GABAA receptors are involved in the analgesic effects of morphine microinjected into the central nucleus of the amygdala

Clinical and Experimental Pharmacology and Physiology

Volumn 41, Issue 5, 2014, Pages 338-344

  Rashvand, Mina ^a   Khajavai, Ali ^a   Parviz, Mohsen ^a   Hasanein, Parisa ^b   Keshavarz, Mansoor ^a  

^a TEHRAN UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b BU ALI SINA UNIVERSITY   (Iran)

Author keywords

Amygdala; Antinociception; Bicuculline; Muscimol; Opioid

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; ANALGESIC AGENT; BICUCULLINE; MORPHINE; MUSCIMOL; NALOXONE; NARCOTIC ANALGESIC AGENT; NARCOTIC ANTAGONIST;

AMYGDALOID NUCLEUS; ANALGESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; BRAIN; CENTRAL NUCLEUS (AMYGDALA); DRUG EFFECT; GABAERGIC SYSTEM; HISTOLOGY; HYPERALGESIA; LATENT PERIOD; MALE; MICROINJECTION; NOCICEPTION; NONHUMAN; PAIN; RAT; TAIL FLICK TEST; ANIMAL; DOSE RESPONSE; DRUG EFFECTS; METABOLISM; PAIN MEASUREMENT;

ANALGESICS, OPIOID; ANIMALS; CENTRAL AMYGDALOID NUCLEUS; DOSE-RESPONSE RELATIONSHIP, DRUG; GABA-A RECEPTOR AGONISTS; MALE; MICROINJECTIONS; MORPHINE; MUSCIMOL; NALOXONE; NARCOTIC ANTAGONISTS; PAIN MEASUREMENT; RATS; RECEPTORS, GABA-A;

EID: 84899079662     PISSN: 03051870     EISSN: 14401681     Source Type: Journal    
DOI: 10.1111/1440-1681.12223     Document Type: Article

References (49)

