Transcutaneous electrical nerve stimulation at both high and low frequencies activates ventrolateral periaqueductal grey to decrease mechanical hyperalgesia in arthritic rats

Neuroscience

Volumn 163, Issue 4, 2009, Pages 1233-1241

  Desantana, J M ^a   Da Silva, L F S ^b   De Resende, M A ^c   Sluka, K A ^b  

^a FEDERAL UNIVERSITY OF SERGIPE   (Brazil)

^b UNIVERSITY OF IOWA   (United States)

^c FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

Author keywords

Analgesia; Hyperalgesia; Inflammation; Opioid; Pain; TENS

Indexed keywords

COBALT CHLORIDE; CENTRAL NERVOUS SYSTEM AGENTS; COBALT;

ADULT ANIMAL; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; HYPERALGESIA; KNEE ARTHRITIS; KNEE PAIN; MALE; MEDULLA OBLONGATA; NONHUMAN; PAIN THRESHOLD; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; RAT; TRANSCUTANEOUS NERVE STIMULATION; VENTROLATERAL PERIAQUEDUCTAL GRAY MATTER; ANIMAL; ARTHRITIS; DRUG EFFECT; INFLAMMATION; KNEE; METHODOLOGY; MICROINJECTION; PAIN; PAIN ASSESSMENT; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT; STIMULATION; TIME;

ANIMALS; ARTHRITIS; CENTRAL NERVOUS SYSTEM AGENTS; COBALT; INFLAMMATION; KNEE JOINT; MALE; MICROINJECTIONS; PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; PERIAQUEDUCTAL GRAY; PHYSICAL STIMULATION; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS; TRANSCUTANEOUS ELECTRIC NERVE STIMULATION;

EID: 75149191404     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.06.056     Document Type: Article

References (78)

