Motor cortex and pain control: exploring the descending relay analgesic pathways and spinal nociceptive neurons in healthy conscious rats

Imagem de Miniatura
Arquivos
art_LOPES_Motor_cortex_and_pain_control_exploring_the_descending_2019.PDF (2.57 MB)
Citações na Scopus
25
Tipo de produção
article
Data de publicação
2019
DOI
Scopus
Web of Science
PubMed
Título da Revista
ISSN da Revista
Título do Volume
Editora
BMC
Autores
LOPES, Patricia Sanae Souza
CAMPOS, Ana Carolina Pinheiro
BRITTO, Luiz Roberto Giorgetti
PAGANO, Rosana Lima
Citação
BEHAVIORAL AND BRAIN FUNCTIONS, v.15, article ID 5, 13p, 2019
Projetos de Pesquisa
Unidades Organizacionais
Fascículo
Resumo
Motor cortex stimulation (MCS) is an effective therapy for refractory neuropathic pain. MCS increases the nociceptive threshold in healthy rats via endogenous opioids, inhibiting thalamic nuclei and activating the periaqueductal gray. It remains unclear how the motor cortex induces top-down modulation of pain in the absence of persistent pain. Here, we investigated the main nuclei involved in the descending analgesic pathways and the spinal nociceptive neurons in rats that underwent one session of MCS and were evaluated with the paw pressure nociceptive test. The pattern of neuronal activation in the dorsal raphe nucleus (DRN), nucleus raphe magnus (NRM), locus coeruleus (LC), and dorsal horn of the spinal cord (DHSC) was assessed by immunoreactivity (IR) for Egr-1 (a marker of activated neuronal nuclei). IR for serotonin (5HT) in the DRN and NRM, tyrosine hydroxylase (TH) in the LC, and substance P (SP) and enkephalin (ENK) in the DHSC was also evaluated. MCS increased the nociceptive threshold of the animals; this increase was accompanied by activation of the NRM, while DRN activation was unchanged. However, cortical stimulation induced an increase in 5HT-IR in both serotonergic nuclei. MCS did not change the activation pattern or TH-IR in the LC, and it inhibited neuronal activation in the DHSC without altering SP or ENK-IR. Taken together, our results suggest that MCS induces the activation of serotonergic nuclei as well as the inhibition of spinal neurons, and such effects may contribute to the elevation of the nociceptive threshold in healthy rats. These results allow a better understanding of the circuitry involved in the antinociceptive top-down effect induced by MCS under basal conditions, reinforcing the role of primary motor cortex in pain control.
Palavras-chave
Motor cortex, Neurostimulation, Antinociception, Raphe nuclei, Spinal cord
URI
https://observatorio.fm.usp.br/handle/OPI/31745
Referências
  1. Allen BJ, 1997, J NEUROSCI, V17, P5921
  2. BASBAUM AI, 1984, ANNU REV NEUROSCI, V7, P309, DOI 10.1146/annurev.ne.07.030184.001521
