Pain-related deactivation of medial prefrontal cortical neurons involves mGluR1 and GABA A receptors

Journal of Neurophysiology

Volumn 106, Issue 5, 2011, Pages 2642-2652

  Ji, Guangchen ^a   Neugebauer, Volker ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

Author keywords

GABAergic inhibition of mPFC; mGluR5

Indexed keywords

2 METHYL 6 (PHENYLETHYNYL)PYRIDINE; 3,5 DIHYDROXYPHENYLGLYCINE; 4 AMINOBUTYRIC ACID RECEPTOR; 4 CARBOXY 2 METHYLPHENYLGLYCINE; BENZYL[3 [[1 (3,4 DICHLOROPHENYL)ETHYL]AMINO] 2 HYDROXYPROPYL]PHOSPHINIC ACID; BICUCULLINE; METABOTROPIC RECEPTOR 1; METABOTROPIC RECEPTOR 5;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR CINGULATE; ARTHRITIS; ARTICLE; BRAIN CELL; CINGULATE GYRUS; CONTROLLED STUDY; EVOKED RESPONSE; GABAERGIC SYSTEM; KNEE; MALE; MICRODIALYSIS; NERVE CELL; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT;

ACTION POTENTIALS; ANIMALS; ARTHRITIS, EXPERIMENTAL; BENZOATES; BICUCULLINE; DISEASE MODELS, ANIMAL; ELECTROPHYSIOLOGY; EXCITATORY AMINO ACID ANTAGONISTS; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GLYCINE; MALE; METHOXYHYDROXYPHENYLGLYCOL; NEURONS; PAIN; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GABA-A; RECEPTORS, METABOTROPIC GLUTAMATE;

EID: 80755143875     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00461.2011     Document Type: Article

References (95)

