No requirement of TRPV1 in long-term potentiation or long-term depression in the anterior cingulate cortex

Molecular Brain

Volumn 7, Issue 1, 2014, Pages

  Liu, Ming Gang ^a,b   Zhuo, Min ^a,b  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Anterior cingulate cortex; Chronic pain; Long term depression; Long term potentiation; Multi electrode array; Transient receptor potential vanilloid type 1

Indexed keywords

4 CHLORO N (3 METHOXYPHENYL)CINNAMAMIDE; N (1,4 BENZODIOXAN 6 YL) 3 (4 TERT BUTYLPHENYL)ACRYLAMIDE; VANILLOID RECEPTOR 1;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTERIOR CINGULATE; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN SLICE; CHRONIC PAIN; CONTROLLED STUDY; CORTICAL ELECTRODE; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; THETA RHYTHM;

MUS;

ACRYLAMIDES; ANILIDES; ANIMALS; BICYCLO COMPOUNDS, HETEROCYCLIC; CINNAMATES; GYRUS CINGULI; LONG-TERM POTENTIATION; LONG-TERM SYNAPTIC DEPRESSION; MALE; MICE; MICE, INBRED C57BL; TRPV CATION CHANNELS;

EID: 84898822647     PISSN: None     EISSN: 17566606     Source Type: Journal    
DOI: 10.1186/1756-6606-7-27     Document Type: Article

References (89)

1. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, Raumann BE, Basbaum AI, Julius D, Neuron 1998 21 3 531 543 10.1016/S0896-6273(00)80564-4 9768840
2. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D, Nature 1997 389 6653 816 824 10.1038/39807 9349813
3. Cellular and molecular mechanisms of pain. Basbaum AI, Bautista DM, Scherrer G, Julius D, Cell 2009 139 2 267 284 10.1016/j.cell.2009.09.028 19837031
4. TRP channels and pain. Julius D, Annu Rev Cell Dev Biol 2013 29 355 384 10.1146/annurev-cellbio-101011-155833 24099085
5. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D, Science 2000 288 5464 306 313 10.1126/science.288.5464.306 10764638
6. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Davis JB, Gray J, Gunthorpe MJ, Hatcher JP, Davey PT, Overend P, Harries MH, Latcham J, Clapham C, Atkinson K, Hughes SA, Rance K, Grau E, Harper AJ, Pugh PL, Rogers DC, Bingham S, Randall A, Sheardown SA, Nature 2000 405 6783 183 187 10.1038/35012076 10821274
7. Investigation of the role of TRPV1 receptors in acute and chronic nociceptive processes using gene-deficient mice. Bolcskei K, Helyes Z, Szabo A, Sandor K, Elekes K, Nemeth J, Almasi R, Pinter E, Petho G, Szolcsanyi J, Pain 2005 117 3 368 376 10.1016/j.pain.2005.06.024 16150543
8. Nerve growth factor contribution via transient receptor potential vanilloid 1 to ectopic orofacial pain. Shinoda M, Asano M, Omagari D, Honda K, Hitomi S, Katagiri A, Iwata K, J Neurosci 2011 31 19 7145 7155 10.1523/JNEUROSCI.0481-11.2011 21562277
9. TRPV1 receptors in the CNS play a key role in broad-spectrum analgesia of TRPV1 antagonists. Cui M, Honore P, Zhong C, Gauvin D, Mikusa J, Hernandez G, Chandran P, Gomtsyan A, Brown B, Bayburt EK, Marsh K, Bianchi B, McDonald H, Niforatos W, Neelands TR, Moreland RB, Decker MW, Lee CH, Sullivan JP, Faltynek CR, J Neurosci 2006 26 37 9385 9393 10.1523/JNEUROSCI.1246-06.2006 16971522
10. The VR1 antagonist capsazepine reverses mechanical hyperalgesia in models of inflammatory and neuropathic pain. Walker KM, Urban L, Medhurst SJ, Patel S, Panesar M, Fox AJ, McIntyre P, J Pharmacol Exp Ther 2003 304 1 56 62 10.1124/jpet.102.042010 12490575
11. Amelioration of neuropathic pain by novel transient receptor potential vanilloid 1 antagonist AS1928370 in rats without hyperthermic effect. Watabiki T, Kiso T, Kuramochi T, Yonezawa K, Tsuji N, Kohara A, Kakimoto S, Aoki T, Matsuoka N, J Pharmacol Exp Ther 2011 336 3 743 750 10.1124/jpet.110.175570 21098091
