Cardiovascular effects of microinjections of opioid agonists into the 'Depressor Region' of the ventrolateral periaqueductal gray region

Brain Research

Volumn 762, Issue 1-2, 1997, Pages 61-71

  Keay, Kevin A ^a   Crowfoot, Laura J ^a   Floyd, Nicole S ^a   Henderson, Luke A ^a   Christie, MacDonald J ^b   Bandler, Richard ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

^b University of Sydney   (Australia)

Author keywords

Analgesia; Bradycardia; Emotion; Hypertension; Hypotension; Opiate; Visceral pain

Indexed keywords

ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; ENKEPHALIN[2,5 DEXTRO PENICILLAMINE]; EXCITATORY AMINO ACID; N METHYL N [7 (1 PYRROLIDINYL) 1 OXASPIRO[4.5]DEC 8 YL]BENZENEACETAMIDE; OPIATE AGONIST;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRADYCARDIA; CARDIOVASCULAR EFFECT; CONTROLLED STUDY; HYPERTENSION; HYPOTENSION; MALE; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; PRIORITY JOURNAL; RAT; TACHYCARDIA;

ANALGESICS; ANIMALS; BENZENEACETAMIDES; BLOOD PRESSURE; BRADYCARDIA; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; ENKEPHALIN, D-PENICILLAMINE (2,5)-; ENKEPHALINS; EXCITATORY AMINO ACIDS; HEART RATE; HOMOCYSTEINE; HYPERTENSION; HYPOTENSION; MALE; MICROINJECTIONS; NEURAL INHIBITION; PAIN; PERIAQUEDUCTAL GRAY; PYRROLIDINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID; RECEPTORS, OPIOID, DELTA; RECEPTORS, OPIOID, KAPPA; RECEPTORS, OPIOID, MU;

EID: 0030789787     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(97)00285-0     Document Type: Article

References (73)