  3. Basbaum AI, 1999, REGION ANESTH PAIN M, V24, P59, DOI 10.1016/S1098-7339(99)90167-0
  4. Basbaum AI, 2009, CELL, V139, P267, DOI 10.1016/j.cell.2009.09.028
  5. Bruinstroop E, 2012, J COMP NEUROL, V520, P1985, DOI 10.1002/cne.23024
  6. Budai D, 1998, J NEUROPHYSIOL, V79, P677
  7. BURITOVA J, 1995, BRAIN RES, V674, P211, DOI 10.1016/0006-8993(95)00009-F
  8. Cha M, 2013, J PAIN, V14, P260, DOI 10.1016/j.jpain.2012.11.007
  9. Dahlstroem A., 1964, ACTA PHYSL SCAND S, V232, P231
  10. FIELDS HL, 1991, ANNU REV NEUROSCI, V14, P219, DOI 10.1146/annurev.ne.14.030191.001251
  11. Fields HL, 2006, WALL MELLZACKS TXB P, P125
  12. Fonoff ET, 2011, STEREOT FUNCT NEUROS, V89, P167, DOI 10.1159/000324895
  13. Fonoff ET, 2009, BEHAV BRAIN RES, V202, P138, DOI 10.1016/j.bbr.2009.03.018
  14. Fonoff ET, 2009, BEHAV BRAIN RES, V196, P63, DOI 10.1016/j.bbr.2008.07.027
  15. Fontaine D, 2009, J NEUROSURG, V110, P251, DOI 10.3171/2008.6.17602
  16. Franca NRM, 2013, BEHAV BRAIN RES, V250, P211, DOI 10.1016/j.bbr.2013.05.019
  17. Francois A, 2017, NEURON, V93, P822, DOI 10.1016/j.neuron.2017.01.008
  18. Freitas RL, 2008, EXP NEUROL, V213, P410, DOI 10.1016/j.expneurol.2008.07.003
  19. Fu WY, 2010, J COMP NEUROL, V518, P3464, DOI 10.1002/cne.22407
  20. Garcia-Larrea L, 1999, PAIN, V83, P259, DOI 10.1016/S0304-3959(99)00114-1
  21. Garcia-Larrea L, 2007, NEUROIMAGE, V37, pS71, DOI 10.1016/j.neuroimage.2007.05.062
  22. Gilbert AK, 2001, PAIN, V90, P25, DOI 10.1016/S0304-3959(00)00383-3
  23. Gjerstad J, 1996, EUR J PHARMACOL, V318, P315, DOI 10.1016/S0014-2999(96)00819-9
  24. GOGAS KR, 1991, NEUROSCIENCE, V42, P617, DOI 10.1016/0306-4522(91)90031-I
  25. Green GM, 1998, EUR J PHARMACOL, V347, P201, DOI 10.1016/S0014-2999(98)00217-9
  26. Harris JA, 1998, BRAIN RES BULL, V45, P1, DOI 10.1016/S0361-9230(97)00277-3
  27. HEINRICHER MM, 1994, NEUROSCIENCE, V63, P533, DOI 10.1016/0306-4522(94)90548-7
  28. HERDEGEN T, 1991, J COMP NEUROL, V313, P178, DOI 10.1002/cne.903130113
  29. Herdegen T, 1998, BRAIN RES REV, V28, P370, DOI 10.1016/S0165-0173(98)00018-6
  30. HERDEGEN T, 1990, NEUROSCI LETT, V120, P21, DOI 10.1016/0304-3940(90)90158-6
  31. HOKFELT T, 1975, SCIENCE, V190, P889, DOI 10.1126/science.242075
  32. HOKFELT T, 1977, P NATL ACAD SCI USA, V74, P3081, DOI 10.1073/pnas.74.7.3081
  33. Howorth PW, 2009, J COMP NEUROL, V512, P141, DOI 10.1002/cne.21879
  34. Hoyer D, 2002, PHARMACOL BIOCHEM BE, V71, P533, DOI 10.1016/S0091-3057(01)00746-8
  35. HUNT SP, 1987, NATURE, V328, P632, DOI 10.1038/328632a0
  36. JACOBS BL, 1992, PHYSIOL REV, V72, P165
  37. JONES SL, 1991, PROG BRAIN RES, V88, P381
  38. LANTERIMINET M, 1993, NEUROSCIENCE, V55, P737, DOI 10.1016/0306-4522(93)90439-M
