Glial nitric oxide-mediated long-term presynaptic facilitation revealed by optical imaging in rat spinal dorsal horn

Journal of Neuroscience

Volumn 24, Issue 44, 2004, Pages 9888-9896

  Ikeda, Hiroshi ^a   Murase, Kazuyuki ^a  

^a UNIVERSITY OF FUKUI   (Japan)

Author keywords

Glia; Hyperalgesia; Long term potentiation; LTP; Nitric oxide; Optical imaging; Spinal dorsal horn

Indexed keywords

DYE; METABOTROPIC RECEPTOR; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR ANTAGONIST; NITRIC OXIDE; NITRIC OXIDE DONOR; NITRIC OXIDE SYNTHASE INHIBITOR;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; CONDITIONING; CONTROLLED STUDY; DORSAL ROOT; ELECTRIC POTENTIAL; ELECTROSTIMULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; GLIA CELL; IMAGING; INFLAMMATION; LONG TERM POTENTIATION; METABOLISM; MUSCLE SPINDLE AFFERENT NERVE; NERVE INJURY; NERVE PROJECTION; NERVE STIMULATION; NOCICEPTIVE STIMULATION; NONHUMAN; OPTICS; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; SENSITIZATION; SPINAL CORD DORSAL HORN; STAINING; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; AFFERENT PATHWAYS; ANIMALS; ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; LONG-TERM POTENTIATION; NEUROGLIA; NITRIC OXIDE; POSTERIOR HORN CELLS; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE; STAINING AND LABELING;

EID: 7744224556     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2608-04.2004     Document Type: Article

References (53)

