of spinal neurones in the neonatal rat by hyperpolarizing the threshold for action potential production. J Physiol 557:355-361. (Pubitemid 38807382)
17. Filipchuk AA, Durand J, Korogod SM (2009) Structural transformations caused by the superoxide dismutase 1 mutation in the mouse model of the human familial amyotrophic lateral sclerosis: developmental and electrotonic aspects. In 2009 Abstract Viewer/Itinerary Planner, Washington, DC: Society for Neuroscience, Online Program number: 146.20.
18. Fleshman JW, Segev I, Burke RB (1988) Electrotonic architecture of type-identified alpha-motoneurons in the cat spinal cord. J Neurophysiol 60:60-85.
19. Frey D, Schneider C, Xu L, Borg J, Spooren W, Caroni P (2000) Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J Neurosci 20:2534-2542. (Pubitemid 30220340)
20. Gordon T, Tyreman N, Li S, Putman CT, Hegedus J (2010) Functional overload saves motor units in the SOD1-G93A transgenic mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 37:412-422.
21. Harvey PJ, Li Y, Li X, Bennett DJ (2006) Persistent sodium currents and repetitive firing in motoneurons of the sacrocaudal spinal cord of adult rats. J Neurophysiol 96:1141-1157. (Pubitemid 44371510)
22. Hegedus J, Putman CT, Gordon T (2007) Time course of preferential motor unit loss in the SOD1G93A mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 28:154-164. (Pubitemid 47615455)
23. Hegedus J, Putman CT, Tyreman N, Gordon T (2008) Preferential motor unit loss in the SOD1 G93A transgenic mouse model of amyotrophic lateral sclerosis. J Physiol 586:3337-3351. (Pubitemid 352003870)
24. Hines ML, Carnevale NT (1997) The NEURON simulation environment. Neural Comput 9:1179-1209.
25. Hochman S, McCrea DA (1994) Effects of chronic spinalization on ankle extensor motoneurons. II. Motoneuron electrical properties. J Neurophysiol 71:1468-1479. (Pubitemid 24121843)
26. Holmes WR, RallW (1992a) Electrotonic length estimates in neurons with dendritic tapering or somatic shunt. J Neurophysiol 68:1421-1437.
27. Holmes WR, Rall W (1992b) Estimating the electrotonic structure of neurons with compartmental models. J Neurophysiol 68:1438-1452.
28. Holmes WR, Segev I, Rall W (1992) Interpretation of time constant and electrotonic length estimates in multicylinder or branched neuronal structures. J Neurophysiol 68:1401-1420.
29. 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.
30. Hsiao CF, Del Negro CA, Trueblood PR, Chandler SH (1998) Ionic basis for serotonin-induced bistable membrane properties in guinea pig trigeminal motoneurons. J Neurophysiol 79:2847-2856.
31. Jiang Z, Rempel J, Li J, Sawchuk MA, Carlin KP, Brownstone RM (1999) Development of L-type calcium channels and a nifedipine-sensitive motor activity in the postnatal mouse spinal cord. Eur J Neurosci 11:3481-3487. (Pubitemid 29484245)
32. Kieran D, Hafezparast M, Bohnert S, Dick JR, Martin J, Schiavo G, Fisher EM, Greensmith L (2005) A mutation in dynein rescues axonal transport defects and extends the life span of ALS mice. J Cell Biol 169:561-567. (Pubitemid 41002849)
33. Kitzman P (2005) Alteration in axial motoneuronal morphology in the spinal cord injured spastic rat. Exp Neurol 192:100-108.
34. Kuo JJ, Schonewille M, Siddique T, Schults AN, Fu R, Bär PR, Anelli R, Heckman CJ, Kroese AB (2004) Hyperexcitability of cultured spinal motoneurons from presymptomatic ALS mice. J Neurophysiol 91:571-575. (Pubitemid 38084396)
35. 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)
36. Larkman PM, Kelly JS (1992) Ionic mechanisms mediating 5-hydroxytryptamine- and noradrenaline-evoked depolarization of adult rat facial motoneurones. J Physiol 456:473-490.
