Descending facilitatory modulation of a behavioral nociceptive response by stimulation in the adult rat anterior cingulate cortex

European Journal of Pain

Volumn 4, Issue 1, 2000, Pages 83-96

  Calejesan, Amelita A ^a   Kim, Susan J ^a   Zhuo, Min ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Anterior cingulate cortex; Descending facilitation; Metabotropic glutamate receptor; Rat; Rostral ventral medulla; Tail flick reflex

Indexed keywords

METABOTROPIC RECEPTOR;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CINGULATE GYRUS; CONTROLLED STUDY; ELECTROSTIMULATION; FACILITATION; MALE; MEDULLA OBLONGATA; NEUROMODULATION; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; RAT; TAIL FLICK TEST;

EID: 0034093384     PISSN: 10903801     EISSN: None     Source Type: Journal    
DOI: 10.1053/eujp.1999.0158     Document Type: Article

References (63)

1. Aimone D. L., Gebhart G. F. Stimulation-produced spinal inhibition from the midbrain in the rat is mediated by an excitatory amino acid transmitter in the medial medulla. J Neurosci. 6:1986;803-1813.
2. Basbaum AI and Fields H. L. Endogenous pain control mechanisms: review and hypothesis. Ann Neurol. 4:1978;451-462.
3. Basbaum A. I., Fields H. L. Endogenous pain control system: brainstem spinal pathways and endorphin circuitry. Ann Rev Neurosci. 7:1984;309-338.
4. Batchelor AM and Garthwaite J. Frequency detection and temporally dispersed synaptic signal association through a metabotropic glutamate receptor pathway. Nature. 385:1997;74-77.
5. Behbehani M. M., Fields H. L. Evidence that an excitatory connection between the periaqueductal gray and nucleus raphe magnus mediates stimulation produced analgesia. Brain Res. 170:1979;85-93.
6. Beitz A. J., Mullett M. A., Weiner K. L. The periaqueductal gray projections to the rat spinal trigeminal, raphe magnus, gigantocellular pars alpha and paragigantocellular nuclei arise from separate neurons. Brain Res. 288:1983;307-314.
7. Calejesan A. A., Ch'ang M. H-C, Zhuo M. Spinal serotonergic receptors mediate facilitation of a nociceptive reflex by subcutaneous formalin injection into the hindpaw in rats. Brain Res. 798:1998;46-54.
8. Cervero F., Wolstencroft J. H. A positive feedback loop between spinal cord nociceptive pathways and antinociceptive areas of the cat's brain stem. Pain. 20:1984;125-138.
9. Devinsky O., Morrell M. J., Vogt B. A. Contributions of anterior cingulate cortex to behaviour. Brain. 118:1995;279-306.
10. Duncan G. H., Bushnell M. C., Bates R., Dubner R. Task related responses of monkey medullary dorsal horn neurons. J Neurophysiol. 57:1987;289-310.
11. Fields H. L., Barbaro N. M., Heinricher M. M. Brain stem neuronal circuitry underlying the antinociceptive action of opiates. Prog Brain Res. 77:1988;245-257.
12. Fields H. L., Bry J., Hentall I., Zorman G. The activity of neurons in the rostral medulla of the rat during withdrawal from noxious heat. J Neurosci. 3:1983a;2545-2552.
13. Fields H. L., Heinricher M. M., Mason P. Neurotransmitters in nociceptive modulatory circuits. Ann Rev Neurosci. 14:1991;219-245.
14. Fields H. L., Vanegas H., Hentall I. D., Zorman G. Evidence that disinhibition of brainstem neurons contributes to morphine analgesia. Nature. 306:1983b;684-686.
15. Floeter M. K., Fields H. L. Evidence that inhibition of a nociceptive flexion reflex by stimulation in the rostroventromedial medulla in rats occurs at a premotoneuronal level. Brain Res. 538:1991;340-342.
16. Gabriel M. Discriminative avoidance learning: a model system. Vogt B. A., Gabriel M. Neurobiology of cingulate cortex and limbic thalamus: a comprehensive handbook. 1993;478-523 Birkhauser, Boston.
17. Gabriel M., Kubota Y., Sparenborg S. P., Straube K., Vogt B. A. Effects of cingulate cortical lesions on avoidance learning, and training-induced unit activity in rabbits. Exp Brain Res. 86:1991;585-600.
18. Gabriel M., Sparenborg S. P., Kubota Y. Anterior and medial thalamic lesions, discriminative avoidance learning, and cingulate cortical neuronal activity in rabbits. Exp Brain Res. 76:1989;441-457.