1. Anwyl R. Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res Brain Res Rev 29: 83-120, 1999.
2. Apkarian AV, Baliki MN, Geha PY. Towards a theory of chronic pain. Prog Neurobiol 87: 81-97, 2009.
3. Apkarian AV, Bushnell MC, Treede RD, Zubieta JK. Human brain mechanisms of pain perception and regulation in health and disease. Eur J Pain 9: 463-484, 2005.
4. Apkarian AV, Hashmi JA, Baliki MN. Pain and the brain: specificity and plasticity of the brain in clinical chronic pain. Pain 152: S49-S64, 2011.
5. Apkarian AV, Sosa Y, Krauss BR, Thomas PS, Fredrickson BE, Levy RE, Harden RN, Chialvo DR. Chronic pain patients are impaired on an emotional decision-making task. Pain 108: 129-136, 2004a.
6. Apkarian AV, Sosa Y, Sonty S, Levy RM, Harden RN, Parrish TB, Gitelman DR. Chronic back pain is associated with decreased prefrontal and thalamic gray matter density. J Neurosci 24: 10410-10415, 2004b.
7. Bacon SJ, Headlam AJ, Gabbott PL, Smith AD. Amygdala input to medial prefrontal cortex (mPFC) in the rat: a light and electron microscope study. Brain Res 720: 211-219, 1996.
8. Ballester-Rosado CJ, Albright MJ, Wu CS, Liao CC, Zhu J, Xu J, Lee LJ, Lu HC. mGluR5 in cortical excitatory neurons exerts both cell-autonomous and -nonautonomous influences on cortical somatosensory circuit formation. J Neurosci 30: 16896-16909, 2010.
9. Battaglia G, Fornai F, Busceti CL, Aloisi G, Cerrito F, De Blasi A, Melchiorri D, Nicoletti F. Selective blockade of mGlu5 metabotropic glutamate receptors is protective against methamphetamine neurotoxicity. J Neurosci 22: 2135-2141, 2002.
10. Beasley CL, Zhang ZJ, Patten I, Reynolds GP. Selective deficits in prefrontal cortical GABAergic neurons in schizophrenia defined by the presence of calcium-binding proteins. Biol Psychiatry 52: 708-715, 2002.
11. Bechara A. Decision making, impulse control and loss of willpower to resist drugs: a neurocognitive perspective. Nat Neurosci 8: 1458-1463, 2005.
12. Bechara A, Damasio H, Damasio AR. Role of the amygdala in decisionmaking. Ann N Y Acad Sci 985: 356-369, 2003.
13. Bechara A, Damasio H, Damasio AR, Lee GP. Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making. J Neurosci 19: 5473-5481, 1999.
14. Bechara A, Damasio H, Tranel D, Anderson SW. Dissociation of working memory from decision making within the human prefrontal cortex. J Neurosci 18: 428-437, 1998.
15. Bechara A, Dolan S, Denburg N, Hindes A, Anderson SW, Nathan PE. Decision-making deficits, linked to a dysfunctional ventromedial prefrontal cortex, revealed in alcohol and stimulant abusers. Neuropsychologia 39: 376-389, 2001.
16. Borsook D, Becerra L, Carlezon WA Jr, Shaw M, Renshaw P, Elman I, Levine J. Reward-aversion circuitry in analgesia and pain: implications for psychiatric disorders. Eur J Pain 11: 7-20, 2007.
17. Bowie CR, Harvey PD. Cognitive deficits and functional outcome in schizophrenia. Neuropsychiatr Dis Treat 2: 531-536, 2006.
18. Cartmell J, Schoepp DD. Regulation of neurotransmitter release by metabotropic glutamate receptors. J Neurochem 75: 889-907, 2000.
19. Cauli B, Porter JT, Tsuzuki K, Lambolez B, Rossier J, Quenet B, Audinat E. Classification of fusiform neocortical interneurons based on unsupervised clustering. Proc Natl Acad Sci USA 97: 6144-6149, 2000.
20. Chu Z, Hablitz JJ. Activation of group I mGluRs increases spontaneous IPSC frequency in rat frontal cortex. J Neurophysiol 80: 621-627, 1998.
21. Clarke HF, Dalley JW, Crofts HS, Robbins TW, Roberts AC. Cognitive inflexibility after prefrontal serotonin depletion. Science 304: 878-880, 2004.
22. Constantinidis C, Goldman-Rakic PS. Correlated discharges among putative pyramidal neurons and interneurons in the primate prefrontal cortex. J Neurophysiol 88: 3487-3497, 2002.
23. Cosford ND, Tehrani L, Roppe J, Schweiger E, Smith ND, Anderson J, Bristow L, Brodkin J, Jiang X, McDonald I, Rao S, Washburn M, Varney MA. 3-[(2-Methyl-1,3-thiazol-4-yl)ethynyl]-pyridine: a potent and highly selective metabotropic glutamate subtype 5 receptor antagonist with anxiolytic activity. J Med Chem 46: 204-206, 2003.