12. N-(4-Tertiarybutylphenyl)-4-(3-cholorphyridin-2-yl)tetrahydropyrazine- 1(2H)-carbox-amide (BCTC), a novel, orally effective vanilloid receptor 1 antagonist with analgesic properties: II. in vivo characterization in rat models of inflammatory and neuropathic pain. Pomonis JD, Harrison JE, Mark L, Bristol DR, Valenzano KJ, Walker K, J Pharmacol Exp Ther 2003 306 1 387 393 10.1124/jpet.102.046268 12721336
13. A-425619 [1-isoquinolin-5-yl-3-(4-trifluoromethyl-benzyl)-urea], a novel transient receptor potential type V1 receptor antagonist, relieves pathophysiological pain associated with inflammation and tissue injury in rats. Honore P, Wismer CT, Mikusa J, Zhu CZ, Zhong C, Gauvin DM, Gomtsyan A, El Kouhen R, Lee CH, Marsh K, Sullivan JP, Faltynek CR, Jarvis MF, J Pharmacol Exp Ther 2005 314 1 410 421 10.1124/jpet.105.083915 15837818
14. Distribution of mRNA for vanilloid receptor subtype 1 (VR1), and VR1-like immunoreactivity, in the central nervous system of the rat and human. Mezey E, Toth ZE, Cortright DN, Arzubi MK, Krause JE, Elde R, Guo A, Blumberg PM, Szallasi A, Proc Natl Acad Sci U S A 2000 97 7 3655 3660 10.1073/pnas.97.7.3655 10725386
15. Immunohistochemical localization of cannabinoid type 1 and vanilloid transient receptor potential vanilloid type 1 receptors in the mouse brain. Cristino L, de Petrocellis L, Pryce G, Baker D, Guglielmotti V, Di Marzo V, Neuroscience 2006 139 4 1405 1415 10.1016/j.neuroscience.2006.02.074 16603318
16. Hot receptors in the brain. Steenland HW, Ko SW, Wu LJ, Zhuo M, Mol Pain 2006 2 34 10.1186/1744-8069-2-34 17092351
17. 3H]Resiniferatoxin autoradiography in the CNS of wild-type and TRPV1 null mice defines TRPV1 (VR-1) protein distribution. Roberts JC, Davis JB, Benham CD, Brain Res 2004 995 2 176 183 10.1016/j.brainres.2003.10.001 14672807
18. Existence of capsaicin-sensitive glutamatergic terminals in rat hypothalamus. Sasamura T, Sasaki M, Tohda C, Kuraishi Y, Neuroreport 1998 9 9 2045 2048 10.1097/00001756-199806220-00025 9674591
19. The distribution and regulation of vanilloid receptor VR1 and VR1 5' splice variant RNA expression in rat. Sanchez JF, Krause JE, Cortright DN, Neuroscience 2001 107 3 373 381 10.1016/S0306-4522(01)00373-6 11718993
20. Hot flash: TRPV channels in the brain. Kauer JA, Gibson HE, Trends Neurosci 2009 32 4 215 224 10.1016/j.tins.2008.12.006 19285736
21. Reduced anxiety, conditioned fear, and hippocampal long-term potentiation in transient receptor potential vanilloid type 1 receptor-deficient mice. Marsch R, Foeller E, Rammes G, Bunck M, Kossl M, Holsboer F, Zieglgansberger W, Landgraf R, Lutz B, Wotjak CT, J Neurosci 2007 27 4 832 839 10.1523/JNEUROSCI. 3303-06.2007 17251423
22. Antistress effect of TRPV1 channel on synaptic plasticity and spatial memory. Li HB, Mao RR, Zhang JC, Yang Y, Cao J, Xu L, Biol Psychiatry 2008 64 4 286 292 10.1016/j.biopsych.2008.02.020 18405883
23. Loss of interneuron LTD and attenuated pyramidal cell LTP in Trpv1 and Trpv3 KO mice. Brown TE, Chirila AM, Schrank BR, Kauer JA, Hippocampus 2013 23 8 662 671 10.1002/hipo.22125 23536486
24. TRPV1 channels mediate long-term depression at synapses on hippocampal interneurons. Gibson HE, Edwards JG, Page RS, Van Hook MJ, Kauer JA, Neuron 2008 57 5 746 759 10.1016/j.neuron.2007.12.027 18341994