19. Gebhart G. F., Sandkuhler J., Thalhammer J. G., Zimmermann M. Inhibition of spinal nociceptive information by stimulation in the midbrain of the cat is blocked by lidocaine microinjected in nucleus raphe magnus and the medullary reticular formation. J Neurophysiol. 50:1983;1446-1457.
20. Gebhart G. F., Randich A. I. Brainstem modulation of nociception. Klemm W. R., Vertes R. P. Brainstem Mechanisms of Behavior. 1990;315-352 Wiley and Sons, New York.
21. Grossman M. L., Basbaum A. I., Fields H. L. Afferent and efferent connections of the rat tail flick reflex (a model used to analyze pain control mechanisms). J Comp Neurol. 206:1982;9-16.
22. Haber L. H., Martin R. F., Chung J. M., Willis W. D. Inhibition and excitation of primate spinothalamic tract neurons by stimulation in region of nucleus reticularis gigantocellularis. J Neurophysiol. 43:1980;1578-1593.
23. Hammond D. L. Control systems for nociceptive afferent processing the descending inhibitory pathways. Yaksh T. L. Spinal Afferent Processing. 1986;363-390 Pleum.
24. Heinricher M. M., Cheng Z. F., Fields H. L. Evidence for two classes of nociceptive modulating neurons in the periaqueductal gray. J Neuroscience. 7:1987;271-278.
25. Hori Y., Endo K., Takahashi T. Long-lasting synaptic facilitation induced by serotonin in superficial dorsal horn neurons of the rat spinal cord. J Physiol. 492:1996;867-876.
26. Kaplan H., Fields H. L. Hyperalgesia during acute opioid abstinence: evidence for a nociceptive facilitating function of the rostral ventromedial medulla. J Neuroscience. 11:1991;1433-1439.
27. Li P., Zhuo M. Silent glutamatergic synapses and nociception in mammalian spinal cord. Nature. 393:1998;695-698.
28. Lichtman A. H., Smith F. L., Martin B. R. Evidence that the antinociceptive tail-flick response is produced independently from changes in either tail-skin temperature or core temperature. Pain. 55:1993;283-295.
29. Light A. R., Casale E. J., Menetrey D. M. The effects of focal stimulation in nucleus raphe magnus and periaqueductal gray on intracellularly recorded neurons in spinal laminae I and II. J Neurophysiol. 56:1986;555-571.
30. Mao J., Mayer D. J., Price D. D. Patterns of increased brain activity indicative of pain in a rat model of peripheral mononeuropathy. J Neurosci. 13:1993;2689-2702.
31. McCreery D. B., Bloedel J. R., Hames E. G. Effects of stimulating in raphe nuclei and in reticular formation on response of spinothalamic neurons to mechanical stimuli. J Neurophysiol. 42:1979;166-182.
32. McMahon S. B., Wall P. D. Descending excitation and inhibition of spinal cord laminae I projection neurons. J Neurophysiol. 59:1988;1204-1219.
33. Meng I. D., Manning B. H., Martin W. J., Fields H. L. An analgesia circuit activated by cannabinoids. Nature. 395:1998;381-383.
34. Mitchell J. M., Lowe D., Fields H. L. The contribution of the rostral ventromedial medulla to the antinociceptive effects of systemic morphine in restrained and unrestrained rats. Neuroscience. 87:1998;123-133.
35. Pastoriza L. N., Morrow T. J., Casey K. L. Medial frontal cortex lesions selectively attenuate the hot plate response: possible nocifensive apraxia in the rat. Pain. 64:1996;11-17.
36. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates, 2nd Edition. 1986;Academic Press, New York.
37. Rainville P., Duncan G. H., Price D. D., Carrier B., Bushnell M. C. Pain affect encoded in human anterior cingulate but not somatosensory cortex. Science. 377:1997;968-971.
38. Ren K., Randich A., Gebhart G. F. Vagal afferent modulation of spinal nociceptive transmission in the rat. J Neurophysiol. 62:1989;401-415.
39. Ren K., Randich A., Gebhart G. F. Electrical stimulation of cervical vagal afferents. I. Central relays for modulation of spinal nociceptive transmission. J Neurophysiol. 64:1990;1098-1114.
40. Sandkühler J. The organization and function of endogenous antinociceptive systems. Prog Neurobiol. 50:1996;49-81.
41. Sandkühler J., Gebhart G. F. Relative contribution 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. 305:1984;77-87.