24. Doyle MW, Andresen MC. Reliability of monosynaptic sensory transmission in brain stem neurons in vitro. J Neurophysiol 85: 2213-2223, 2001.
25. Ehrlich I, Humeau Y, Grenier F, Ciocchi S, Herry C, Luthi A. Amygdala inhibitory circuits and the control of fear memory. Neuron 62: 757-771, 2009.
26. Ferrante M, Migliore M, Ascoli GA. Feed-forward inhibition as a buffer of the neuronal input-output relation. Proc Natl Acad Sci USA 106: 18004-18009, 2009.
27. Gabbott PLA, Warner TA, Busby SJ. Amygdala input monosynaptically innervates parvalbumin immunoreactive local circuit neurons in rat medial prefrontal cortex. Neuroscience 139: 1039-1048, 2006.
28. Galhardo V, Pais-Vieira M. Decision-making cognitive deficits in a rat model of chronic pain. Soc Neurosci Abstracts 50.3, vol 35, 2005.
29. Goto Y, Yang CR, Otani S. Functional and dysfunctional synaptic plasticity in prefrontal cortex: roles in psychiatric disorders. Biol Psychiatry 67: 199-207, 2010.
30. Gu BM, Park JY, Kang DH, Lee SJ, Yoo SY, Jo HJ, Choi CH, Lee JM, Kwon JS. Neural correlates of cognitive inflexibility during task-switching in obsessive-compulsive disorder. Brain 131: 155-164, 2008.
31. Han JS, Bird GC, Li W, Neugebauer V. Computerized analysis of audible and ultrasonic vocalizations of rats as a standardized measure of pain-related behavior. J Neurosci Methods 141: 261-269, 2005.
32. Han JS, Neugebauer V. 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, 2005.
33. Herry C, Ciocchi S, Senn V, Demmou L, Muller C, Luthi A. Switching on and off fear by distinct neuronal circuits. Nature 454: 600-606, 2008.
34. Holland PC, Gallagher M. Amygdala-frontal interactions and reward expectancy. Curr Opin Neurobiol 14: 148-155, 2004.
35. Homayoun H, Moghaddam B. Group 5 metabotropic glutamate receptors: role in modulating cortical activity and relevance to cognition. Eur J Pharmacol 639: 33-39, 2010.
36. Homayoun H, Moghaddam B. NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons. J Neurosci 27: 11496-11500, 2007.
37. Ji G, Neugebauer V. Differential effects of CRF1 and CRF2 receptor antagonists on pain-related sensitization of neurons in the central nucleus of the amygdala. J Neurophysiol 97: 3893-3904, 2007.
38. Ji G, Neugebauer V. Hemispheric lateralization of pain processing by amygdala neurons. J Neurophysiol 102: 2253-2264, 2009.
39. Ji G, Neugebauer V. Reactive oxygen species are involved in group I mGluR-mediated facilitation of nociceptive processing in amygdala neurons. J Neurophysiol 104: 218-229, 2010.
40. Ji G, Sun H, Fu Y, Li Z, Pais-Vieira M, Galhardo V, Neugebauer V. Cognitive impairment in pain through amygdala-driven prefrontal cortical deactivation. J Neurosci 30: 5451-5464, 2010.
41. Karakossian MH, Otis TS. Excitation of cerebellar interneurons by group I metabotropic glutamate receptors. J Neurophysiol 92: 1558-1565, 2004.
42. Kingston AE, Griffey K, Johnson MP, Chamberlain MJ, Kelly G, Tomlinson R, Wright RA, Johnson BG, Schoepp DD, Harris JR, Clark BP, Baker RS, Tizzano JT. Inhibition of group I metabotropic glutamate receptor responses in vivo in rats by a new generation of carboxyphenylglycine- like amino acid antagonists. Neurosci Lett 330: 127-130, 2002.
43. Kita H, Kitai ST. Amygdaloid projections to the frontal cortex and the striatum in the rat. J Comp Neurol 298: 40-49, 1990.
44. Kouneiher F, Charron S, Koechlin E. Motivation and cognitive control in the human prefrontal cortex. Nat Neurosci 12: 939-945, 2009.
45. Laviolette SR, Grace AA. Cannabinoids potentiate emotional learning plasticity in neurons of the medial prefrontal cortex through basolateral amygdala inputs. J Neurosci 26: 6458-6468, 2006.
46. Lawrence JJ, McBain CJ. Interneuron diversity series: containing the detonation- feedforward inhibition in the CA3 hippocampus. Trends Neurosci 26: 631-640, 2003.