1. Arancio O, Kiebler M, Lee CJ, Lev-Ram V, Tsien RY, Kandel ER, Hawkins RD (1996) Nitric oxide acts directly in the presynaptic neuron to produce long-term potentiation in cultured hippocampal neurons. Cell 87:1025-1035.
2. Cattaert D, El Manira A (1999) Shunting versus inactivation: analysis of presynaptic inhibitory mechanisms in primary afferents of the crayfish. J Neurosci 19:6079-6089.
3. Cattaert D, Libersat F, El Manira A (2001) Presynaptic inhibition and antidromic spikes in primary afferents of the crayfish: a computational and experimental analysis. J Neurosci 21:1007-1021.
4. Dolan S, Nolan AM (2002) Behavioral evidence supporting a differential role for spinal group I and II metabotropic glutamate receptors in inflammatory hyperalgesia in sheep. Neuropharmacology 43:319-326.
5. Dolan S, Kelly JG, Monteiro AM, Nolan AM (2003) Up-regulation of metabotropic glutamate receptor subtypes 3 and 5 in spinal cord in a clinical model of persistent inflammation and hyperalgesia. Pain 106:501-512.
6. Doyle C, Holscher C, Rowan MJ, Anwyl R (1996) The selective neuronal NO synthase inhibitor 7-nitro-indazole blocks both long-term potentiation and depotentiation of field EPSPs in rat hippocampal CA1 in vivo. J Neurosci 16:418-424.
7. Hawkins RD, Son H, Arancio O (1998) Nitric oxide as a retrograde messenger during long-term potentiation in hippocampus. Prog Brain Res 118:155-172.
8. Hulsmann S, Oku Y, Zhang W, Richter DW (2000) Metabolic coupling between glia and neurons is necessary for maintaining respiratory activity in transverse medullary slices of neonatal mouse. Eur J Neurosci 12:856-862.
9. Ikeda H, Ryu PD, Park JB, Tanifuji M, Asai T, Murase K (1998) Optical responses evoked by single-pulse stimulation to the dorsal root in the rat spinal dorsal horn in slice. Brain Res 812:81-90.
10. Ikeda H, Asai T, Murase K (2000) Robust changes of afferent-induced excitation in the rat spinal dorsal horn after conditioning high-frequency stimulation. J Neurophysiol 83:2412-2420.
11. Ikeda H, Heinke B, Ruscheweyh R, Sandkühler J (2003) Synaptic plasticity in spinal lamina I projection neurons that mediate hyperalgesia. Science 299:1237-1240.
12. Isaac JT (2003) Postsynaptic silent synapses: evidence and mechanisms. Neuropharmacology 45:450-460.
13. Kantor DB, Lanzrein M, Stary SJ, Sandoval GM, Smith WB, Sullivan BM, Davidson N, Schuman EM (1996) A role for endothelial NO synthase in LTP revealed by adenovirus-mediated inhibition and rescue. Science 274:1744-1748.
14. Kim JH, Udo H, Li HL, Youn TY, Chen M, Kandel ER, Bailey CH (2003) Presynaptic activation of silent synapses and growth of new synapses contribute to intermediate and long-term facilitation in Aplysia. Neuron 40:151-165.
15. Klein T, Magerl W, Hopf HC, Sandkühler J, Treede RD (2004) Perceptual correlates of nociceptive long-term potentiation and long-term depression in humans. J Neurosci 24:964-971.
16. Lee CJ, Bardoni R, Tong CK, Engelman HS, Joseph DJ, Magherini PC, MacDermott AB (2002) Functional expression of AMPA receptors on central terminals of rat dorsal root ganglion neurons and presynaptic inhibition of glutamate release. Neuron 35:135-146.
17. Li P, Zhuo M (1998) Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 393:695-698.
18. Liao D, Hessler NA, Malinow R (1995) Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375:400-404.
19. Luscher C, Frerking M (2001) Restless AMPA receptors: implications for synaptic transmission and plasticity. Trends Neurosci 24:665-670.
20. MacDermott AB, Role LW, Siegelbaum SA (1999) Presynaptic ionotropic receptors and the control of transmitter release. Annu Rev Neurosci 22:443-485.
21. Maffei A, Prestori F, Shibuki K, Rossi P, Taglietti V, D'Angelo E (2003) NO enhances presynaptic currents during cerebellar mossy fiber-granule cell LTP. J Neurophysiol 90:2478-2483.
22. Maihofner C, Euchenhofer C, Tegeder I, Beck KF, Pfeilschifter J, Geisslinger G (2000) Regulation and immunohistochemical localization of nitric oxide synthases and soluble guanylyl cyclase in mouse spinal cord following nociceptive stimulation. Neurosci Lett 290:71-75.
23. Malenka RC, Nicoll RA (1999) Long-term potentiation - a decade of progress? Science 285:1870-1874.
24. Malinow R (2003) AMPA receptor trafficking and long-term potentiation. Philos Trans R Soc Lond B Biol Sci 358:707-714.
25. Meller ST, Dykstra C, Grzybycki D, Murphy S, Gebhart GF (1994) The possible role of glia in nociceptive processing and hyperalgesia in the spinal cord of the rat. Neuropharmacology 33:1471-1478.