25. TRPV1 activation by endogenous anandamide triggers postsynaptic long-term depression in dentate gyrus. Chavez AE, Chiu CQ, Castillo PE, Nat Neurosci 2010 13 12 1511 1518 10.1038/nn.2684 21076423
26. Postsynaptic TRPV1 triggers cell type-specific long-term depression in the nucleus accumbens. Grueter BA, Brasnjo G, Malenka RC, Nat Neurosci 2010 13 12 1519 1525 10.1038/nn.2685 21076424
27. Vanilloid (capsaicin) receptors in the rat: distribution in the brain, regional differences in the spinal cord, axonal transport to the periphery, and depletion by systemic vanilloid treatment. Szallasi A, Nilsson S, Farkas-Szallasi T, Blumberg PM, Hokfelt T, Lundberg JM, Brain Res 1995 703 1-2 175 183 8719630
28. Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Toth A, Boczan J, Kedei N, Lizanecz E, Bagi Z, Papp Z, Edes I, Csiba L, Blumberg PM, Brain Res Mol Brain Res 2005 135 1-2 162 168 15857679
29. Specific binding of [3H]resiniferatoxin by human and rat preoptic area, locus ceruleus, medial hypothalamus, reticular formation and ventral thalamus membrane preparations. Acs G, Palkovits M, Blumberg PM, Life Sci 1996 59 22 1899 1908 10.1016/S0024-3205(96)00537-1 8950287
30. Pharmacological characterization of vanilloid receptor located in the brain. Szabo T, Biro T, Gonzalez AF, Palkovits M, Blumberg PM, Brain Res Mol Brain Res 2002 98 1-2 51 57 11834295
31. Transient receptor potential vanilloid 1 agonists modulate hippocampal CA1 LTP via the GABAergic system. Bennion D, Jensen T, Walther C, Hamblin J, Wallmann A, Couch J, Blickenstaff J, Castle M, Dean L, Beckstead S, Merrill C, Muir C, St Pierre T, Williams B, Daniel S, Edwards JG, Neuropharmacology 2011 61 4 730 738 10.1016/j.neuropharm.2011.05.018 21645527
32. Calcineurin is required for TRPV1-induced long-term depression of hippocampal interneurons. Jensen T, Edwards JG, Neurosci Lett 2012 510 2 82 87 10.1016/j.neulet.2012.01.006 22260796
33. TRPV1 channels control synaptic plasticity in the developing superior colliculus. Maione S, Cristino L, Migliozzi AL, Georgiou AL, Starowicz K, Salt TE, Di Marzo V, J Physiol 2009 587 Pt 11 2521 2535 19406878
34. Polymodal activation of the endocannabinoid system in the extended amygdala. Puente N, Cui Y, Lassalle O, Lafourcade M, Georges F, Venance L, Grandes P, Manzoni OJ, Nat Neurosci 2011 14 12 1542 1547 10.1038/nn.2974 22057189
35. Capsaicin-induced changes in LTP in the lateral amygdala are mediated by TRPV1. Zschenderlein C, Gebhardt C, von Bohlen Und Halbach O, Kulisch C, Albrecht D, PLoS One 2011 6 1 16116 10.1371/journal.pone.0016116 21249195
36. Critical role of nociceptor plasticity in chronic pain. Reichling DB, Levine JD, Trends Neurosci 2009 32 12 611 618 10.1016/j.tins.2009.07.007 19781793
37. Central mechanisms of pathological pain. Kuner R, Nat Med 2010 16 11 1258 1266 10.1038/nm.2231 20948531
38. Cortical excitation and chronic pain. Zhuo M, Trends Neurosci 2008 31 4 199 207 10.1016/j.tins.2008.01.003 18329111
39. Long-term potentiation in the anterior cingulate cortex and chronic pain. Zhuo M, Philos Trans R Soc Lond B Biol Sci 2014 369 1633 20130146 24298148
40. Understanding LTP in pain pathways. Sandkuhler J, Mol Pain 2007 3 9 10.1186/1744-8069-3-9 17407590
41. Long-term potentiation in spinal nociceptive pathways as a novel target for pain therapy. Ruscheweyh R, Wilder-Smith O, Drdla R, Liu XG, Sandkuhler J, Mol Pain 2011 7 20 10.1186/1744-8069-7-20 21443797
42. Cortical plasticity as a new endpoint measurement for chronic pain. Zhuo M, Mol Pain 2011 7 54 10.1186/1744-8069-7-54 21798042