37. Lee RH, Heckman CJ (1999) Enhancement of bistability in spinal motoneurons in vivo by the noradrenergic alpha 1 agonist methoxamine. J Neurophysiol 81:2164-2174.
38. Lee RH, Heckman CJ (2000) Adjustable amplification of synaptic input in the dendrites of spinal motoneurons in vivo. J Neurosci 20:6734-6740.
39. Lev-Tov A, Miller JP, Burke RE, Rall W (1983) Factors that control amplitude of EPSPs in dendritic neurons. J Neurophysiol 50:399-412. (Pubitemid 13038386)
40. Li Y, Bennett DJ (2003) Persistent sodium and calcium currents cause plateau potentials in motoneurons of chronic spinal rats. J Neurophysiol 90:857-869. (Pubitemid 37092571)
41. 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)
42. Morrison BM, Janssen WG, Gordon JW, Morrison JH (1998) Time course of neuropathology in the spinal cord of G86R superoxide dismutase transgenic mice. J Comp Neurol 391:64-77.
43. Nagao M, Misawa H, Kato S, Hirai S (1998) Loss of cholinergic synapses on the spinal motor neurons of amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 57:329-333. (Pubitemid 28182630)
44. Pambo-Pambo A, Durand J, Gueritaud JP (2009) Early excitability changes in lumbar motoneurons of transgenic SOD1G85R and SOD1G93A-Low mice. J Neurophysiol 102:3627-3642.
45. Powers RK, Binder MD (2000) Summation of effective synaptic currents and firing rate modulation in cat spinal motoneurons. J Neurophysiol 83:483-500.
46. Prather JF, Powers RK, Cope TC (2001) Amplification and linear summation of synaptic effects on motoneuron firing rate. J Neurophysiol 85:43-53.
47. Pun S, Santos AF, Saxena S, Xu L, Caroni P (2006) Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nat Neurosci 9:408-419. (Pubitemid 43290971)
48. Rall W (1967) Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. J Neurophysiol 30:1138-1168.
49. Rall W (1969) Time constants and electrotonic length of membrane cylinders and neurons. Biophys J 9:1483-1508.
50. 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.
51. Raoul C, Estévez AG, Nishimune H, Cleveland DW, deLapeyrièreO, Henderson CE, Haase G, Pettmann B (2002) Motoneuron death triggered by a specific pathway downstream of Fas: potentiation by ALS-linked SOD1 mutations. Neuron 35:1067-1083. (Pubitemid 35279535)
52. Rose PK, Cushing S (1999) 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.
53. Rose PK, Vanner SJ (1988) 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.
54. Saxena S, Cabuy E, Caroni P (2009) A role for motoneuron subtypeselective ER stress in disease manifestations of FALS mice. Nat Neurosci 12:627-636.
55. Segev I, Fleshman JW Jr, Burke RE (1990) Computer simulation of group Ia EPSPs using morphologically realistic models of cat alpha-motoneurons. J Neurophysiol 64:648-660. (Pubitemid 20264069)
56. Shelton DP (1985) Membrane resistivity estimated for the Purkinje neuron by means of a passive computer model. Neuroscience 14:111-131.
57. Stephens B, Guiloff RJ, Navarrete R, Newman P, Nikhar N, Lewis P (2006) Widespread loss of neuronal populations in the spinal ventral horn in sporadic motor neuron disease. A morphometric study. J Neurol Sci 244:41-58.
58. Takahashi T (1990) Inward rectification in neonatal rat spinal motoneurones. J Physiol 423:47-62. (Pubitemid 20137683)
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. Williamson TL, Cleveland DW (1999) Slowing of axonal transport is a very early event in the toxicity of ALS-linked SOD1 mutants to motor neurons. Nat Neurosci 2:50-56.