Brainstem modulation of pain during sleep and waking

Sleep Medicine Reviews

Volumn 7, Issue 2, 2003, Pages 145-154

  Foo, H ^a   Mason, Peggy ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Behavioral state; Nociception; Raphe magnus; Serotonin

Indexed keywords

ALERTNESS; AROUSAL; BEHAVIOR; BRAIN STEM; CHRONIC PAIN; EVOKED BRAIN STEM RESPONSE; HUMAN; NERVE CELL; NERVE STIMULATION; NONHUMAN; REVIEW; SEROTONINERGIC SYSTEM; SLEEP WAKING CYCLE; STIMULUS RESPONSE; WAKEFULNESS;

EID: 0037375504     PISSN: 10870792     EISSN: None     Source Type: Journal    
DOI: 10.1053/smrv.2002.0224     Document Type: Review

References (77)

1. Becker N, Bondegaard Thomsen A, Olsen AK et al. Pain epidemiology and health related quality of life in chronic non-malignant pain patients referred to a Danish multidisciplinary pain center. Pain 1997; 73: 393-400.
2. Drewes AM, Jennum P, Andreasen A et al. Self-reported sleep disturbances and daytime complaints in women with fibromyalgia and rheumatoid arthritis. J Musculoskel Pain 1994; 2: 15-31.
3. Galer BS, Gianas A, Jensen MP. Painful diabetic polyneuropathy: epidemiology, pain description, and quality of life. Diabetes Res Clin Pract 2000; 47: 123-128.
4. Gudbjornsson B, Broman JE, Hetta J et al. Sleep disturbances in patients with primary Sjogren's syndrome. Br J Rheumatol 1993; 32: 1072-1076.
5. Hagen KB, Kvien TK, Bjorndal A. Musculoskeletal pain and quality of life in patients with noninflammatory joint pain compared to rheumatoid arthritis: a population survey. J Rheumatol 1997; 24: 1703-1709.
6. Hart FD, Taylor RT, Huskisson EC. Pain at night. Lancet 1970; 1: 881-884.
7. Jones SD, Koh WH, Steiner A et al. Fatigue in ankylosing spondylitis: its prevalence and relationship to disease activity, sleep, and other factors. J Rheumatol 1996; 23: 487-490.
8. Lavsky-Shulan M, Wallace RB, Kohout FJ et al. Prevalence and functional correlates of low back pain in the elderly: the Iowa 65+ Rural Health Study. J Am Geriatr Soc 1985; 33: 23-28.
9. Locker D, Grushka M. The impact of dental and facial pain. J Dent Res 1987; 66: 1414-1417.
10. Morin CM, Gibson D, Wade J. Self-reported sleep and mood disturbance in chronic pain patients. Clin J Pain 1998; 14: 311-314.
11. Portenoy RK, Miransky J, Thaler HT et al. Pain in ambulatory patients with lung or colon cancer. Prevalence, characteristics, and effect. Cancer 1992; 70: 1616-1624.
12. Tishler M, Barak Y, Paran D et al. Sleep disturbances, fibromyalgia and primary Sjogren's syndrome. Clin Exp Rheumatol 1997; 15: 71-74.
13. Wilcox S, Brenes GA, Levine D et al. Factors related to sleep disturbance in older adults experiencing knee pain or knee pain with radiographic evidence of knee osteoarthritis. J Am Geriatr Soc 2000; 48: 1241-1251.
14. Wittig RM, Zorick FJ, Blumer D et al. Disturbed sleep in patients complaining of chronic pain. J Nerv Ment Dis 1982; 170: 429-431.
15. Drewes AM, Svendsen L, Taagholt SJ et al. Sleep in rheumatoid arthritis: a comparison with healthy subjects and studies of sleep/wake interactions. Br J Rheumatol 1998; 37: 71-81.
16. Lavie P, Epstein R, Tzischinsky O et al. Actigraphic measurements of sleep in rheumatoid arthritis: comparison of patients with low back pain and healthy controls. J Rheumatol 1992; 19: 362-365.
17. Mahowald MW, Mahowald ML, Bundlie SR et al. Sleep fragmentation in rheumatoid arthritis. Arthritis Rheum 1989; 32: 974-983.
18. Moldofsky H, Lue FA, Smythe HA. Alpha EEG sleep and morning symptoms in rheumatoid arthritis. J Rheumatol 1983; 10: 373-379.