47. Lea PM, Faden AI. Metabotropic glutamate receptor subtype 5 antagonists MPEP and MTEP. CNS Drug Rev 12: 149-166, 2006.
48. Legrain V, Damme SV, Eccleston C, Davis KD, Seminowicz DA, Crombez G. A neurocognitive model of attention to pain: behavioral and neuroimaging evidence. Pain 144: 230-232, 2009.
49. Lesage A, Steckler T. Metabotropic glutamate mGlu1 receptor stimulation and blockade: therapeutic opportunities in psychiatric illness. Eur J Pharmacol 639: 2-16, 2010.
50. Li W, Neugebauer V. Differential roles of mGluR1 and mGluR5 in brief and prolonged nociceptive processing in central amygdala neurons. J Neurophysiol 91: 13-24, 2004.
51. Li XY, Ko HG, Chen T, Descalzi G, Koga K, Wang H, Kim SS, Shang Y, Kwak C, Park SW, Shim J, Lee K, Collingridge GL, Kaang BK, Zhuo M. Alleviating neuropathic pain hypersensitivity by inhibiting PKMzeta in the anterior cingulate cortex. Science 330: 1400-1404, 2010.
52. Li Z, Ji G, Neugebauer V. Mitochondrial reactive oxygen species are activated by mGluR5 through IP3 and activate ERK and PKA to increase excitability of amygdala neurons and pain behavior. J Neurosci 31: 1114-1127, 2011.
53. Ling DS, Benardo LS. Recruitment of GABAA inhibition in rat neocortex is limited and not NMDA dependent. J Neurophysiol 74: 2329-2335, 1995.
54. Loane DJ, Stoica BA, Pajoohesh-Ganji A, Byrnes KR, Faden AI. Activation of metabotropic glutamate receptor 5 modulates microglial reactivity and neurotoxicity by inhibiting NADPH oxidase. J Biol Chem 284: 15629-15639, 2009.
55. Lorenz J, Casey KL. Imaging of acute versus pathological pain in humans. Eur J Pain 9: 163-165, 2005.
56. Mannaioni G, Marino MJ, Valenti O, Traynelis SF, Conn PJ. Metabotropic glutamate receptors 1 and 5 differentially regulate CA1 pyramidal cell function. J Neurosci 21: 5925-5934, 2001.
57. Marek GJ, Zhang C. Activation of metabotropic glutamate 5 (mGlu5) receptors induces spontaneous excitatory synaptic currents in layer V pyramidal cells of the rat prefrontal cortex. Neurosci Lett 442: 239-243, 2008.
58. Maren S, Quirk GJ. Neuronal signalling of fear memory. Nat Rev Neurosci 5: 844-852, 2004.
59. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5: 793-807, 2004.
60. McDonald AJ. Organization of amygdaloid projections to the prefrontal cortex and associated striatum in the rat. Neuroscience 44: 1-14, 1991.
61. McGaugh JL. The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 27: 1-28, 2004.
62. Melendez RI, Vuthiganon J, Kalivas PW. Regulation of extracellular glutamate in the prefrontal cortex: focus on the cystine glutamate exchanger and group I metabotropic glutamate receptors. J Pharmacol Exp Ther 314: 139-147, 2005.
63. Metz AE, Yau HJ, Centeno MV, Apkarian AV, Martina M. Morphological and functional reorganization of rat medial prefrontal cortex in neuropathic pain. Proc Natl Acad Sci USA 106, 2423-2428, 2009.
64. Moriarty O, McGuire BE, Finn DP. The effect of pain on cognitive function: a review of clinical and preclinical research. Prog Neurobiol 93: 385-404, 2011.
65. Muly EC, Maddox M, Smith Y. Distribution of mGluR1alpha and mGluR5 immunolabeling in primate prefrontal cortex. J Comp Neurol 467: 521-535, 2003.
66. Neugebauer V. Metabotropic glutamate receptors: novel targets for pain relief. Expert Rev Neurother 1: 207-224, 2001.
67. Neugebauer V. Subcortical processing of nociceptive information: basal ganglia and amygdala. In: Pain, edited by Cervero F and Jensen TS. Amsterdam: Elsevier, 2006, p. 141-158.
68. Neugebauer V, Galhardo V, Maione S, Mackey SC. Forebrain pain mechanisms. Brain Res Rev 60: 226-242, 2009.
69. Neugebauer V, Han JS, Adwanikar H, Fu Y, Ji G. Techniques for assessing knee joint pain in arthritis. Mol Pain 3: 8-20, 2007.
70. Neugebauer V, Li W. Processing of nociceptive mechanical and thermal information in central amygdala neurons with knee-joint input. J Neurophysiol 87: 103-112, 2002.
71. Neugebauer V, Li W, Bird GC, Bhave G, Gereau RW. 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, 2003.