1. R. Bandler, P. Carrive, S. Zhang, Integration of somatic and autonomic reactions within the midbrain periaqueductal grey: viscerotopic, somatotopic and functional organisation, in: G. Holstege (Ed.), The Role of the Forebrain in Sensation and Behavior, Elsevier, Amsterdam, 1991, pp. 67-154.
2. R. Bandler, K.A. Keay, Columnar organization in the midbrain periaqueductal gray and the integration of emotional expression, in: G. Holstege, R. Bandler, C. Saper (Eds.), The Emotional Motor System, Elsevier, Amsterdam, 1996, pp. 285-300.
3. Bandler R., Shipley M. Columnar organization in midbrain periaqueductal gray: Modules for emotional expression? Trends Neurosci. 17:1994;379-389.
4. Behbehani M., Fields H. Evidence that an excitatory connection between the periaqueductal gray and nucleus raphe magnus mediates stimulation produced analgesia. Brain Res. 170:1979;85-93.
5. Behbehani M., Jiang M., Chandler S. The effect of [Met]-enkephalin on the periaqueductal neurons of the rat: an in vitro study. Neuroscience. 38:1990;373-380.
6. A.J. Beitz, Periaqueductal gray, in: G. Paxinos (Ed.), The Rat Nervous System, Academic Press, Sydney, 1995, pp. 173-181.
7. Benus R.F., Bohus B., Koolhaas J.M., Van-Oortmerssen G.A. Heritable variation for aggression as a reflection of individual coping strategies. Experientia. 47:1991;1008-1019.
8. Bernard J.F., Huang G.F., Besson J.M. The parabrachial area: electrophysiological evidence for an involvement in visceral nociceptive processes. J. Neurophysiol. 71:1994;551-569.
9. Bodnar R.J., Williams C.L., Lee S.J., Pasternak G.W. Role of μ1 opiate receptors in supraspinal opiate analgesia: a microinjection study. Brain Res. 447:1988;25-34.
10. Cameron A.A., Khan I.A., Westlund K.N., Willis W.D. The efferent projections of the periaqueductal gray in the rat: a phaseolus vulgaris-leucoagglutinin study. II. Descending projections J. Comp. Neurol. 35(1):1995;585-601.
11. Carrive P., Bandler R. Viscerotopic organization of neurons subserving hypotensive reactions within the midbrain periaqueductal grey: a correlative functional and anatomical study. Brain Res. 541:1991;206-215.
12. Chandler M., Garrison D., Brennan T., Foreman R. Effects of chemical and electrical stimulation of the midbrain on feline T2-T6 spinoreticular and spinal cell activity evoked by cardiopulmonary afferent input. Brain Res. 496:1989;148-164.
13. Chen S., Aston-Jones G. Anatomical evidence for inputs to ventrolateral medullary catecholaminergic neurons from the midbrain periaqueductal gray of the rat. Neurosci. Lett. 195:1995;140-144.
14. Chen S., Aston-Jones G. Extensive projections from the midbrain periaqueductal gray to the caudal ventrolateral medulla: a retrograde and anterograde tracing study in the rat. Neuroscience. 71:1996;443-459.
15. Chieng B., Christie M. Hyperpolarisation by opioids acting on mu receptors of a subpopulation of rat periaqueductal gray neurons in vitro. Br. J. Pharmacol. 113:1994;121-128.
16. Chieng B., Christie M. Inhibition by opioids acting on mu receptors of GABA-ergic and glutaminergic post-synaptic potentials in single rat periaqueductal gray neurons in vitro. Br. J. Pharmacol. 113:1994;303-309.
17. Clement C.I., Keay K.A., Bandler R. Halothane anesthesia-induced activation of medullary adrenergic and noradrenergic projections to the midbrain periaqueductal gray. Proc. Aust. Neurosci. Soc. 6:1995;180.
18. Clement C.I., Keay K.A., Owler B.K., Bandler R. Common patterns of increased and decreased Fos expression in midbrain and pons evoked by noxious deep somatic and noxious visceral manipulations in the rat. J. Comp. Neurol. 366:1996;495-515.
19. Depaulis A., Keay K.A., Bandler R. Longitudinal neuronal organisation of defensive reactions in the midbrain periaqueductal gray region of the rat. Exp. Brain Res. 90:1992;307-318.
20. Depaulis A., Keay K.A., Bandler R. Quiescence and hyporeactivity evoked by activation of cell bodies in the ventrolateral midbrain periaqueductal gray of the rat. Exp. Brain Res. 99:1994;75-83.
21. Duggan A.W. Injury pain and analgesia. Proc. Aust. Physiol. Pharmacol. Soc. 14:1983;218-240.
22. Duggan A.W., Morton C.R. Periaqueductal grey stimulation: an association between selective inhibition of dorsal horn neurones and changes in peripheral circulation. Pain. 15:1983;237-248.
23. Engel G.L., Schmale A.H. Conservation-withdrawal: a primary regulatory process for organismic homeostasis. CIBA Foundation Symposium. 8:1972;57-76.
24. Ennis M., Xu S.-J., Rizvi T.A., Behbehani M.M., Shipley M.T. The midbrain periaqueductal gray (PAG) densely innervates medullary regions containing cholinergic vago-cardiac neurons. Soc. Neurosci. Abstr. 19:1993;953.