19. Moldofsky H, Scarisbrick P, England R et al. Musculosketal symptoms and non-REM sleep disturbance in patients with "fibrositis syndrome" and healthy subjects. Psychosom Med 1975; 37: 341-351.
20. Schneider-Helmert D, Whitehouse I, Kumar A et al. Insomnia and alpha sleep in chronic non-organic pain as compared to primary insomnia. Neuropsychobiol 2001; 43: 54-58.
21. Affleck G, Urrows S, Tennen H et al. Sequential daily relations of sleep, pain intensity, and attention to pain among women with fibromyalgia. Pain 1996; 68: 363-368.
22. Jamieson AH, Alford CA, Bird HA et al. The effect of sleep and nocturnal movement on stiffness, pain, and psychomotor performance in ankylosing spondylitis. Clin Exp Rheumatol 1995; 13: 73-78.
23. Raymond I, Nielsen TA, Lavigne G et al. Quality of sleep and its daily relationship to pain intensity in hospitalized adult burn patients. Pain 2001; 92: 381-388.
24. Dement WC. Perception during sleep. Proc Annu Meet Am Psychopathol Assoc 1965; 53: 247-270.
25. Beydoun A, Morrow TJ, Shen JF et al. Variability of laser-evoked potentials: attention, arousal and lateralized differences. Electroencephalogr Clin Neurophysiol 1993; 88: 173-181.
26. Lavigne G, Zucconi M, Castronovo C et al. Sleep arousal response to experimental thermal stimulation during sleep in human subjects free of pain and sleep problems. Pain 2000; 84: 283-290.
27. Drewes AM, Nielsen KD, Arendt-Nielsen L et al. The effect of cutaneous and deep pain on the electroencephalogram during sleep - an experimental study. Sleep 1997; 20: 632-640.
28. American Sleep Disorders Association. EEG arousals: scoring rules and examples: a preliminary report from the Sleep Disorders Atlas Task Force of the American Sleep Disorders Association. Sleep 1992; 15: 173-184.
29. Willer JC, Boureau F, Albe-Fessard D. Supraspinal influences on nociceptive flexion reflex and pain sensation in man. Brain Res 1979; 179: 61-68.
30. Mason P, Escobedo I, Burgin C et al. Nociceptive responsiveness during slow-wave sleep and waking in the rat. Sleep 2001; 24: 32-38.
31. Chase MH. The digastric reflex in the kitten and adult cat: paradoxical amplitude fluctuations during sleep and wakefulness. Arch Ital Biol 1970; 108: 403-422.
32. Kshatri AM, Baghdoyan HA, Lydic R. Cholinomimetics, but not morphine, increase antinociceptive behavior from pontine reticular regions regulating rapideye-movement sleep. Sleep 1998; 21: 677-685.
33. Mason P. Contributions of the medullary raphe and ventromedial reticular region to pain modulation and other homeostatic functions. Ann Rev Neurosci 2001; 24: 737-777.
34. Carli G, Montesano A, Rapezzi S et al. Differential effects of persistent nociceptive stimulation on sleep stages. Behav Brain Res 1987; 26: 89-98.
35. Landis CA, Robinson CR, Levine JD. Sleep fragmentation in the arthritic rat. Pain 1988; 34: 93-99.
36. Landis CA, Levine JD, Robinson CR. Decreased slow-wave and paradoxical sleep in a rat chronic pain model. Sleep 1989; 12: 167-177.
37. Willis WD, Westlund KN. Neuroanatomy of the pain system and of the pathways that modulate pain. J Clin Neurophysiol 1997; 14: 2-31.
38. Zhuo M, Gebhart GF. Characterization of descending inhibition and facilitation from the nuclei reticularis gigantocellutaris and gigantocellularis pars alpha in the rat. Pain 1990; 42: 337-350.
39. Zhuo M, Gebhart GF. Characterization of descending facilitation and inhibition of spinal nociceptive transmission from the nuclei reticularis gigantocellularis and gigantocellularis pars alpha in the rat. J Neurophysiol 1992; 67: 1599-1614.