72. Neugebauer V, Li W, Bird GC, Han JS. The amygdala and persistent pain. Neuroscientist 10: 221-234, 2004.
73. Nicoletti F, Bockaert J, Collingridge GL, Conn PJ, Ferraguti F, Schoepp DD, Wroblewski JT, Pin JP. Metabotropic glutamate receptors: from the workbench to the bedside. Neuropharmacology 60: 1017-1041, 2010.
74. Niswender CM, Conn PJ. Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu Rev Pharmacol Toxicol 50: 295-322, 2010.
75. Ohara S, Crone NE, Weiss N, Lenz FA. Analysis of synchrony demonstrates "pain networks" defined by rapidly switching, task-specific, functional connectivity between pain-related cortical structures. Pain 123: 244-253, 2006.
76. Olive MF. Cognitive effects of group I metabotropic glutamate receptor ligands in the context of drug addiction. Eur J Pharmacol 639: 47-58, 2010.
77. Pais-Vieira M, Lima D, Galhardo V. Orbitofrontal cortex lesions disrupt risk assessment in a novel serial decision-making task for rats. Neuroscience 145: 225-231, 2007.
78. Pais-Vieira M, Mendes-Pinto MM, Lima D, Galhardo V. Cognitive impairment of prefrontal-dependent decision-making in rats after the onset of chronic pain. Neuroscience 161: 671-679, 2009.
79. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. New York: Academic, 1998.
80. Phelps EA, Ledoux JE. Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron 48: 175-187, 2005.
81. Pinheiro PS, Mulle C. Presynaptic glutamate receptors: physiological functions and mechanisms of action. Nat Rev Neurosci 9: 423-436, 2008.
82. Ren W, Neugebauer V. Pain-related increase of excitatory transmission and decrease of inhibitory transmission in the central nucleus of the amygdala are mediated by mGluR1. Mol Pain 6: 93, 2010.
83. Ren WJ, Liu Y, Zhou LJ, Li W, Zhong Y, Pang RP, Xin WJ, Wei XH, Wang J, Zhu HQ, Wu CY, Qin ZH, Liu G, Liu XG. Peripheral nerve injury leads to working memory deficits and dysfunction of the hippocampus by upregulation of TNF-alpha in rodents. Neuropsychopharmacology 36: 979-992, 2011.
84. Roozendaal B, McEwen BS, Chattarji S. Stress, memory and the amygdala. Nat Rev Neurosci 10: 423-433, 2009.
85. Segovia G, Mora F. Effects of the metabotropic glutamate receptor agonist, ACPD, on the extracellular concentrations of GABA and acetylcholine in the prefrontal cortex of the rat during the normal process of aging. Brain Res Bull 65: 11-16, 2005.
86. Seutin V, Johnson SW. Recent advances in the pharmacology of quaternary salts of bicuculline. Trends Pharmacol Sci 20: 268-270, 1999.
87. Seymour B, Dolan R. Emotion, decision making, and the amygdala. Neuron 58: 662-671, 2008.
88. Silberberg G, Markram H. Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 53: 735-746, 2007.
89. Stalnaker TA, Franz TM, Singh T, Schoenbaum G. Basolateral amygdala lesions abolish orbitofrontal-dependent reversal impairments. Neuron 54: 51-58, 2007.
90. Stalnaker TA, Takahashi Y, Roesch MR, Schoenbaum G. Neural substrates of cognitive inflexibility after chronic cocaine exposure. Neuropharmacology 56, Suppl 1: 63-72, 2009.
91. Sun H, Neugebauer V. mGluR1, but not mGluR5, activates feed-forward inhibition in the medial prefrontal cortex to impair decision making. J Neurophysiol 106: 960-973, 2011.
92. Sun QQ, Zhang Z, Jiao Y, Zhang C, Szabo G, Erdelyi F. Differential metabotropic glutamate receptor expression and modulation in two neocortical inhibitory networks. J Neurophysiol 101: 2679-2692, 2009.
93. Swanson CJ, Bures M, Johnson MP, Linden AM, Monn JA, Schoepp DD. Metabotropic glutamate receptors as novel targets for anxiety and stress disorders. Nat Rev Drug Discov 4: 131-144, 2005.
94. Vertes RP. Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 142: 1-20, 2006.
95. Wu LJ, Toyoda H, Zhao MG, Lee YS, Tang J, Ko SW, Jia YH, Shum FWF, Zerbinatti CV, Bu G, Wei F, Xu TL, Muglia LJ, Chen ZF, Auberson YP, Kaang BK, Zhuo M. Upregulation of forebrain NMDA NR2B receptors contributes to behavioral sensitization after inflammation. J Neurosci 25: 11107-11116, 2005.