Activation of metabotropic glutamate receptor 5 in the amygdala modulates pain-like behavior

Journal of Neuroscience

Volumn 30, Issue 24, 2010, Pages 8203-8213

  Kolber, Benedict J ^a   Montana, Michael C ^a,b   Carrasquillo, Yarimar ^a   Xu, Jian ^c   Heinemann, Stephen F ^c   Muglia, Louis J ^d   Gereau IV, Robert W ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY   (United States)

^c SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^d VANDERBILT UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3,5 DIHYDROXYPHENYLGLYCINE; METABOTROPIC RECEPTOR 5; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3;

AMYGDALOID NUCLEUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN FUNCTION; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVATION; GENE DISRUPTION; HEMISPHERIC DOMINANCE; HYPERSENSITIVITY; INFLAMMATION; MALE; MOUSE; NOCICEPTIVE STIMULATION; NONHUMAN; PAIN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSITIZATION;

AMYGDALA; ANALYSIS OF VARIANCE; ANIMALS; BUTADIENES; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; FORMALDEHYDE; FUNCTIONAL LATERALITY; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HYPERALGESIA; METHOXYHYDROXYPHENYLGLYCOL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASE 3; NITRILES; PAIN; PAIN MEASUREMENT; PYRIDINES; RECEPTORS, GLUCOCORTICOID; RECEPTORS, KAINIC ACID;

EID: 77953744614     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1216-10.2010     Document Type: Article

References (41)

