Progressive changes in synaptic inputs to motoneurons in adult sacral spinal cord of a mouse model of amyotrophic lateral sclerosis

Journal of Neuroscience

Volumn 29, Issue 48, 2009, Pages 15031-15038

  Jiang, Mingchen ^a   Schuster, Jenna E ^a   Fu, Ronggen ^a   Siddique, Teepu ^a   Heckman, C J ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; GLUTAMATE RECEPTOR AGONIST; GLYCINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AGE; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIDROMIC STIMULATION; ARTICLE; CONTROLLED STUDY; DISEASE MODEL; DORSAL ROOT; ELECTROSTIMULATION; EVOKED RESPONSE; EXCITOTOXICITY; INTERNEURON; LATENT PERIOD; MOTONEURON; MOTOR ACTIVITY; MOUSE; MOUSE MUTANT; NERVE CELL; NERVE POTENTIAL; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; SACRUM; SPINAL CORD; SPINAL CORD NERVE CELL; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE; VENTRAL ROOT;

ACTION POTENTIALS; AGE FACTORS; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BIOPHYSICS; CHI-SQUARE DISTRIBUTION; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; HUMANS; INTERNEURONS; MICE; MICE, TRANSGENIC; MOTOR NEURONS; MUTATION; N-METHYLASPARTATE; PATCH-CLAMP TECHNIQUES; PSYCHOMOTOR PERFORMANCE; QUINOXALINES; REACTION TIME; REFLEX; SPINAL CORD; SUPEROXIDE DISMUTASE; SYNAPSES;

EID: 72849120555     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0574-09.2009     Document Type: Article

References (51)