40. Behbehani MM, Fields HL. Evidence that an excitatory connection between the periaqueductal gray and nucleus raphe magnus mediates stimulation produced analgesia. Brain Res 1979; 170: 85-93.
41. Gebhart GF, Sandkuhler J, Thalhammer JG et al. Inhibition of spinal nociceptive information by stimulation in midbrain of the cat is blocked by lidocaine microinjected in nucleus raphe magnus and medullary reticular formation. J Neurophysiol 1983; 50: 1446-1459.
42. Kaplan H, Fields HL. Hyperalgesia during acute opioid abstinence: evidence for a nociceptive facilitating function of the rostral ventromedial medulla. J Neurosci 1991; 11: 1433-1439.
43. Sandkuhler J, Gebhart GF. 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 1984; 305: 77-87.
44. Fields HL, Bry J, Hentall I et al. The activity of neurons in the rostral medulla of the rat during withdrawal from noxious heat. J Neurosci 1983; 3: 2545-2552.
45. Barbaro NM, Heinricher MM, Fields HL. Putative nociceptive modulatory neurons in the rostral ventromedial medulla of the rat display highly correlated firing patterns. Somatosens Mot Res 1989; 6: 413-425.
46. Heinricher MM, Barbara NM, Fields HL. Putative nociceptive modulating neurons in the rostral ventromedial medulla of the rat: firing of on- and off-cells is related to nociceptive responsiveness. Somatosens Mot Res 1989; 6: 427-439.
47. Bederson JB, Fields HL, Barbaro NM. Hyperalgesia during naloxone-precipitated withdrawal from morphine is associated with increased on-cell activity in the rostral ventromedial medulla. Somatosens Mot Res 1990; 7: 185-203.
48. Heinricher MM, Drasner K. Lumbar intrathecal morphine alters activity of putative nociceptive modulatory neurons in rostral ventromedial medulla. Brain Res 1991; 549: 338-341.
49. Heinricher MM, Morgan MM, Tortorici V et al. Disinhibition of off-cells and antinociception produced by an opioid action within the rostral ventromedial medulla. Neurosci 1994; 63: 279-288.
50. Heinricher MM, Morgan MM, Fields HL. Direct and indirect actions of morphine on medullary neurons that modulate nociception. Neurosci 1992; 48: 533-543.
51. Heinricher MM, McGaraughty S. Analysis of excitatory amino acid transmission within the rostral ventromedial medulla: implications for circuitry. Pain 1998; 75: 247-255.
52. Heinricher MM, McGaraughty S, Farr DA. The role of excitatory amino acid transmission within the rostral ventromedial medulla in the antinociceptive actions of systemically administered morphine. Pain 1999; 81: 57-65.
53. Dahlstrom A, Fuxe K. Evidence for the existence of monoamine-containing neurons in the central nervous system I. Demonstration of monoamine in the cell bodies of brain stem neurons. Acta Physiol Scan 1964; 232: 1-36.
54. Oliveras JL, Bourgoin S, Hery F et al. The topographical distribution of serotoninergic terminals in the spinal cord of the cat: biochemical mapping by the combined use of microdissection and microassay procedures. Brain Res 1977; 138: 393-406.
55. Yaksh TL, Wilson PR. Spinal serotonin terminal system mediates antinociception. J Pharmacol Exp Ther 1979; 208: 446-453.
56. Belcher G, Ryall RW, Schaffner R. The differential effects of 5-hydroxytryptamine, noradrenaline and raphe stimulation on nociceptive and non-nociceptive dorsal horn interneurones in the cat. Brain Res 1978; 151: 307-321.
57. Randic M, Yu HH. Effects of 5-hydroxytryptamine and bradykinin in cat dorsal horn neurones activated by noxious stimuli. Brain Res 1976; 111: 197-203.
58. Zhuo M, Gebhart GF. Spinal serotonin receptors mediate descending facilitation of a nociceptive reflex from the nuclei reticularis gigantocellularis and gigantocellularis pars alpha in the rat. Brain Res 1991; 550: 35-48.