43. Enhanced presynaptic neurotransmitter release in the anterior cingulate cortex of mice with chronic pain. Zhao MG, Ko SW, Wu LJ, Toyoda H, Xu H, Quan J, Li J, Jia Y, Ren M, Xu ZC, Zhuo M, J Neurosci 2006 26 35 8923 8930 10.1523/JNEUROSCI.2103-06.2006 16943548
44. Presynaptic and postsynaptic amplifications of neuropathic pain in the anterior cingulate cortex. Xu H, Wu LJ, Wang H, Zhang X, Vadakkan KI, Kim SS, Steenland HW, Zhuo M, J Neurosci 2008 28 29 7445 7453 10.1523/JNEUROSCI.1812-08. 2008 18632948
45. Enhanced quantal release of excitatory transmitter in anterior cingulate cortex of adult mice with chronic pain. Toyoda H, Zhao MG, Zhuo M, Mol Pain 2009 5 4 10.1186/1744-8069-5-4 19171071
46. Alleviating neuropathic pain hypersensitivity by inhibiting PKMzeta in the anterior cingulate cortex. 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, Science 2010 330 6009 1400 1404 10.1126/science.1191792 21127255
47. Presynaptic and postsynaptic cortical mechanisms of chronic pain. Descalzi G, Kim S, Zhuo M, Mol Neurobiol 2009 40 3 253 259 10.1007/s12035-009- 8085-9 19821080
48. Targeting neuronal adenylyl cyclase for the treatment of chronic pain. Zhuo M, Drug Discov Today 2012 17 11-12 573 582 22405897
49. Genetic elimination of behavioral sensitization in mice lacking calmodulin-stimulated adenylyl cyclases. Wei F, Qiu CS, Kim SJ, Muglia L, Maas JW, Pineda VV, Xu HM, Chen ZF, Storm DR, Muglia LJ, Zhuo M, Neuron 2002 36 4 713 726 10.1016/S0896-6273(02)01019-X 12441059
50. Identification of an adenylyl cyclase inhibitor for treating neuropathic and inflammatory pain. Wang H, Xu H, Wu LJ, Kim SS, Chen T, Koga K, Descalzi G, Gong B, Vadakkan KI, Zhang X, Kaang BK, Zhuo M, Sci Transl Med 2011 3 65 65ra63
51. Upregulation of forebrain NMDA NR2B receptors contributes to behavioral sensitization after inflammation. Wu LJ, Toyoda H, Zhao MG, Lee YS, Tang J, Ko SW, Jia YH, Shum FW, Zerbinatti CV, Bu G, Bu G, Wei F, Xu TL, Muglia LJ, Chen ZF, Auberson YP, Kaang BK, Zhuo M, J Neurosci 2005 25 48 11107 11116 10.1523/JNEUROSCI.1678-05.2005 16319310
52. Targeting the NMDA receptor subunit NR2B for the treatment of neuropathic pain. Wu LJ, Zhuo M, Neurotherapeutics 2009 6 4 693 702 10.1016/j.nurt.2009.07. 008 19789073
53. NMDA NR2A and NR2B receptors in the rostral anterior cingulate cortex contribute to pain-related aversion in male rats. Li TT, Ren WH, Xiao X, Nan J, Cheng LZ, Zhang XH, Zhao ZQ, Zhang YQ, Pain 2009 146 1-2 183 193 19695778
54. NMDA and AMPA receptors in the anterior cingulate cortex mediates visceral pain in visceral hypersensitivity rats. Zhou L, Huang J, Gao J, Zhang G, Jiang J, Cell Immunol 2014 287 2 86 90 10.1016/j.cellimm.2013.12.001 24487031
55. Upregulation of presynaptic proteins and protein kinases associated with enhanced glutamate release from axonal terminals (synaptosomes) of the medial prefrontal cortex in rats with neuropathic pain. Hung KL, Wang SJ, Wang YC, Chiang TR, Wang CC, Pain 2014 155 2 377 387 10.1016/j.pain.2013.10.026 24211726
56. Increased synaptic GluR1 subunits in the anterior cingulate cortex of rats with peripheral inflammation. Bie B, Brown DL, Naguib M, Eur J Pharmacol 2011 653 1-3 26 31 21147092
57. TRPV1: a therapeutic target for novel analgesic drugs? Szallasi A, Cruz F, Geppetti P, Trends Mol Med 2006 12 11 545 554 10.1016/j.molmed.2006.09.001 16996800
58. Transient receptor potential channels: targeting pain at the source. Patapoutian A, Tate S, Woolf CJ, Nat Rev Drug Discov 2009 8 1 55 68 10.1038/nrd2757 19116627