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. Andries M, Van Damme P, Robberecht W, Van Den Bosch L (2007) Iver- mectin inhibits AMPA receptor-mediated excitotoxicity in cultured motor neurons and extends the life span of a transgenic mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 25:8-16. (Pubitemid 44765212)
4. Arundine M, Tymianski M (2003) Molecular mechanisms of calciumdependent neurodegeneration in excitotoxicity. Cell Calcium 34:325-337. (Pubitemid 37021228)
5. Bennett DJ, Gorassini M, Fouad K, Sanelli L, Han Y, Cheng J (1999) Spasticity in rats with sacral spinal cord injury. J Neurotrauma 16:69-84. (Pubitemid 29061897)
6. Berger ML, Veitl M, Malessa S, Sluga E, Hornykiewicz O (1992) Cholinergic markers in ALS spinal cord. J Neurol Sci 108:114-117.
7. Bonnot A, Morin D (1998) Hemisegmental localisation of rhythmic networks in the lumbosacral spinal cord of neonate mouse. Brain Res 793:136-148. (Pubitemid 28294082)
8. Bonnot A, Whelan PJ, Mentis GZ, O'Donovan MJ (2002) Locomotor-like activity generated by the neonatal mouse spinal cord. Brain Res Brain Res Rev 40:141-151. (Pubitemid 36183165)
9. 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.
10. Chang Q, Pereda A, Pinter MJ, Balice-Gordon RJ (2000) Nerve injury induces gap junctional coupling among axotomized adult motor neurons. J Neurosci 20:674-684. (Pubitemid 30225570)
11. Chiu AY, Zhai P, Dal Canto MC, Peters TM, Kwon YW, Prattis SM, Gurney ME (1995) Age-dependent penetrance of disease in a transgenic mouse model of familial amyotrophic lateral sclerosis.MolCell Neurosci 6:349-362.
12. Cleveland DW, Rothstein JD (2001) From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat Rev Neurosci 2:806-819.
13. Cowley KC, Schmidt BJ (1995) Effects of inhibitory amino acid antagonists on reciprocal inhibitory interactions during rhythmic motor activity in the in vitro neonatal rat spinal cord. J Neurophysiol 74:1109-1117.
14. Doyle MW, Andresen MC (2001) Reliability of monosynaptic sensory transmission in brain stem neurons in vitro. J Neurophysiol 85:2213-2223.
15. Durand J, Amendola J, Bories C, Lamotte d'Incamps B (2006) Early abnormalities in transgenic mouse models of amyotrophic lateral sclerosis. J Physiol Paris 99:211-220.
16. Geracitano R, Paolucci E, Prisco S, Guatteo E, Zona C, Longone P, Ammassari-Teule M, Bernardi G, Berretta N, Mercuri NB (2003) Altered long-term corticostriatal synaptic plasticity in transgenic mice overexpressing human CU/ZN superoxide dismutase (GLY933ALA) mutation. Neuroscience 118:399-408. (Pubitemid 36423255)
17. Gonzàlez-Forero D, Alvarez FJ (2005) Differential postnatal maturation of GABAA, glycine receptor, and mixed synaptic currents in Renshaw cells and ventral spinal interneurons. J Neurosci 25:2010-2023. (Pubitemid 40289406)
18. Hamson DK, Hu JH, Krieger C, Watson NV (2002) Lumbar motoneuron fate in a mouse model of amyotrophic lateral sclerosis. Neuroreport 13:2291-2294. (Pubitemid 36044445)
19. Hinckley C, Seebach B, Ziskind-Conhaim L (2005) Distinct roles of glycinergic and GABAergic inhibition in coordinating locomotor-like rhythms in the neonatal mouse spinal cord. Neuroscience 131:745-758. (Pubitemid 40261228)
20. Hochman S, Jordan LM, Schmidt BJ (1994) TTX-resistant NMDA receptormediated voltage oscillations in mammalian lumbar motoneurons. J Neurophysiol 72:2559-2562. (Pubitemid 24362650)
21. Jiang MC, Heckman CJ (2006) In vitro sacral cord preparation and motoneuron recording from adult mice. J Neurosci Methods 156:31-36.
22. Kiehn O (2006) Locomotor circuits in the mammalian spinal cord. Annu Rev Neurosci 29:279-306.
23. Kiehn O, Tresch MC (2002) Gap junctions and motor behavior. Trends Neurosci 25:108-115.
24. 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)
25. 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)
26. Lester RA, Jahr CE (1992) NMDA channel behavior depends on agonist affinity. J Neurosci 12:635-643.
27. Li Y, Li X, Harvey PJ, Bennett DJ (2004) Effects of baclofen on spinal reflexes and persistent inward currents in motoneurons of chronic spinal rats with spasticity. J Neurophysiol 92:2694-2703. (Pubitemid 40340482)
28. Machacek DW, Hochman S (2006) Noradrenaline unmasks novel selfreinforcing motor circuits within the mammalian spinal cord. J Neurosci 26:5920-5928.
29. Mayer ML, Vyklicky L Jr (1989) Concanavalin A selectively reduces desensitization of mammalian neuronal quisqualate receptors. Proc Natl Acad Sci U S A 86:1411-1415.
30. Moghaddasi M, Velumian AA, Zhang L, Fehlings MG (2007) An ex vivo preparation of mature mice spinal cord to study synaptic transmission on motoneurons. J Neurosci Methods 159:1-7. (Pubitemid 44792266)
31. 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)
32. Pasinelli P, Brown RH (2006) Molecular biology of amyotrophic lateral sclerosis: insights from genetics. Nat Rev Neurosci 7:710-723. (Pubitemid 44267495)
33. Powers RK, Binder MD (2001) Input-output functions of mammalian motoneurons. Rev Physiol Biochem Pharmacol 143:137-263.
34. Rao SD, Weiss JH (2004) Excitotoxic and oxidative cross-talk between motor neurons and glia in ALS pathogenesis. Trends Neurosci 27:17-23.
35. Rash JE, Staines WA, Yasumura T, Patel D, Furman CS, Stelmack GL, Nagy JI (2000) Immunogold evidence that neuronal gap junctions in adult rat brain and spinal cord contain connexin-36 but not connexin-32 or connexin-43. Proc Natl Acad Sci U S A 97:7573-7578. (Pubitemid 30431505)
36. Schmidt BJ, Hochman S, MacLean JN (1998) NMDA receptor-mediated oscillatory properties: potential role in rhythm generation in the mammalian spinal cord. Ann N Y Acad Sci 860:189-202. (Pubitemid 29045970)
37. Schütz B (2005) Imbalanced excitatory to inhibitory synaptic input precedes motor neuron degeneration in an animal model of amyotrophic lateral sclerosis. Neurobiol Dis 20:131-140.
38. Sornarajah L, Vasuta OC, Zhang L, Sutton C, Li B, El-Husseini A, Raymond LA (2008) NMDA receptor desensitization regulated by direct binding to PDZ1-2 domains of PSD-95. J Neurophysiol 99:3052-3062.
39. 93→ALA) mutation. Exp Neurol 197:505-514.
40. 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.
41. Tazerart S, Viemari JC, Darbon P, Vinay L, Brocard F (2007) Contribution of persistent sodium current to locomotor pattern generation in neonatal rats. J Neurophysiol 98:613-628. (Pubitemid 47236019)
42. Tresch MC, Kiehn O (2000) Motor coordination without action potentials in the mammalian spinal cord. Nat Neurosci 3:593-599.
43. Van Damme P, Leyssen M, Callewaert G, Robberecht W, Van Den Bosch L (2003) The AMPA receptor antagonist NBQX prolongs survival in a transgenic mouse model of amyotrophic lateral sclerosis. Neurosci Lett 343:81-84. (Pubitemid 36577521)
44. Van Den Bosch L, Van Damme P, Bogaert E, RobberechtW (2006) The role of excitotoxicity in the pathogenesis of amyotrophic lateral sclerosis. Biochim Biophys Acta 1762:1068-1082. (Pubitemid 44781176)
45. 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.
46. Vanselow BK, Keller BU (2000) Calcium dynamics and buffering in oculomotor neurones from mouse that are particularly resistant during amyotrophic lateral sclerosis (ALS)-related motoneurone disease. J Physiol 525:433-445.
47. von Lewinski F, Keller BU (2005) Mitochondrial Ca2+ buffering in hypoglossal motoneurons from mouse. Neurosci Lett 380:203-208.
48. Wang R, Zhang D (2005) Memantine prolongs survival in an amyotrophic lateral sclerosis mouse model. Eur J Neurosci 22:2376-2380. (Pubitemid 41653551)
49. Wilson JM, Cowan AI, Brownstone RM (2007) Heterogeneous electrotonic coupling and synchronization of rhythmic bursting activity in mouse Hb9 interneurons. J Neurophysiol 98:2370-2381.
50. Zhong G, Masino MA, Harris-Warrick RM (2007) Persistent sodium currents participate in fictive locomotion generation in neonatal mouse spinal cord. J Neurosci 27:4507-4518. (Pubitemid 46663577)
51. Ziskind-Conhaim L, Wu L, Wiesner EP (2008) Persistent sodium current contributes to induced voltage oscillations in locomotor-related hb9 interneurons in the mouse spinal cord. J Neurophysiol 100:2254-2264.