26. Meyer RA, Campbell JN, Raja SN (1994) Peripheral neural mechanisms of nociception. In: Textbook of pain, Ed 3 (Wall PD, Melzack R, eds), pp 13-44. Edinburgh: Churchill Livingstone.
27. Mori K, Togashi H, Ueno KI, Matsumoto M, Yoshioka M (2001) Aminoguanidine prevented the impairment of learning behavior and hippocampal long-term potentiation following transient cerebral ischemia. Behav Brain Res 120:159-168.
28. Muir D, Berl S, Clarke DD (1986) Acetate and fluoroacetate as possible markers for glial metabolism in vivo. Brain Res 380:336-340.
29. Murase K, Saka T, Asai T, Ikeda H (1999) Functional circuitry for the induction of prolonged excitation in the rat spinal dorsal horn. Eur J Neurosci 11:3355-3358.
30. Park YK, Galik J, Ryu PD, Randić M (2004) Activation of presynaptic group I metabotropic glutamate receptors enhances glutamate release in the rat spinal cord substantia gelatinosa. Neurosci Lett 361:220-224.
31. Parnas I, Rashkovan G, Ravin R, Fischer Y (2000) Novel mechanism for presynaptic inhibition: GABA(A) receptors affect the release machinery. J Neurophysiol 84:1240-1246.
32. Randić M (1996) Plasticity of excitatory synaptic transmission in the spinal cord dorsal horn. Prog Brain Res 113:463-506.
33. Randić M, Jiang MC, Cerne R (1993) Long-term potentiation and long-term depression of primary afferent neurotransmission in the rat spinal cord. J Neurosci 13:5228-5241.
34. Ruscheweyh R, Ikeda H, Heinke B, Sandkuhler J (2004) Distinctive membrane and discharge properties of rat spinal lamina I projection neurones in vitro. J Physiol (Lond) 555:527-543.
35. Sandkühler J (1996) Neurobiology of spinal nociception: new concepts. Prog Brain Res 110:207-224.
36. Sandkühler J (2000) Learning and memory in pain pathways. Pain 88:113-118.
37. Sandkühler J, Ikeda H (2003) Two forms of synaptic long-term potentiation in ascending pain pathways. Soc Neurosci Abstr 33:13.1.
38. Sandkühler J, Liu X (1998) Induction of long-term potentiation at spinal synapses by noxious stimulation or nerve injury. Eur J Neurosci 10:2476-2480.
39. Son H, Hawkins RD, Martin K, Kiebler M, Huang PL, Fishman MC, Kandel ER (1996) Long-term potentiation is reduced in mice that are doubly mutant in endothelial and neuronal nitric oxide synthase. Cell 87:1015-1023.
40. Spike RC, Puskar Z, Andrew D, Todd AJ (2003) A quantitative and morphological study of projection neurons in lamina I of the rat lumbar spinal cord. Eur J Neurosci 18:2433-2448.
41. Swanson RA, Graham SH (1994) Fluorocitrate and fluoroacetate effects on astrocyte metabolism in vitro. Brain Res 664:94-100.
42. Tanifuji M, Sugiyama T, Murase K (1994) Horizontal propagation of excitation in rat visual cortical slices revealed by optical imaging. Science 266:1057-1059.
43. Tao F, Tao YX, Mao P, Zhao C, Li D, Liaw WJ, Raja SN, Johns RA (2003) Intact carrageenan-induced thermal hyperalgesia in mice lacking inducible nitric oxide synthase. Neuroscience 120:847-854.
44. Treede RD, Meyer RA, Raja SN, Campbell JN (1992) Peripheral and central mechanisms of cutaneous hyperalgesia. Prog Neurobiol 38:397-421.
45. Volgushev M, Balaban P, Chistiakova M, Eysel UT (2000) Retrograde signalling with nitric oxide at neocortical synapses. Eur J Neurosci 12:4255-4267.
46. Voronin LL, Cherubini E (2003) "Presynaptk silence" may be golden. Neuropharmacology 45:439-449.
47. Wall PD (1995) Do nerve impulses penetrate terminal arborizations? A pre-presynaptic control mechanism. Trends Neurosci 18:99-103.
48. Watkins LR, Milligan ED, Maier SF (2001) Spinal cord glia: new players in pain. Pain 93:201-205.
49. Wolpaw JR, Tennissen AM (2001) Activity-dependent spinal cord plasticity in health and disease. Annu Rev Neurosci 24:807-843.
50. Woolf CJ (1994) A new strategy for the treatment of inflammatory pain. Prevention or elimination of central sensitisation. Drugs 47:46-47.
51. Wu J, Fang L, Lin Q, Willis WD (2001) Nitric oxide synthase in spinal cord central sensitization following intradermal injection of capsaicin. Pain 94:47-58.
52. Zhong J, Gerber G, Kojic L, Randić M (2000) Dual modulation of excitatory synaptic transmission by agonists at group I metabotropic glutamate receptors in the rat spinal dorsal horn. Brain Res 887:359-377.
53. Ziegler EA, Magerl W, Meyer RA, Treede RD (1999) Secondary hyperalgesia to punctate mechanical stimuli. Central sensitization to A-fibre nociceptor input. Brain 122:2245-2257.