59. Moving towards supraspinal TRPV1 receptors for chronic pain relief. Palazzo E, Luongo L, de Novellis V, Berrino L, Rossi F, Maione S, Mol Pain 2010 6 66 10.1186/1744-8069-6-66 20937102
60. Therapeutic potential of vanilloid receptor TRPV1 agonists and antagonists as analgesics: recent advances and setbacks. Wong GY, Gavva NR, Brain Res Rev 2009 60 1 267 277 10.1016/j.brainresrev.2008.12.006 19150372
61. Targeting TRPV1 for pain relief: limits, losers and laurels. Szallasi A, Sheta M, Expert Opin Investig Drugs 2012 21 9 1351 1369 10.1517/13543784.2012. 704021 22780443
62. Resolving TRPV1- and TNF-alpha-mediated spinal cord synaptic plasticity and inflammatory pain with neuroprotectin D1. Park CK, Lu N, Xu ZZ, Liu T, Serhan CN, Ji RR, J Neurosci 2011 31 42 15072 15085 10.1523/JNEUROSCI.2443-11. 2011 22016541
63. Plasticity of metabotropic glutamate receptor-dependent long-term depression in the anterior cingulate cortex after amputation. Kang SJ, Liu MG, Chen T, Ko HG, Baek GC, Lee HR, Lee K, Collingridge GL, Kaang BK, Zhuo M, J Neurosci 2012 32 33 11318 11329 10.1523/JNEUROSCI.0146-12.2012 22895715
64. Long-term potentiation of synaptic transmission in the adult mouse insular cortex: multielectrode array recordings. Liu MG, Kang SJ, Shi TY, Koga K, Zhang MM, Collingridge GL, Kaang BK, Zhuo M, J Neurophysiol 2013 110 2 505 521 10.1152/jn.01104.2012 23636718
65. Long-term depression of synaptic transmission in the adult mouse insular cortex in vitro. Liu MG, Koga K, Guo YY, Kang SJ, Collingridge GL, Kaang BK, Zhao MG, Zhuo M, Eur J Neurosci 2013 38 8 3128 3145 10.1111/ejn.12330 23930740
66. Identification and characterisation of SB-366791, a potent and selective vanilloid receptor (VR1/TRPV1) antagonist. Gunthorpe MJ, Rami HK, Jerman JC, Smart D, Gill CH, Soffin EM, Luis Hannan S, Lappin SC, Egerton J, Smith GD, Worby A, Howett L, Owen D, Nasir S, Davies CH, Thompson M, Wyman PA, Randall AD, Davis JB, Neuropharmacology 2004 46 1 133 149 10.1016/S0028-3908(03)00305-8 14654105
67. AMG 9810 [(E)-3-(4-t-butylphenyl)-N-(2,3-dihydrobenzo[b][1,4] dioxin-6-yl)acrylamide], a novel vanilloid receptor 1 (TRPV1) antagonist with antihyperalgesic properties. Gavva NR, Tamir R, Qu Y, Klionsky L, Zhang TJ, Immke D, Wang J, Zhu D, Vanderah TW, Porreca F, Doherty EM, Norman MH, Wild KD, Bannon AW, Louis JC, Treanor JJ, J Pharmacol Exp Ther 2005 313 1 474 484 15615864
68. N-type voltage gated calcium channels mediate excitatory synaptic transmission in the anterior cingulate cortex of adult mice. Kang SJ, Liu MG, Shi TY, Zhao MG, Kaang BK, Zhuo M, Mol Pain 2013 9 1 58 10.1186/1744-8069-9-58 24228737
69. Loss of long-term depression in the insular cortex after tail amputation in adult mice. Liu MG, Zhuo M, Mol Pain 2014 10 1 1 10.1186/1744-8069-10-1 24398034
70. Long-term depression: multiple forms and implications for brain function. Massey PV, Bashir ZI, Trends Neurosci 2007 30 4 176 184 10.1016/j.tins.2007.02. 005 17335914
71. Long-term depression in the CNS. Collingridge GL, Peineau S, Howland JG, Wang YT, Nat Rev Neurosci 2010 11 7 459 473 20559335
72. The TRP ion channel family. Clapham DE, Runnels LW, Strubing C, Nat Rev Neurosci 2001 2 6 387 396 10.1038/35077544 11389472
73. p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia. Ji RR, Samad TA, Jin SX, Schmoll R, Woolf CJ, Neuron 2002 36 1 57 68 10.1016/S0896-6273(02)00908-X 12367506
74. Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2-mediated inhibition. Chuang HH, Prescott ED, Kong H, Shields S, Jordt SE, Basbaum AI, Chao MV, Julius D, Nature 2001 411 6840 957 962 10.1038/35082088 11418861