  39. Lefaucheur JP, 2010, EXP NEUROL, V223, P609, DOI 10.1016/j.expneurol.2010.02.008
  40. LEVINE JD, 1993, J NEUROSCI, V13, P2273
  41. Li P, 2001, BRAIN RES BULL, V54, P639, DOI 10.1016/S0361-9230(01)00470-1
  42. Lima MC, 2008, NEUROLOGY, V70, P2329, DOI 10.1212/01.wnl.0000314649.38527.93
  43. Llorca-Torralba M, 2016, NEUROSCIENCE, V338, P93, DOI 10.1016/j.neuroscience.2016.05.057
  44. Lopez WOC, 2016, PAIN PHYSICIAN, V19, pE631
  45. Lucas JM, 2011, PAIN, V152, P1398, DOI 10.1016/j.pain.2011.02.025
  46. Luo MM, 2015, LEARN MEMORY, V22, P452, DOI 10.1101/lm.037317.114
  47. Maarrawi J, 2007, NEUROLOGY, V69, P827, DOI 10.1212/01.wnl.0000269783.86997.37
  48. Maarrawi J, 2013, PAIN, V154, P2563, DOI 10.1016/j.pain.2013.07.042
  49. Mantyh PW, 2002, J CLIN PSYCHIAT, V63, P6
  50. Mantyh PW, 1997, SCIENCE, V278, P275, DOI 10.1126/science.278.5336.275
  51. MANTYH PW, 1995, P NATL ACAD SCI USA, V92, P2622, DOI 10.1073/pnas.92.7.2622
  52. Marshall GE, 1996, NEUROSCIENCE, V72, P255, DOI 10.1016/0306-4522(95)00558-7
  53. Marvizon JCG, 2003, NEUROSCIENCE, V118, P535, DOI 10.1016/S0306-4522(02)00977-6
  54. Mason P, 1997, J NEUROPHYSIOL, V77, P1087
  55. Millan MJ, 2002, PROG NEUROBIOL, V66, P355, DOI 10.1016/S0301-0082(02)00009-6
  56. MOLANDER C, 1984, J COMP NEUROL, V230, P133, DOI 10.1002/cne.902300112
  57. MORGAN JI, 1989, TRENDS NEUROSCI, V12, P459, DOI 10.1016/0166-2236(89)90096-9
  58. Muto Y, 2012, BRIT J PHARMACOL, V166, P1047, DOI 10.1111/j.1476-5381.2011.01820.x
  59. Nguyen JP, 2008, BRAIN STIMUL, V1, P89, DOI 10.1016/j.brs.2008.03.007
  60. Nguyen JP, 1999, PAIN, V82, P245, DOI 10.1016/S0304-3959(99)00062-7
  61. Nichols ML, 1999, SCIENCE, V286, P1558, DOI 10.1126/science.286.5444.1558
  62. Nuti C, 2005, PAIN, V118, P43, DOI 10.1016/j.pain.2005.07.020
  63. Ossipov MH, 2010, J CLIN INVEST, V120, P3779, DOI 10.1172/JCI43766
  64. Pagano RL, 2012, PAIN, V153, P2359, DOI 10.1016/j.pain.2012.08.002
  65. Pagano RL, 2011, EUR J PAIN, V15, DOI 10.1016/j.ejpain.2010.08.003
  66. Palazzo E, 2006, EUR J NEUROSCI, V24, P2011, DOI 10.1111/j.1460-9568.2006.05086.x
  67. Paxinos G., 2007, RAT BRAIN STEREOTAXI
  68. Pertovaara A, 2006, PROG NEUROBIOL, V80, P53, DOI 10.1016/j.pneurobio.2006.08.001
  69. Pertovaara A, 2013, EUR J PHARMACOL, V716, P2, DOI 10.1016/j.ejphar.2013.01.067
  70. PEYRON R, 1995, PAIN, V62, P275, DOI 10.1016/0304-3959(94)00211-V
  71. Peyron R, 2007, NEUROIMAGE, V34, P310, DOI 10.1016/j.neuroimage.2006.08.037
  72. PROUDFIT HK, 1991, PROG BRAIN RES, V88, P123
  73. RANDALL LO, 1957, ARCH INT PHARMACOD T, V111, P409
  74. Rasche D, 2006, PAIN, V121, P43, DOI 10.1016/j.pain.2005.12.006
  75. Rojas-Piloni G, 2010, BRAIN RES, V1351, P104, DOI 10.1016/j.brainres.2010.06.010
