Astrocytes are involved in long-term facilitation of neuronal excitation in the anterior cingulate cortex of mice with inflammatory pain

Pain

Volumn 154, Issue 12, 2013, Pages 2836-2843

  Ikeda, Hiroshi ^a   Mochizuki, Keiichi ^a   Murase, Kazuyuki ^a  

^a UNIVERSITY OF FUKUI   (Japan)

Author keywords

Emotion; Glia; Hyperalgesia; Long term potentiation (LTP); Optical imaging

Indexed keywords

AMINOADIPIC ACID; FREUND ADJUVANT; L ALPHA AMINOADIPIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR CINGULATE; ANXIETY; ARTICLE; ASTROCYTE; FEMALE; IMMUNOREACTIVITY; INFLAMMATORY PAIN; MALE; MOUSE; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL;

EMOTION; GLIA; HYPERALGESIA; LONG-TERM POTENTIATION (LTP); OPTICAL IMAGING;

ANIMALS; ASTROCYTES; FEMALE; GYRUS CINGULI; INFLAMMATION; MALE; MICE; MICE, INBRED ICR; NEURONAL PLASTICITY; NEURONS; PAIN; TIME FACTORS;

EID: 84889080505     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2013.08.023     Document Type: Article

References (45)

1. B. Bie, D.L. Brown, and M. Naguib Increased synaptic GluR1 subunits in the anterior cingulate cortex of rats with peripheral inflammation Eur J Pharmacol 653 2011 26 31
2. T.V. Bliss, and G.L. Collingridge A synaptic model of memory: long-term potentiation in the hippocampus Nature 361 1993 31 39
3. K.L. Casey Forebrain mechanisms of nociception and pain: analysis through imaging Proc Natl Acad Sci U S A 96 1999 7668 7674
4. F.L. Chen, Y.L. Dong, Z.J. Zhang, D.L. Cao, J. Xu, J. Hui, L. Zhu, and Y.J. Gao Activation of astrocytes in the anterior cingulate cortex contributes to the affective component of pain in an inflammatory pain model Brain Res Bull 87 2012 60 66
5. S.J. Cheng, C.C. Chen, H.W. Yang, Y.T. Chang, S.W. Bai, C.C. Chen, C.T. Yen, and M.Y. Min Role of extracellular signal-regulated kinase in synaptic transmission and plasticity of a nociceptive input on capsular central amygdaloid neurons in normal and acid-induced muscle pain mice J Neurosci 31 2011 2258 2270
6. Y.J. Gao, W.H. Ren, Y.Q. Zhang, and Z.Q. Zhao Contributions of the anterior cingulate cortex and amygdala to pain- and fear-conditioned place avoidance in rats PAIN® 110 2004 343 353
7. Y.J. Gao, and R.R. Ji Targeting astrocyte signaling for chronic pain Neurotherapeutics 7 2010 482 493
8. R.D. Grinvald, E. Frosting, R. Lieke, and R. Hildesheim Optical imaging of neuronal activity Physiol Rev 68 1988 1285 1365
9. W. Guo, H. Wang, M. Watanabe, K. Shimizu, S. Zou, S.C. LaGraize, F. Wei, R. Dubner, and K. Ren Glial-cytokine-neuronal interactions underlying the mechanisms of persistent pain J Neurosci 27 2007 6006 6018
10. C. Henneberger, T. Papouin, S.H. Oliet, and D.A. Rusakov Long-term potentiation depends on release of d-serine from astrocytes Nature 463 2010 232 236
11. S. Huck, F. Grass, and H. Hörtnagl The glutamate analogue alpha-aminoadipic acid is taken up by astrocytes before exerting its gliotoxic effect in vitro J Neurosci 4 1984 2650 2657
12. S.E. Hyman, R.C. Malenka, and E.J. Nestler Neural mechanisms of addiction: the role of reward-related learning and memory Annu Rev Neurosci 29 2006 565 598
13. H. Ikeda, P.D. Ryu, J.B. Park, M. Tanifuji, T. Asai, and K. Murase Optical responses evoked by single-pulse stimulation to the dorsal root in the rat spinal dorsal horn in slice Brain Res 812 1998 81 90
14. H. Ikeda, and K. Murase Glial nitric oxide-mediated long-term presynaptic facilitation revealed by optical imaging in rat spinal dorsal horn J Neurosci 24 2004 9888 9896
15. H. Ikeda, J. Stark, H. Fischer, M. Wagner, R. Drdla, T. Jäger, and J. Sandkühler Synaptic amplifier of inflammatory pain in the spinal dorsal horn Science 312 2006 1659 1662
16. R.R. Ji, T. Kohno, K.A. Moore, and C.J. Woolf Central sensitization and LTP: do pain and memory share similar mechanisms? Trends Neurosci 26 2003 696 705
17. J.P. Johansen, H.L. Fields, and B.H. Manning The affective component of pain in rodents: direct evidence for a contribution of the anterior cingulate cortex Proc Natl Acad Sci U S A 98 2001 8077 8082
18. E.R. Kandel The molecular biology of memory storage: a dialogue between genes and synapses Science 294 2001 1030 1038
19. S.S. Kim, H. Wang, X.Y. Li, T. Chen, V. Mercaldo, G. Descalzi, L.J. Wu, and M. Zhuo Neurabin in the anterior cingulate cortex regulates anxiety-like behavior in adult mice Mol Brain 4 2011 6
20. T. Kiritoshi, H. Ikeda, and K. Murase Long-term potentiation of neuronal excitation in the central nucleus of the rat amygdala revealed by imaging with a voltage-sensitive dye Brain Res 1349 2010 32 40