42. Scanziani M., Salin P. A., Vogt K. E., Malenka R. C., Nicoll R. A. Use-dependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors. Nature. 385:1997;630-634.
43. Sikes R. W., Vogt B. A. Nociceptive neurons in area 24 of rabbit cingulate cortex. J Neurophysiol. 68:1992;1720-1732.
44. Talbot J. D., Marrett S., Evans A. C., Meyer E., Bushnell M. C., Duncan G. H. Multiple representations of pain in human cerebral cortex. Science. 251:1991;1355-1358.
45. Tanaka E., North R. A. Opioid actions on rat anterior cingulate cortex neurons in vitro. J Neurosci. 14:1994;1106-1113.
46. Thomas D. A., McGowan M. K., Hammond D. L. Microinjection of baclofen in the ventromedial medulla of rats: antinociception at low doses and hyperalgesia at high doses. J Pharmacol Exp Ther. 275:1995;274-284.
47. Tjolsen A., Berge O-G., Eide P. K., Broch O. J., Hole K. Apparent hyperalgesia after lesions of the descending serotonergic pathways is due to increased tail skin temperature. Pain. 33:1988;225-231.
48. Traub R. J., Silva E., Gebhart G. F., Solodkin A. Noxious colorectal distension induced-c-Fos protein in limbic brain structures in the rat. Neurosci Lett. 215:1996;165-168.
49. Urban M. O., Gebhart G. F. Characterization of biphasic modulation of spinal nociceptive transmission by neurotensin in the rat rostral ventromedial medulla. J Neurophysiol. 78:1997;1550-1562.
50. Urban M. O., Jiang M. C., Gebhart G. F. Participation of central descending nociceptive facilitatory systems in secondary hyperalgesia produced by mustard oil. Brain Res. 737:1996;83-91.
51. Urban M. O., Coutinho S. V., Gebhart G. F. Involvement of excitatory amino acid receptors and nitric oxide in the rostral ventromedial medulla in modulating secondary hyperalgesia produced by mustard oil. Pain. 81:1999;45-55.
52. Vogt B. A., Derbyshire S., Jones A. K. P. Pain processing in four regions of human cingulate cortex localized with co-registered PET and MR imaging. Eur J Neurosci. 8:1996;1461-1473.
53. Vogt B. A., Sikes R. W., Vogt L. J. Anterior cingulate cortex and the medial pain system. Vogt B. A., Gabriel M. Neurobiology of cingulate cortex and limbic thalamus: a comprehensive handbook. 1993;313-344.
54. Wei F., Dubner R., Ren K. Nucleus reticularis gigantocellularis and nucleus raphe magnus in the brain stem exert opposite effects on behavioral hyperalgesia and spinal Fos protein expression after peripheral inflammation. Pain. 80:1999;127-141.
55. Wiertelak E. P., Furness L., Horan R., Martinez J., Maier S., Watkins L. R. Subcutaneous formalin produces centrifugal hyperalgesia at a non-injected site via the NMDA-nitric oxide cascade. Brain Res. 649:1994;19-26.
56. Willis W. D. Anatomy and physiology of descending control of nociceptive responses of dorsal horn neurons: comprehensive review. Prog Brain Res. 77:1988;1-29.
57. Willis W. D., Westlund K. N. Neuroanatomy of the pain system and of the pathways that modulate pain. J Clin Neurophysiol. 14:1997;2-31.
58. Zhuo M., Gebhart G. F. Characterization of descending inhibition and facilitation from the nuclei reticularis gigantocellularis and gigantocellularis pars alpha in the rat. Pain. 42:1990;337-350.
59. Zhuo M., Gebhart G. F. Spinal serotonin receptors mediate descending facilitation of a nociceptive reflex from the nuclei reticularis gigantocellularis and gigantocellularis pars alpha in the rat. Brain Res. 550:1991;35-48.
60. Zhuo M., Gebhart G. F. Characterization of descending facilitation and inhibition of spinal nociceptive transmission from the nuclei reticularis gigantocellularis and gigantocellularis pars alpha in the rat. J. Neurophysiol. 67:1992;1599-1614.
61. Zhuo M., Gebhart G. F. Central pain modulation: descending facilitatory system. Prog Physiol Sci. 24:1993;252-254.
62. Zhuo M., Gebhart G. F. Biphasic modulation of spinal nociceptive transmission from the medullary raphe nuclei in the rat. J Neurophysiol. 78:1997;746-758.
63. Zhuo M., Lee D. E., Li P., Calejesan A. A. The cingulate cortex biphasically regulates spinal nociception. Soc Neurosci Abst. 24:1998;1135.