  76. RUDA MA, 1982, SCIENCE, V215, P1523, DOI 10.1126/science.6121374
  77. RUDA MA, 1986, PROG BRAIN RES, V66, P219, DOI 10.1016/S0079-6123(08)64606-3
  78. Rusina R, 2005, NEUROENDOCRINOL LETT, V26, P283
  79. Salas R, 2016, BRAIN RES, V1652, P103, DOI 10.1016/j.brainres.2016.10.001
  80. Senapati AK, 2005, BRAIN RES, V1036, P173, DOI 10.1016/j.jbrainres.2004.12.043
  81. SEYBOLD V, 1980, J HISTOCHEM CYTOCHEM, V28, P367, DOI 10.1177/28.4.6154731
  82. Seybold V S, 2009, Handb Exp Pharmacol, P451, DOI 10.1007/978-3-540-79090-7_13
  83. SHENG M, 1990, NEURON, V4, P477, DOI 10.1016/0896-6273(90)90106-P
  84. Soiza-Reilly M, 2014, FRONT NEURAL CIRCUIT, V8, DOI 10.3389/fncir.2014.00105
  85. Suzuki R, 2004, TRENDS PHARMACOL SCI, V25, P613, DOI 10.1016/j.tips.2004.10.002
  86. Tao R, 2003, BRAIN RES, V961, P109, DOI 10.1016/S0006-8993(02)03851-9
  87. Tazawa T, 2015, MOL PAIN, V11, DOI 10.1186/s12990-015-0039-9
  88. Teixeira Manoel Jacobsen, 2013, Acta Neurochir Suppl, V117, P73, DOI 10.1007/978-3-7091-1482-7_12
  89. Todd AJ, 2002, J NEUROSCI, V22, P4103, DOI 10.1523/JNEUROSCI.22-10-04103.2002
  90. Todd AJ, 2017, MOL PAIN, V13, P1, DOI 10.1177/1744806917693003
  91. Todd AJ, 2010, NAT REV NEUROSCI, V11, P823, DOI 10.1038/nrn2947
  92. TORK I, 1990, ANN NY ACAD SCI, V600, P9
  93. Tsubokawa T, 1991, Acta Neurochir Suppl (Wien), V52, P137
  94. Tsuruoka M, 2003, PAIN, V104, P353, DOI 10.1016/S0304-3959(03)00042-3
  95. Tsuruoka M, 2012, FRONT INTEGR NEUROSC, V6, DOI 10.3389/fnint.2012.00087
  96. Vaculin S, 2008, EXP BRAIN RES, V185, P331, DOI 10.1007/s00221-007-1158-y
  97. Velasco F, 2008, J NEUROSURG, V108, P698, DOI 10.3171/JNS/2008/108/4/0698
  98. Viisanen H, 2012, BRAIN RES BULL, V89, P133, DOI 10.1016/j.brainresbull.2012.08.002
  99. Viisanen H, 2010, NEUROSCI LETT, V476, P133, DOI 10.1016/j.neulet.2010.04.014
  100. Viisanen H, 2010, EXP BRAIN RES, V201, P283, DOI 10.1007/s00221-009-2038-4
  101. WANG QP, 1994, BRAIN RES BULL, V34, P575
  102. Wei F, 2010, J NEUROSCI, V30, P8624, DOI 10.1523/JNEUROSCI.5389-09.2010
  103. WESTLUND KN, 1983, BRAIN RES, V263, P15, DOI 10.1016/0006-8993(83)91196-4
  104. Wu YY, 2017, EXP THER MED, V14, P107, DOI 10.3892/etm.2017.4479
  105. Yasaka T, 2010, PAIN, V151, P475, DOI 10.1016/j.pain.2010.08.008
  106. Yoshimura M, 2006, J PHARMACOL SCI, V101, P107, DOI 10.1254/jphys.CRJ06008X
  107. Zhang C, 1997, BRAIN RES BULL, V42, P273, DOI 10.1016/S0361-9230(96)00262-6
  108. ZIMMERMANN M, 1983, PAIN, V16, P109, DOI 10.1016/0304-3959(83)90201-4

Coleções
Artigos e Materiais de Revistas Científicas - FM/MNE
Artigos e Materiais de Revistas Científicas - HC/IPq
Artigos e Materiais de Revistas Científicas - LIM/45