1. Bagley EE, Chieng BC, Christie MJ, Connor M (2005) Opioid tolerance in periaqueductal gray neurons isolated from mice chronically treated with morphine. Br J Pharmacol 146(1):68-76.
2. Basbaum AI, Fields HL (1984) Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu Rev Neurosci 7:309-338.
3. Behbehani MM (1995) Functional characteristics of the midbrain periaqueductal gray. Prog Neurobiol 46:575-605.
4. Burgess SE, Gardell LR, Ossipov MH, Malan TP Jr, Vanderah TW, Lai J, Porreca F (2002) Time-dependent descending facilitation from the rostral ventromedial medulla maintains, but does not initiate, neuropathic pain. J Neurosci 22(12):5129-5136.
5. Cannon JT, Prieto GJ, Lee A, Liebeskind JC (1982) Evidence for opioid and non-opioid forms of stimulation-produced analgesia in the rat. Brain Res 243:315-321.
6. Castiglioni AJ, Gallaway MC, Coulter JD (1978) Spinal projections from the midbrain in monkey. J Comp Neurol 178:329-346.
7. Cavun S, Goktalay G, Millington WR (2004) The hypotension evoked by visceral nociception is mediated by delta opioid receptors in the periaqueductal gray. Brain Res 1019(1-2):237-245.
8. Chandran P, Sluka KA (2003) Development of opioid tolerance with repeated transcutaneous electrical nerve stimulation administration. Pain 102(1-2):195-201.
9. Cheng ZF, Fields HL, Heinricher MM (1986) Morphine microinjected into the periaqueductal gray has differential effects on 3 classes of medullary neurons. Brain Res 375(1):57-65.
10. DeSantana JM, Santana-Filho VJ, Sluka KA (2008) Modulation between high- and low-frequency transcutaneous electric nerve stimulation delays the development of analgesic tolerance in arthritic rats. Arch Phys Med Rehabil 89(4):754-760.
11. Fields HL, Heinricher MM, Mason P (1991) Neurotransmitters in nociceptive modulatory circuits. Annu Rev Neurosci 14:219-245.
12. Fisk GD, Wyss JM (2000) Descending projections of infralimbic cortex that mediate stimulation-evoked changes in arterial pressure. Brain Res 859(1):83-95.
13. Gebhart GF, Jones SL, Besson JM (1988) Effects of morphine given in the brain stem on the activity of dorsal horn nociceptive neurons. In: Progress in brain research: pain modulation (Fields HL, ed), pp 229-243. Amsterdam: Elsevier.
14. Gopalkrishnan P, Sluka KA (2000) Effect of varying frequency, intensity, and pulse duration of transcutaneous electrical nerve stimulation on primary hyperalgesia in inflamed rats. Arch Phys Med Rehabil 81(7):984-990.
15. Guan Y, Guo W, Robbins MT, Dubner R, Ren K (2004) Changes in AMPA receptor phosphorylation in the rostral ventromedial medulla after inflammatory hyperalgesia in rats. Neurosci Lett 366(2): 201-205.
16. Guo W, Robbins MT, Wei F, Zou S, Dubner R, Ren K (2006) Supraspinal brain-derived neurotrophic factor signaling: a novel mechanism for descending pain facilitation. J Neurosci 26(1):126-137.
17. Hagiwara S, Byerly L (1981) Calcium channel. Annu Rev Neurosci 4:69-125.
18. Han JS, Chen XH, Sun SL, Xu XJ, Yuan Y, Yan SC, Hao JX, Terenius L (1991) Effect of low and high frequency TENS on met-enkephalin-arg-phe and dynorphin a immunoreactivity in human lumbar CSF. Pain 47:295-298.
19. Heinricher MM, Martenson ME, Neubert MJ (2004) Prostaglandin E2 in the midbrain periaqueductal gray produces hyperalgesia and activates pain-modulating circuitry in the rostral ventromedial medulla. Pain 110(1-2):419-426.
20. Hingne PM, Sluka KA (2008) Blockade of NMDA receptors prevents analgesic tolerance to repeated transcutaneous electrical nerve stimulation (TENS) in rats. J Pain 9(3):217-225.
21. Hosobuchi Y, Adams JE, Linchitz R (1977) Pain relief by electrical stimulation of the central gray matter in humans and its reversal by naloxone. Science 197:183-186.
22. Jacquet YF, Lajtha A (1976) The periaqueductal gray: site of morphine analgesia and tolerance as shown by 2-way cross tolerance between systemic and intracerebral injections. Brain Res 103:501-513.
23. Jensen TS, Yaksh TL (1989) Comparison of the antinociceptive effect of morphine and glutamate at coincidental sites in the periaqueductal gray and medial medulla in rats. Brain Res 476(1):1-9.
24. Jensen TS, Yaksh TL (1986) Comparison of the antinociceptive action of mu and delta opioid receptor ligands in the periaqueductal gray matter, medial and paramedial ventral medulla in the rats as studied by the microinjection technique. Brain Res 372:301-312.
25. Kalra A, Urban MO, Sluka KA (2001) Blockade of opioid receptors in rostral ventral medulla prevents antihyperalgesia produced by transcutaneous electrical nerve stimulation (TENS). J Pharmacol Exp Ther 298(1):257-263.
26. Kiefel JM, Rossi GC, Bodnar RJ (1993) Medullary mu and delta opioid receptors modulate mesencephalic morphine analgesia in rats. Brain Res 624(1-2):151-161.
27. King EW, Audette K, Athman GA, Nguyen HO, Sluka KA, Fairbanks CA (2005) Transcutaneous electrical nerve stimulation activates peripherally located alpha-2A adrenergic receptors. Pain 115(3): 364-373.