25. M. Faneslow, The midbrain periaqueductal gray as a coordinator of action in response to fear and anxiety, in: A. Depaulis, R. Bandler (Eds.), The Midbrain Periaqueductal Gray Matter: Functional, Anatomical and Neurochemical Organization, Plenum, New York, 1991, pp. 151-173.
26. Fields H., Basbaum A. Brainstem control of spinal pain-transmission neurons. Annu. Rev. Physiol. 40:1978;217-248.
27. Floyd N.S., Keay K.A., Bandler R. A calbindin-immunoreactive "deep pain" recipient thalamic nucleus in the rat. NeuroReport. 7:1996;622-626.
28. Goldstein A., Naidu A. Multiple opioid receptors: ligand selectivity profiles and binding site signatures. Mol. Pharmacol. 36:1989;265-272.
29. Henderson L.A., Keay K.A., Bandler R. Ventrolateral midbrain periaqueductal gray: descending projections to medullary cardiovascular regions. Soc. Neurosci. Abstr. 21:1996;639.
30. J.P. Henry, P.M., Stephens, Stress Health and the Social Environment: A Sociobiological Approach to Medicine, Springer-Verlag, New York, 1977.
31. Herbert H., Saper C.B. Organization of medullary adrenergic and noradrenergic projections to the periaqueductal gray matter in the rat. J. Comp. Neurol. 315:1992;34-52.
32. G. Holstege, Descending pathways from the periaqueductal grey and adjacent areas, in: A. Depaulis, R. Bandler (Eds.), The Midbrain Periaqueductal Gray Matter: Functional, Anatomical and Neurochemical Organization, Plenum, New York, 1991, pp. 239-265.
33. Jensen T., Yaksh T. III. Comparison of the antinociceptive action of mu and delta opioid receptor ligands in the periaqueductal gray matter, medial and paramedial ventral medulla in the rat as studied by the microinjection technique. Brain Res. 372:1986;301-312.
34. Jensen T., Yaksh T. Brainstem excitatory amino acid receptors in nociception: microinjection mapping and pharmacological characterization of glutamate sensitive sites in the brainstem associated with algogenic behavior. Neuroscience. 46:1992;535-547.
35. Jensen T.S., Yaksh T.L. Spinal monoamine and opioid systems partially mediate an analgesia produced by glutamate at brainstem sites. Brain Res. 363:1984;114-127.
36. A. Kalyuzhny, U. Arvidsson, W. Wu, M. Wessendorf, Mu- and delta-opioid receptors are expressed in brainstem antinociceptive circuits: studies using immunocytochemistry and retrograde tract tracing, J. Neurosci., (in press).
37. K.A. Keay, K. Feil, B. Gordon, H. Herbert, R. Bandler, Spinal afferents to functionally-distinct PAG columns in the rat: An anterograde and retrograde tracing study, J. Comp. Neurol., (in press).
38. Keay K.A., Clement C.I., Owler B., Depaulis A., Bandler R. Convergence of deep somatic and visceral nociceptive information onto a discrete ventrolateral midbrain periaqueductal gray region. Neuroscience. 61:1994;727-732.
39. Levine R., Morgan M., Cannon J., Liebeskind J. Stimulation of the periaqueductal gray matter of the rat produces a preferential ipsilateral antinociception. Brain Res. 567:1991;140-144.
40. T. Lewis, Pain, McMillan, London, 1942.
41. Lewis T., Kellgren R.D. Observations related to referred pain, viscerosomatic reflexes and other associated phenomena. Clin. Sci. 4:1939;47.
42. Lewis V.A., Gebhart G.F. Evaluation of the periaqueductal gray (PAG) as a morphine-specific locus of action and examination of morphine-induced and stimulation produced analgesia at coincident PAG loci. Brain Res. 124:1977;283-303.
43. Li Y., Dampney R. Expression of Fos-like protein in brain following sustained hypertension and hypotension in conscious rabbits. Neuroscience. 61:1993;613-634.
44. Liebeskind J.C., Guilbaud G., Besson J.M., Oliveras J.L. Analgesia from electrical stimulation of the periaqueductal gray matter in the cat: behavioural observations and inhibitory effects on spinal cord interneurons. Brain Res. 50:1973;441-446.
45. Lovick T. Ventrolateral medullary lesions block the antinociceptive and cardiovascular responses elicited by stimulating the dorsal periaqueductal grey matter in rats. Pain. 21:1985;241-252.
46. Lovick T. Central nervous system integration of pain control and autonomic function. News Physiol. Sci. 6:1991;82-86.
47. T.A. Lovick, Interactions between descending pathways from the dorsal and ventrolateral periaqueductal gray matter in the rat, in: A. Depaulis, R. Bandler (Eds.), The Midbrain Periaqueductal Gray Matter: Functional, Anatomical and Neurochemical Organization, Plenum, New York, 1991, pp. 101-120.
48. Lovick T.A. Inhibitory modulation of the cardiovascular defence response by the ventrolateral periaqueductal grey matter in rats. Exp. Brain Res. 89:1992;133-139.