1. Adwanikar H, Karim F, Gereau RW (2004) Inflammation persistently enhances nocifensive behaviors mediated by spinal group I mGluRs through sustained ERK activation. Pain 111:125-135.
2. Alkire MT, Gruver R, Miller J, McReynolds JR, Hahn EL, Cahill L (2008) Neuroimaging analysis of an anesthetic gas that blocks human emotional memory. Proc Natl Acad Sci U S A 105:1722-1727.
3. Ansah OB, Goncalves L, Almeida A, Pertovaara A (2009) Enhanced pronociception by amygdaloid group I metabotropic glutamate receptors in nerve-injured animals. Exp Neurol 216:66-74.
4. Bernard JF, Peschanski M, Besson JM (1989) A possible spino (trigemino)- ponto-amygdaloid pathway for pain. Neurosci Lett 100:83-88.
5. Bhave G, Karim F, Carlton SM, Gereau RW (2001) Peripheral group I metabotropic glutamate receptors modulate nociception in mice. Nat Neurosci 4:417-423.
6. Bradbury MJ, Giracello DR, Chapman DF, Holtz G, Schaffhauser H, Rao SP, Varney MA, Anderson JJ (2003) Metabotropic glutamate receptor 5 antagonist-induced stimulation of hypothalamic-pituitary-adrenal axis activity: interaction with serotonergic systems. Neuropharmacology 44:562-572.
7. Cahill L, Uncapher M, Kilpatrick L, Alkire MT, Turner J (2004) Sex-related hemispheric lateralization of amygdala function in emotionally influenced memory: an FMRI investigation. Learn Mem 11:261-266.
8. Carrasquillo Y, Gereau RW (2007) Activation of the extracellular signal-regulated kinase in the amygdala modulates pain perception. J Neurosci 27:1543-1551.
9. Carrasquillo Y, Gereau RW (2008) Hemispheric lateralization of a molecular signal for pain modulation in the amygdala. Mol Pain 4:24.
10. Coghill RC, Gilron I, Iadarola MJ (2001) Hemispheric lateralization of somatosensory processing. J Neurophysiol 85:2602-2612.
11. Ferraguti F, Corti C, Valerio E, Mion S, Xuereb J (2001) Activated astrocytes in areas of kainate-induced neuronal injury upregulate the expression of the metabotropic glutamate receptors 2/3 and 5. Exp Brain Res 137:1-11. (Pubitemid 32186610)
12. Fu KY, Light AR, Maixner W (2001) Long-lasting inflammation and long-term hyperalgesia after subcutaneous formalin injection into the rat hind-paw. J Pain 2:2-11.
13. Greenwood-Van Meerveld B, Gibson M, Gunter W, Shepard J, Foreman R, Myers D (2001) Stereotaxic delivery of corticosterone to the amygdala modulates colonic sensitivity in rats. Brain Res 893:135-142.
14. Han JS, Neugebauer V (2005) mGluR1 and mGluR5 antagonists in the amygdala inhibit different components of audible and ultrasonic vocalizations in a model of arthritic pain. Pain 113:211-222.
15. Hu HJ, Gereau RW (2003) ERK integrates PKA and PKC signaling in superficial dorsal horn neurons. II. Modulation of neuronal excitability. J Neurophysiol 90:1680-1688.
16. Hu HJ, Glauner KS, Gereau RW (2003) ERK integrates PKA and PKC signaling in superficial dorsal horn neurons. I. Modulation of A-type K+ currents. J Neurophysiol 90:1671-1679.
17. Hu HJ, Alter BJ, Carrasquillo Y, Qiu CS, Gereau RW (2007) Metabotropic glutamate receptor 5 modulates nociceptive plasticity via extracellular signal-regulated kinase-Kv4.2 signaling in spinal cord dorsal horn neurons. J Neurosci 27:13181-13191.
18. Ikeda R, Takahashi Y, Inoue K, Kato F (2007) NMDA receptor-independent synaptic plasticity in the central amygdala in the rat model of neuropathic pain. Pain 127:161-172.
19. Ji G, Neugebauer V (2009) Hemispheric lateralization of pain processing by amygdala neurons. J Neurophysiol 102:2253-2264.
20. Jia Z, Lu Y, Henderson J, Taverna F, Romano C, Abramow-Newerly W, Wojtowicz JM, Roder J (1998) Selective abolition of the NMDA component of long-term potentiation in mice lacking mGluR5. Learn Mem 5:331-343.
21. Karim F, Wang CC, Gereau RW (2001a) Metabotropic glutamate receptor subtypes 1 and 5 are activators of extracellular signal-regulated kinase signaling required for inflammatory pain in mice. J Neurosci 21:3771-3779. (Pubitemid 32466469)
22. Karim F, Bhave G, Gereau RW (2001b) Metabotropic glutamate receptors on peripheral sensory neuron terminals as targets for the development of novel analgesics. Mol Psychiatry 6:615-617.
23. Kolber BJ, Roberts MS, Howell MP, Wozniak DF, Sands MS, Muglia LJ (2008) Central amygdala glucocorticoid receptor action promotes fear-associated CRH activation and conditioning. Proc Natl Acad Sci U S A 105:12004-12009.
24. Lalumiere RT, McGaugh JL (2005) Memory enhancement induced by post-training intrabasolateral amygdala infusions of beta-adrenergic or muscarinic agonists requires activation of dopamine receptors: involvement of right, but not left, basolateral amygdala. Learn Mem 12:527-532.
25. Li W, Neugebauer V (2004) Differential roles of mGluR1 and mGluR5 in brief and prolonged nociceptive processing in central amygdala neurons. J Neurophysiol 91:13-24.
26. Lu CL,WuYT, Yeh TC, Chen LF, Chang FY, Lee SD, Ho LT, Hsieh JC (2004) Neuronal correlates of gastric pain induced by fundus distension: a 3T-fMRI study. Neurogastroenterol Motil 16:575-587.
27. Manning BH, Mayer DJ (1995a) The central nucleus of the amygdala contributes to the production of morphine antinociception in the formalin test. Pain 63:141-152.
28. Manning BH, Mayer DJ (1995b) The central nucleus of the amygdala contributes to the production of morphine antinociception in the rat tail-flick test. J Neurosci 15:8199-8213.
29. Montana MC, Cavallone LF, Stubbert KK, Stefanescu AD, Kharasch ED, Gereau RW (2009) The metabotropic glutamate receptor subtype 5 antagonist fenobam is analgesic and has improved in vivo selectivity compared with the prototypical antagonist 2-methyl-6-(phenylethynyl)- pyridine. J Pharmacol Exp Ther 330:834-843.
30. Neugebauer V, Li W, Bird GC, Bhave G, Gereau RW (2003) Synaptic plasticity in the amygdala in a model of arthritic pain: differential roles of metabotropic glutamate receptors 1 and 5. J Neurosci 23:52-63. (Pubitemid 36050404)
31. Neugebauer V, Li W, Bird GC, Han JS (2004) The amygdala and persistent pain. Neuroscientist 10:221-234.
32. Romano C, Sesma MA, McDonald CT, O'Malley K, Van den Pol AN, Olney JW (1995) Distribution of metabotropic glutamate receptor mGluR5 immunoreactivity in rat brain. J Comp Neurol 355:455-469.
33. Ryo Y, Miyawaki A, Furuichi T, Mikoshiba K (1993) Expression of the metabotropic glutamate receptor mGluR1 alpha and the ionotropic glutamate receptor GluR1 in the brain during the postnatal development of normal mouse and in the cerebellum from mutant mice. J Neurosci Res 36:19-32. (Pubitemid 23260459)
34. Schneider F, Habel U, Holthusen H, Kessler C, Posse S, Muller-Gartner HW, Arndt JO (2001) Subjective ratings of pain correlate with subcorticallimbic blood flow: an fMRI study. Neuropsychobiology 43:175-185.
35. Tjolsen A, Berge OG, Hunskaar S, Rosland JH, Hole K (1992) The formalin test: an evaluation of the method. Pain 51:5-17.
36. Varney MA, Gereau RW (2002) Metabotropic glutamate receptor involvement in models of acute and persistent pain: prospects for the development of novel analgesics. Curr Drug Targets CNS Neurol Disord 1:283-296.
37. Vissers K, Adriaensen H, De Coster R, De Deyne C, Meert TF (2003) A chronic-constriction injury of the sciatic nerve reduces bilaterally the responsiveness to formalin in rats: a behavioral and hormonal evaluation. Anesth Analg 97:520-525.
38. Vissers KC, De Jongh RF, Crul BJ, Vinken P, Meert TF (2004) Adrenalectomy affects pain behavior of rats after formalin injection. Life Sci 74:1243-1251.
39. Walker K, Bowes M, Panesar M, Davis A, Gentry C, Kesingland A, Gasparini F, Spooren W, Stoehr N, Pagano A, Flor PJ, Vranesic I, Lingenhoehl K, Johnson EC, Varney M, Urban L, Kuhn R (2001) Metabotropic glutamate receptor subtype 5 (mGlu5) and nociceptive function. I. Selective blockade of mGlu5 receptors in models of acute, persistent and chronic pain. Neuropharmacology 40:1-9.
40. Xu J, Zhu Y, Contractor A, Heinemann SF (2009) mGluR5 has a critical role in inhibitory learning. J Neurosci 29:3676-3684.
41. Yang D, Gereau RW (2003) Peripheral group II metabotropic glutamate receptors mediate endogenous anti-allodynia in inflammation. Pain 106: 411-417.