28. Kretz R (1984) Local cobalt injection: a method to discriminate presynaptic axonal from postsynaptic neuronal activity. J Neurosci Methods 11(2):129-135.
29. Krzanowska EK, Bodnar RJ (1999) Morphine antinociception elicited from the ventrolateral periaqueductal gray is sensitive to sex and gonadectomy differences in rats. Brain Res 821:224-230.
30. Kuypers HGJM, Maisky VA (1975) Retrograde axonal transport of horseradish peroxidase from spinal cord to brainstem cell groups in cats. Neurosci Lett 1:9-14.
31. Lewis VA, Gebhart GF (1977) Morphine-induced and stimulation-produced analgesias at coincident periaqueductal central gray loci: evaluation of analgesic congruence, tolerance, and cross-tolerance. Exp Neurol 57:934-955.
32. Ma YT, Sluka KA (2001) Reduction in inflammation-induced sensitization of dorsal horn neurons by transcutaneous electrical nerve stimulation in anesthetized rats. Exp Brain Res 137(1):94-102.
33. Maeda Y, Lisi TL, Vance CG, Sluka KA (2007) Release of GABA and activation of GABA(A) in the spinal cord mediates the effects of TENS in rats. Brain Res 1136(1):43-50.
34. Mantyh PW, Peschanski M (1982) Spinal projections from the periaqueductal grey and dorsal raphe in the rat, cat and monkey. Neuroscience 7(11):2769-2776.
35. Morgan MM, Clayton CC, Boyer-Quick JS (2005a) Differential susceptibility of the PAG and RVM to tolerance to the antinociceptive effect of morphine in the rat. Pain 113:91-98.
36. Morgan MM, Depaulis A, Liebeskind JC (1987) Diazepam dissociates the analgesic and aversive effects of periaqueductal gray stimulation in the rats. Brain Res 423(1-2):395-398.
37. Morgan MM, Tierney BW, Ingram SL (2005b) Intermittent dosing prolongs tolerance to the antinociceptive effect of morphine microinjection into the periaqueductal gray. Brain Res 1059:173-178.
38. Morgan MM (1991) Differences in antinociception evoked from dorsal and ventral regions of the caudal periaqueductal gray matter. In: The midbrain periaqueductal gray mattered (DePaulis A, Bandler R, eds), pp 139-150. New York: Plenum.
39. Morgan MM, Whitney PK (2000) Immobility accompanies the antinociception mediated by the rostral ventromedial medulla of the rat. Brain Res 872(1-2):276-281.
40. Morgan MM, Whitney PK, Gold MS (1998) Immobility and flight associated with antinociception produced by activation of the ventral and lateral/dorsal regions of the rat periaqueductal gray. Brain Res 804:159-166.
41. Morgan MM, Sohn JH, Liebeskind JC (1989) Stimulation of the periaqueductal gray matter inhibits nociception at the supraspinal as well as spinal level. Brain Res 502:61-66.
42. Nuseir K, Heidenreich BA, Proudfit HK (1999) The antinociception produced by microinjection of a cholinergic agonist in the ventromedial medulla is mediated by noradrenergic neurons in the A7 catecholamine cell group. Brain Res 822:1-7.
43. Oliveras JL, Besson JM, Guilbaud G, Liebeskind JC (1974) Behavioral and electrophysiological evidence of pain inhibition from midbrain stimulation in the cat. Exp Brain Res 20:32-44.
44. Osborne PB, Vaughan CW, Wilson HI, Christie MJ (1996) Opioid inhibition of rat periaqueductal grey neurones with identified projections to rostral ventromedial medulla in vitro. J Physiol 490(2): 383-389.
45. Pajolla GP, Tavares RF, Pelosi GG, Corrêa FM (2005) Involvement of the periaqueductal gray in the hypotensive response evoked by L-glutamate microinjection in the lateral hypothalamus of unanesthetized rats. Auton Neurosci 122(1-2):84-93.
46. Paxinos G, Watson SJ (2005) The rat brain, in stereotaxic coordinates. San Diego: Elsevier Academic Press.
47. Prieto GJ, Cannon JT, Liebeskind JC (1983) N. raphe magnus lesions disrupt stimulation-produced analgesia from ventral but not dorsal midbrain areas in the rat. Brain Res 261:53-57.
48. Radhakrishnan R, Moore SA, Sluka KA (2003) Unilateral carrageenan injection into muscle or joint induces chronic bilateral hyperalgesia in rats. Pain 104(3):567-577.
49. Radhakrishinan R, Sluka KA (2003) Spinal muscarinic receptors are activated during low and high frequency TENS-induced antihyperalgesia in rats. Neuropharmacology 45:1111-1119.
50. Reichling DB, Basbaum AI (1991) Collateralization of periaqueductal gray neurons to forebrain or diencephalon and to the medullary nucleus raphe magnus in the rat. Neuroscience 42(1):183-200.
51. Resende MA, Sabino GG, Cândido CR, Pereira LS, Francischi JN (2004) Local transcutaneoous electrical stimulation (TENS) effects in experimental inflammatory edema and pain. Eur J Pharmacol 504(3):217-222.
52. Rossi GC, Pasternak GW, Bodnar RJ (1994) Mu and delta opioid synergy between the periaqueductal gray and the rostro-ventral medulla. Brain Res 665:85-93.
53. Salar G, Job I, Mingrino S, Bosio A, Trabucchi M (1981) Effect of transcutaneous electrotherapy on CSF β-endorphin content in patients without pain problems. Pain 10:169-172.