75. Protease-activated receptor 2 sensitizes the capsaicin receptor transient receptor potential vanilloid receptor 1 to induce hyperalgesia. Amadesi S, Nie J, Vergnolle N, Cottrell GS, Grady EF, Trevisani M, Manni C, Geppetti P, McRoberts JA, Ennes H, Davis JB, Mayer EA, Bunnett NW, J Neurosci 2004 24 18 4300 4312 10.1523/JNEUROSCI.5679-03.2004 15128844
76. Elevation of endocannabinoid levels in the ventrolateral periaqueductal grey through inhibition of fatty acid amide hydrolase affects descending nociceptive pathways via both cannabinoid receptor type 1 and transient receptor potential vanilloid type-1 receptors. Maione S, Bisogno T, de Novellis V, Palazzo E, Cristino L, Valenti M, Petrosino S, Guglielmotti V, Rossi F, Di Marzo V, J Pharmacol Exp Ther 2006 316 3 969 982 16284279
77. Tonic endovanilloid facilitation of glutamate release in brainstem descending antinociceptive pathways. Starowicz K, Maione S, Cristino L, Palazzo E, Marabese I, Rossi F, de Novellis V, Di Marzo V, J Neurosci 2007 27 50 13739 13749 10.1523/JNEUROSCI.3258-07.2007 18077685
78. 17-Beta-estradiol enhanced allodynia of inflammatory temporomandibular joint through upregulation of hippocampal TRPV1 in ovariectomized rats. Wu YW, Bi YP, Kou XX, Xu W, Ma LQ, Wang KW, Gan YH, Ma XC, J Neurosci 2010 30 26 8710 8719 10.1523/JNEUROSCI.6323-09.2010 20592193
79. Extensive co-localization and heteromultimer formation of the vanilloid receptor-like protein TRPV2 and the capsaicin receptor TRPV1 in the adult rat cerebral cortex. Liapi A, Wood JN, Eur J Neurosci 2005 22 4 825 834 10.1111/j.1460-9568.2005.04270.x 16115206
80. Molecular mechanisms of pain in the anterior cingulate cortex. Zhuo M, J Neurosci Res 2006 84 5 927 933 10.1002/jnr.21003 16862566
81. Neuronal mechanism for neuropathic pain. Zhuo M, Mol Pain 2007 3 14 10.1186/1744-8069-3-14 17553143
82. Nonnociceptive afferent activity depresses nocifensive behavior and nociceptive synapses via an endocannabinoid-dependent mechanism. Yuan S, Burrell BD, J Neurophysiol 2013 110 11 2607 2616 10.1152/jn.00170.2013 24027102
83. Brain TRPV1: a depressing TR(i)P down memory lane? Di Marzo V, Gobbi G, Szallasi A, Trends Pharmacol Sci 2008 29 12 594 600 10.1016/j.tips.2008.09.004 18947889
84. A synaptic model for pain: long-term potentiation in the anterior cingulate cortex. Zhuo M, Mol Cells 2007 23 3 259 271 17646700
85. Investigation of molecular mechanism of chronic pain in the anterior cingulate cortex using genetically engineered mice. Kim SS, Descalzi G, Zhuo M, Curr Genomics 2010 11 1 70 76 10.2174/138920210790217990 20808527
86. Estrogen in the anterior cingulate cortex contributes to pain-related aversion. Xiao X, Yang Y, Zhang Y, Zhang XM, Zhao ZQ, Zhang YQ, Cereb Cortex 2013 23 9 2190 2203 10.1093/cercor/bhs201 22784608
87. GABAA but not GABAB receptors in the rostral anterior cingulate cortex selectively modulate pain-induced escape/avoidance behavior. LaGraize SC, Fuchs PN, Exp Neurol 2007 204 1 182 194 10.1016/j.expneurol.2006.10.007 17141761
88. Descending facilitatory modulation of a behavioral nociceptive response by stimulation in the adult rat anterior cingulate cortex. Calejesan AA, Kim SJ, Zhuo M, Eur J Pain 2000 4 1 83 96 10.1053/eujp.1999.0158 10833558
89. The vanilloid receptor TRPV1: 10 years from channel cloning to antagonist proof-of-concept. Szallasi A, Cortright DN, Blum CA, Eid SR, Nat Rev Drug Discov 2007 6 5 357 372 10.1038/nrd2280 17464295