59. Fields HL, Heinricher MM, Mason P. Neurotransmitters in nociceptive modulatory circuits. Annu Rev Neurosci 1991; 14: 219-245.
60. Mason P. Physiological identification of pontomedullary serotonergic neurons in the rat. J Neurophysiol 1997; 77: 1087-1098.
61. Potrebic SB, Fields HL, Mason P. Serotonin immunoreactivity is contained in one physiological cell class in the rat rostral ventromedial medulla. J Neurosci 1994; 14: 1655-1665.
62. Gao K, Mason P. Serotonergic raphe magnus cells that respond to noxious tail heat are not ON or OFF cells. J Neurophysiol 2000; 84: 1719-1725.
63. Chiang CY, Pan ZZ. Differential responses of serotonergic and non-serotonergic neurons in nucleus raphe magnus to systemic morphine in rats. Brain Res 1985; 337: 146-150.
64. Gao K, Kim YH, Mason P. Serotonergic pontomedullary neurons are not activated by antinociceptive stimulation in the periaqueductal gray. J Neurosci 1997; 17: 3285-3292.
65. Gao K, Chen DO, Genzen JR et al. Activation of serotonergic neurons in the raphe magnus is not necessary for morphine analgesia. J Neurosci 1998; 18: 1860-1868.
66. Mason P, Gao K. Raphe magnus serotonergic neurons tonically modulate nociceptive transmission. Pain Forum 1998; 7: 143-150.
67. Fornal C, Auerbach S, Jacobs BL. Activity of serotonin -containing neurons in nucleus raphe magnus in freely moving cats. Exp Neurol 1985; 88: 590-608.
68. Auerbach S, Fornal C, Jacobs BL. Response of serotonin-containing neurons in nucleus raphe magnus to morphine, noxious stimuli, and periaqueductal gray stimulation in freely moving cats. Exp Neurol 1985; 88: 609-628.
69. Sorkin LS, McAdoo DJ, Willis WD. Raphe magnus stimulation-induced antinociception in the cat is associated with release of amino acids as well as serotonin in the lumbar dorsal horn. Brain Res 1993; 618: 95-108.
70. Leung CG, Mason P. Physiological properties of raphe magnus neurons during sleep and waking. J Neurophysiol 1999; 81: 584-595.
71. Oliveras JL, Vos B, Martin G et al. Electrophysiological properties of ventromedial medulla neurons in response to noxious and non-noxious stimuli in the awake, freely moving rat: a single-unit study. Brain Res 1989; 486: 1-14.
72. Montagne-Clavel J, Oliveras JL. Are ventromedial medulla neuronal properties modified by chronic peripheral inflammation? A single-unit study in the awake, freely moving polyarthritic rat. Brain Res 1994; 657: 92-104.
73. Martin G, Montagne-Clavel J, Oliveras JL. Involvement of ventromedial medulla "multimodal, multireceptive" neurons in opiate spinal descending control system: a single-unit study of the effect of morphine in the awake, freely moving rat. J Neurosci 1992; 12: 1511-1522.
74. Foo H, Mason P. Bicuculline microinjection into the raphe magnus suppresses air puff-evoked awakenings in behaving rats. Soc Neurosci 2000; 26: 660 (Abstr.)
75. Heinricher MM, Tortorici V. Interference with GABA transmission in the rostral ventromedial medulla: disinhibition of off-cells as a central mechanism in nociceptive modulation. Neurosci 1994; 63: 533-546.
76. Heinricher MM, Haws CM, Fields HL. Evidence for GABA-mediated control of putative nociceptive modulating neurons in the rostral ventromedial medulla: iontophoresis of bicuculline eliminates the off-cell pause. Somatosens Mot Res 1991; 8: 215-225.
77. Coutinho SV, Urban MO, Gebhart GF. Role of glutamate receptors and nitric oxide in the rostral ventromedial medulla in visceral hyperalgesia. Pain 1998; 78: 59-69.