54. Sandkuhler J, Gebhart GF (1984) Relative contributions of the nucleus raphe magnus and adjacent medullary reticular formation to the inhibition by stimulation in the periaqueductal gray of a spinal nociceptive reflex in the pentobarbital-anesthetized rat. Brain Res 305:77-87.
55. Siuciak JA, Advokat C (1987) Tolerance to morphine microinjections in the periaqueductal gray (PAG) induces tolerance to systemic, but not intrathecal morphine. Brain Res 424:311-319.
56. Sjolund BH, Eriksson MB (1979) The influence of naloxone on analgesia produced by peripheral conditioning stimulation. Brain Res 173(2):295-301.
57. Sluka KA, Deacon M, Stibal A, Strissel S, Terpstra A (1999) Spinal blockade of opioid receptors prevents the analgesia produced by TENS in arthritic rats. J Pharmacol Exp Ther 289(2):840-846.
58. Sluka KA, Lisi TL, Westlund KN (2006) Increased release of serotonin in the spinal cord during low, but not high, frequency transcutaneous electric nerve stimulation in rats with joint inflammation. Arch Phys Med Rehabil 87(8):1137-1140.
59. Sluka KA, Bailey K, Bogush J, Olson R, Ricketts A (1998) Treatment with either high or low frequency TENS reduces the secondary hyperalgesia observed after injection of kaolin and carrageenan into the knee joint. Pain 77(1):97-102.
60. Sluka KA, Judge MA, McColley MM, Reveiz PM, Taylor BM (2000) Low frequency TENS is less effective than high frequency TENS at reducing inflammation-induced hyperalgesia in morphine-tolerant rats. Eur J Pain 4(2):185-193.
61. Sluka KA, Chandran P (2002) Enhanced reduction in hyperalgesia by combined administration of clonidine and TENS. Pain 100(1-2): 183-190.
62. Sluka KA (2000) Systemic morphine in combination with TENS produces an increased antihyperalgesia in rats with acute inflammation. J Pain 1(3):204-211.
63. Sluka KA, Westlund KN (1993) Behavioral and immunohistochemical changes in an experimental arthritis model in rats. Pain 55(3): 367-377.
64. Spinella M, Cooper ML, Bodnar RJ (1996) Excitatory amino acid antagonists in the rostral ventromedial medulla inhibit mesencephalic morphine analgesia in rats. Pain 64(3):545-552.
65. Sugiyo S, Takemura M, Dubner R, Ren K (2005) Trigeminal transition zone/rostral ventromedial medulla connections and facilitation of orofacial hyperalgesia after masseter inflammation in rats. J Comp Neurol 493(4):510-523.
66. Tershner SA, Helmstetter FJ (2000) Antinociception produced by mu opioid receptor activation in the amygdala is partly dependent on activation of mu opioid and neurotensin receptors in the ventral periaqueductal gray. Brain Res 865(1):17-26.
67. Tershner SA, Mitchell JM, Fields HL (2000) Brainstem pain modulating circuitry is sexually dimorphic with respect to mu and kappa opioid receptor function. Pain 85:153-159.
68. Tortorici V, Morgan MM, Vanegas H (2001) Tolerance to repeated microinjection of morphine into the periaqueductal gray is associated with changes in the behavior of off- and on-cells in the rostral ventromedial medulla of rats. Pain 89:237-244.
69. Tortorici VT, Robbins CS, Morgan MM (1999) Tolerance to the antinociceptive effect of morphine microinjections into the ventral but not lateral-dorsal periaqueductal gray of the rat. Behav Neurosci 113:833-839.
70. Urban MO, Smith DJ (1994) Nuclei within the rostral ventromedial medulla mediating morphine antinociception from the periaqueductal gray. Brain Res 652(1):9-16.
71. Urban MO, Jiang MC, Gebhart GF (1996) Participation of central descending nociceptive facilitatory systems in secondary hyperalgesia produced by mustard oil. Brain Res 737(1-2):83-91.
72. Vance CG, Radhakrishnan R, Skyba DA, Sluka KA (2007) Transcutaneous electrical nerve stimulation at both high and low frequencies reduces primary hyperalgesia in rats with joint inflammation in a time-dependent manner. Phys Ther 87(1):44-51.
73. Vaughan CW, Christie MJ (1997) Presynaptic inhibitory action of opioids on synaptic transmission in the rat periaqueductal grey in vitro. J Physiol 498(2):463-472.
74. Vera-Portocarrero LP, Xie JY, Kowal J, Ossipov MH, King T, Porreca F (2006) Descending facilitation from the rostral ventromedial medulla maintains visceral pain in rats with experimental pancreatitis. Gastroenterology 130(7):2155-2164.
75. Yaksh TL, Yeung JC, Rudy TA (1976) Systematic examination in the rat of brain sites sensitive to the direct application of morphine: observation of differential effects within the periaqueductal gray. Brain Res 114:83-103.
76. Zhuo M, Gebhart GF (2002) Facilitation and attenuation of a visceral nociceptive reflex from the rostroventral medulla in the rat. Gastroenterology 122(4):1007-1019.
77. Zhuo M, Gebhart GF (1991) Spinal serotonin receptors mediate descending facilitation of a nociceptive reflex from the nuclei reticularis gigantocellularis and gigantocellularis pars alpha in the rat. Brain Res 550(1):35-48.
78. Zhuo M, Gebhart GF (1997) Biphasic modulation of spinal nociceptive transmission from the medullary raphe nuclei in the rat. J Neurophysiol 78(2):746-758.