49. Mansour A., Fox C., Burke S., Meng F., Thompson R., Akil H., Watson S. Mu, delta and kappa opioid receptor mRNA expression in the rat CNS: an in situ hybridization study. J. Comp. Neurol. 350:1994;412-438.
50. Mansour A., Khachaturian H., Lewis M., Akil H., Watson S. Autoradiographic differentiation of mu, delta and kappa opioid receptors in the rat forebrain and midbrain. J. Neurosci. 7:1987;2445-2464.
51. Mayer D.J., Hayes R.L. Stimulation produced analgesia: development of tolerance and cross-tolerance to morphine. Science. 188:1975;941-943.
52. Mayer D.J., Leibeskind J.C. Pain reduction by focal electrical stimulation of the brain: an anatomical and behavioural analysis. Brain Res. 68:1974;73-93.
53. Mayer D.J., Wolfe T.L., Akil H. Analgesia from electrical stimulation in the brainstem of the rat. Science. 174:1971;1351-1354.
54. Murphy A., Ennis M., Rizvi T., Behbehani M., Shipley M.T. Fos expression induced by changes in arterial pressure is localised in distinct longitudinally organised columns of neurons in the rat midbrain periaqueductal gray. J. Comp. Neurol. 360:1995;286-300.
55. Osborne P., Vaughan C., Wilson H., Christie M. Opioid inhibition of rat periaqueductal gray neurones with projections to the rostral ventromedial medulla in vitro. J. Physiol. 490:1996;383-389.
56. G. Paxinos, C. Watson, The Rat Brain in Stereotaxic Co-ordinates, Academic Press, Sydney, 1986.
57. Reynolds D.V. Surgery in the rat during electrical analgesia induced by focal brain stimulation. Science. 164:1969;444-445.
58. Rossi G.C., Pasternak G.W., Bodnar R.J. μ and δ opioid synergy between the periaqueductal gray and the rostro-ventral medulla. Brain Res. 665:1994;85-93.
59. Satoh M., Kubota A., Iwama T., Wada T., Yasui M., Fujibashi K., Takagi H. Comparison of analgesic potencies of mu, delta and kappa agonists locally applied to various CNS regions relevant to analgesia in rats. Life Sci. 33:1983;689-692.
60. Sharpe L.G., Garnett J.E., Cicero T.J. Analgesia and hypersensitivity produced by intracranial microinjections of morphine into the periaqueductal grey matter of the rat. Behav. Biol. 11:1974;303-313.
61. M.T. Shipley, M.T. Ennis, T.A. Rizvi, M.M. Behbehani, Topographical specificity of forebrain inputs to the midbrain periaqueductal gray: Evidence for discrete longitudinally organised input columns, in: A. Depaulis, R. Bandler (Eds.), The Midbrain Periaqueductal Gray Matter: Functional, Anatomical and Neurochemical Organization, Plenum Press, New York, 1991, pp. 417-448.
62. Snowball R.K., Dampney R.A.L., Lumb B.M. A role for the caudal medullary raphe nuclei in the cardiovascular responses to noxious visceral stimulation? J. Physiol. 491:1995;114P.
63. Urca G., Nahin R., Liebeskind J. Glutamate-induced analgesia: blockade and potentiation by naloxone. Brain Res. 1980:1980;523-530.
64. Van Bockstaele E.J., Aston-Jones G. Distinct populations of neurons in the ventromedial periaqueductal gray project to the rostral ventral medulla and abducens nucleus. Brain Res. 576:1992;59-67.
65. VanBockstaele E.J., Aston-Jones G., Pieribone V.A., Ennis M., Shipley M.T. Subregions of the periaqueductal gray topographically innervate the rostral ventrolateral medulla in the rat. J. Comp. Neurol. 309:1991;305-327.
66. C. Vaughan, M. Christie, Presynaptic inhibitory action of opioids on synaptic transmission in the rat periaqueductal grey in vitro, J. Physiol., (1996).
67. Wall P.D. On the relation of injury to pain. Pain. 6:1979;253-264.
68. Yaksh T.L., Yeung J.C., Rudy T.A. Systematic examination in the rat of brain sites sensitive to the direct application of morphine: observation of differential effects within the periaqueductal grey. Brain Res. 114:1976;83-103.
69. Yasui Y., Breder C., Saper C., Cechetto D. Autonomic responses and efferent pathways from the insular cortex in the rat. J. Comp. Neurol. 303:1991;355-374.
70. Yasui Y., Saper C., Cechetto D. Calcitonin-gene related peptide immunoreactivity in the visceral sensory cortex, thalamus and related pathways in the rat. J. Comp. Neurol. 290:1989;487-501.
71. R.P. Yezierski, Somatosensory input to the periaqueductal gray: a spinal relay to a descending control centre, in: A. Depaulis, R. Bandler (Eds.), The Midbrain Periaqueductal Gray Matter: Functional, Anatomical and Neurochemical Organization, Plenum, New York, 1991, pp. 365-386.
72. Yezierski R.P., Mendez C.M. Spinal distribution and collateral projections of rat spinomesencephalic tract cells. Neuroscience. 44:1991;113-130.
73. Zhang S.P., Bandler R., Carrive P. Flight and immobility evoked by excitatory amino acid microinjection within distinct parts of the subtentorial periaqueductal grey of the cat. Brain Res. 520:1990;73-82.