21. V.K. Kontinen, T. Kauppila, S. Paananen, A. Pertovaara, and E. Kalso Behavioural measures of depression and anxiety in rats with spinal nerve ligation-induced neuropathy PAIN® 80 1999 341 346
22. L.G. Lei, Y.Q. Zhang, and Z.Q. Zhao Pain-related aversion and Fos expression in the central nervous system in rats Neuroreport 15 2004 67 71
23. Y. Lu, L. Zhu, and Y.J. Gao Pain-related aversion induces astrocytic reaction and proinflammatory cytokine expression in the anterior cingulate cortex in rats Brain Res Bull 84 2011 178 182
24. M.A. McCall, R.G. Gregg, R.R. Behringer, M. Brenner, C.L. Delaney, E.J. Galbreath, C.L. Zhang, R.A. Pearce, S.Y. Chiu, and A. Messing Targeted deletion in astrocyte intermediate filament (Gfap) alters neuronal physiology Proc Natl Acad Sci U S A 93 1996 6361 6366
25. R.F. Miller d-Serine as a glial modulator of nerve cell Glia 47 2004 275 283
26. E.D. Milligan, C. Twining, M. Chacur, J. Biedenkapp, K. O'Connor, S. Poole, K. Tracey, D. Martin, S.F. Maier, and L.R. Watkins Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain in rats J Neurosci 23 2003 1026 1040
27. V. Neugebauer, V. Galhardo, S. Maione, and S.C. Mackey Forebrain pain mechanisms Brain Res Rev 60 2009 226 242
28. T. Otto, H. Eichenbaum, S.I. Wiener, and C.G. Wible Learning-related patterns of CA1 spike trains parallel stimulation parametersoptimal for inducing hippocampal long-term potentiation Hippocampus 1 1991 181 192
29. A. Panatier, D.T. Theodosis, J.P. Mothet, B. Touquet, L. Pollegioni, D.A. Poulain, and S.H. Oliet Glia-derived d-serine controls NMDA receptor activity and synaptic memory Cell 125 2006 775 784
30. L.N. Pastoriza, T.J. Morrow, and K.L. Casey Medial frontal cortex lesions selectively attenuate the hot plate response: possible nocifensive apraxia in the rat PAIN® 64 1996 11 17
31. D.D. Price Psychological and neural mechanisms of the affective dimension of pain Science 288 2000 1769 1772
32. P. Rainville, G.H. Duncan, D.D. Price, B. Carrier, and M.C. Bushnell Pain affect encoded in human anterior cingulate but not somatosensory cortex Science 277 1997 968 971
33. V. Raghavendra, F.Y. Tanga, and J.A. DeLeo Complete Freund adjuvant-induced peripheral inflammation evokes glial activation and proinflammatory cytokine expression in the CNS Eur J Neurosci 20 2004 467 473
34. K. Ren, and R. Dubner Neuron-glia crosstalk gets serious: role in pain hypersensitivity Curr Opin Anaesthesiol 21 2008 570 579
35. M. Schäfers, C.I. Svensson, C. Sommer, and L.S. Sorkin Tumor necrosis factor-alpha induces mechanical allodynia after spinal nerve ligation by activation of p38 MAPK in primary sensory neurons J Neurosci 23 2003 2517 2521
36. H. Toyoda, M.G. Zhao, and M. Zhuo Enhanced quantal release of excitatory transmitter in anterior cingulate cortex of adult mice with chronic pain Mol Pain 5 2009 4
37. H. Toyoda, M.G. Zhao, B. Ulzhöfer, L.J. Wu, H. Xu, P.H. Seeburg, R. Sprengel, R. Kuner, and M. Zhuo Roles of the AMPA receptor subunit GluA1 but not GluA2 in synaptic potentiation and activation of ERK in the anterior cingulate cortex Mol Pain 5 2009 46
38. I. Tracey, and P.W. Mantyh The cerebral signature for pain perception and its modulation Neuron 55 2007 377 391
39. K.S. Vikman, A.W. Duggan, and P.J. Siddall Increased ability to induce long-term potentiation of spinal dorsal horn neurons in monoarthritic rats Brain Res 990 2003 51 57
40. F. Wei, and M. Zhuo Potentiation of sensory responses in the anterior cingulate cortex following digit amputation in the anaesthetised rat J Physiol 532 2001 823 833
41. F. Wei, W. Guo, S. Zou, K. Ren, and R. Dubner Supraspinal glial-neuronal interactions contribute to descending pain facilitation J Neurosci 28 2008 10482 10495
42. L.J. Wu, H. Toyoda, M.G. Zhao, Y.S. Lee, J. Tang, S.W. Ko, Y.H. Jia, F.W. Shum, C.V. Zerbinatti, G. Bu, F. Wei, T.L. Xu, L.J. Muglia, Z.F. Chen, Y.P. Auberson, B.K. Kaang, and M. Zhuo Upregulation of forebrain NMDA NR2B receptors contributes to behavioral sensitization after inflammation J Neurosci 25 2005 11107 11116
43. H. Xu, L.J. Wu, H. Wang, X. Zhang, K.I. Vadakkan, S.S. Kim, H.W. Steenland, and M. Zhuo Presynaptic and postsynaptic amplifications of neuropathic pain in the anterior cingulate cortex J Neurosci 28 2008 7445 7453
44. Z.Y. Zhuang, Y.R. Wen, D.R. Zhang, T. Borsello, C. Bonny, G.R. Strichartz, I. Decosterd, and R.R. Ji A peptide c-Jun N-terminal kinase (JNK) inhibitor blocks mechanical allodynia after spinal nerve ligation: respective roles of JNK activation in primary sensory neurons and spinal astrocytes for neuropathic pain development and maintenance J Neurosci 26 2006 3551 3560
45. M. Zhuo Cortical excitation and chronic pain Trends Neurosci 31 2008 199 207