1. Rizvi TA, Ennis M, Behbehani MM, Shipley MT. Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: Topography and reciprocity. J. Comp. Neurol. 1991; 303: 121-31.
2. Manning BH, Mayer DJ. The central nucleus of the amygdala contributes to the production of morphine antinociception in the formalin test. Pain 1995; 63: 141-52.
3. Manning BH, Mayer DJ. The central nucleus of the amygdala contributes to the production of morphine antinociception in the rat tail-flick test. J. Neurosci. 1995; 15: 8199-213.
4. Rodgers RJ. Elevation of aversive threshold in rats by intra-amygdaloid injection of morphine sulphate. Pharmacol. Biochem. Behav. 1977; 6: 385-90.
5. Kalivas PW, Gau BA, Nemeroff CB, Prange AJ Jr. Antinociception after microinjection of neurotensin into the central amygdaloid nucleus of the rat. Brain Res. 1982; 243: 279-86.
6. al-Rodhan N, Chipkin R, Yaksh TL. The antinociceptive effects of SCH-32615, a neutral endopeptidase (enkephalinase) inhibitor, microinjected into the periaqueductal, ventral medulla and amygdala. Brain Res. 1990; 520: 123-30.
7. Klamt JG, Prado WA. Antinociception and behavioral changes induced by carbachol microinjected into identified sites of the rat brain. Brain Res. 1991; 549: 9-18.
8. Helmstetter FJ, Bellgowan PS, Tershner SA. Inhibition of the tail flick reflex following microinjection of morphine into the amygdala. NeuroReport 1993; 4: 471-4.
9. Helmstetter FJ, Bellgowan PS, Poore LH. Microinfusion of mu but not delta or kappa opioid agonists into the basolateral amygdala results in inhibition of the tail flick reflex in pentobarbital-anesthetized rats. J. Pharmacol. Exp. Ther. 1995; 275: 381-8.
10. Oliveira MA, Prado WA. Antinociception and behavioral manifestations induced by intracerebroventricular or intra-amygdaloid administration of cholinergic agonists in the rat. Pain 1994; 57: 383-91.
11. Pavlovic ZW, Bodnar RJ. Opioid supraspinal analgesic synergy between the amygdala and periaqueductal gray in rats. Brain Res. 1998; 779: 158-69.
12. Pavlovic ZW, Cooper ML, Bodnar RJ. Opioid antagonists in the periaqueductal gray inhibit morphine and beta-endorphin analgesia elicited from the amygdala of rats. Brain Res. 1996; 741: 13-26.
13. Helmstetter FJ, Tershner SA, Poore LH, Bellgowan PS. Antinociception following opioid stimulation of the basolateral amygdala is expressed through the periaqueductal gray and rostral ventromedial medulla. Brain Res. 1998; 779: 104-18.
14. Aggleton JP. The contribution of the amygdala to normal and abnormal emotional states. Trends Neurosci. 1993; 16: 328-33.
15. Gallagher M, Chiba AA. The amygdala and emotion. Curr. Opin. Neurobiol. 1996; 6: 221-7.
16. Graeff FG. Neuroanatomy and neurotransmitter regulation of defensive behaviors and related emotions in mammals. Braz. J. Med. Biol. Res. 1994; 27: 811-29.
17. Sabetkasaei M, Masoudnia F, Khansefid N, Behzadi G. Opioid receptors of the central amygdala and morphine-induced antinociception. Iran. Biomed. J. 2007; 11: 75-80.
18. Millan MJ. Descending control of pain. Prog. Neurobiol. 2002; 66: 355-474.
19. Marowsky A, Fritschy JM, Vogt KE. Functional mapping of GABA A receptor subtypes in the amygdala. Eur. J. Neurosci. 2004; 20: 1281-9.
20. Delaney AJ, Sah P. Pathway-specific targeting of GABA(A) receptor subtypes to somatic and dendritic synapses in the central amygdala. J. Neurophysiol. 2001; 86: 717-23.
21. Finnegan TF, Chen SR, Pan HL. Effect of the mu opioid on excitatory and inhibitory synaptic inputs to periaqueductal gray-projecting neurons in the amygdala. J. Pharmacol. Exp. Ther. 2005; 312: 441-8.
22. Foster AC, Kemp JA. Glutamate- and GABA-based CNS therapeutics. Curr. Opin. Pharmacol. 2006; 6: 7-17.
23. Gilbert AK, Franklin KB. GABAergic modulation of descending inhibitory systems from the rostral ventromedial medulla (RVM). Dose-response analysis of nociception and neurological deficits. Pain 2001; 90: 25-36.
24. Heinricher MM, Tortorici V. Interference with GABA transmission in the rostral ventromedial medulla: Disinhibition of off-cells as a central mechanism in nociceptive modulation. Neuroscience 1994; 63: 533-46.
25. 1 cannabinoid and mu opioid receptors mediating inhibition of neurotransmitter release in rat nucleus accumbens core. Neuropharmacology 2006; 51: 773-81.
26. Qu CL, Tang JS, Jia H. Involvement of GABAergic modulation of antinociception induced by morphine microinjected into the ventrolateral orbital cortex. Brain Res. 2006; 1073-1074: 281-9.
27. da Silva LF, Coutinho MR, Menescal-de-Oliveira L. Opioidergic and GABAergic mechanisms in the rostral ventromedial medulla modulate the nociceptive response of vocalization in guinea pigs. Brain Res. Bull. 2010; 82: 177-83.
28. Fowler CJ, Fraser GL. Mu-, delta-, kappa-opioid receptors and their subtypes. A critical review with emphasis on radioligand binding experiments. Neurochem. Int. 1994; 24: 401-26.
29. Kang-Park MH, Kieffer BL, Roberts AJ, Siggins GR, Moore SD. Presynaptic delta opioid receptors regulate ethanol actions in central amygdala. J. Pharmacol. Exp. Ther. 2007; 320: 917-25.
30. Zagon A, Meng X, Fields HL. Intrinsic membrane characteristics distinguish two subsets of nociceptive modulatory neurons in rat RVM. J. Neurophysiol. 1997; 78: 2848-58.
31. Heinricher MM, Morgan MM, Fields HL. Direct and indirect actions of morphine on medullary neurons that modulate nociception. Neuroscience 1992; 48: 533-43.
32. Heinricher MM, Morgan MM, Tortorici V, Fields HL. Disinhibition of off-cells and antinociception produced by an opioid action within the rostral ventromedial medulla. Neuroscience 1994; 63: 279-88.
33. Depaulis A, Morgan MM, Liebeskind JC. GABAergic modulation of the analgesic effects of morphine microinjected in the ventral periaqueductal gray matter of the rat. Brain Res. 1987; 436: 223-8.
34. Moreau JL, Fields HL. Evidence for GABA involvement in midbrain control of medullary neurons that modulate nociceptive transmission. Brain Res. 1986; 397: 37-46.
35. Calvo F, Coimbra NC. Interactions between opioid-peptides-containing pathways and GABA(A)-receptors-mediated systems modulate panic-like-induced behaviors elicited by electric and chemical stimulation of the inferior colliculus. Brain Res. 2006; 1104: 92-102.
36. Kiefel JM, Rossi GC, Bodnar RJ. Medullary mu and delta opioid receptors modulate mesencephalic morphine analgesia in rats. Brain Res. 1993; 624: 151-61.
37. Pan ZZ, Fields HL. Endogenous opioid-mediated inhibition of putative pain-modulating neurons in rat rostral ventromedial medulla. Neuroscience 1996; 74: 855-62.
38. Roychowdhury SM, Fields HL. Endogenous opioids acting at a medullary mu-opioid receptor contribute to the behavioral antinociception produced by GABA antagonism in the midbrain periaqueductal gray. Neuroscience 1996; 74: 863-72.
39. Zambotti F, Zonta N, Parenti M et al. Periaqueductal gray matter involvement in the muscimol-induced decrease of morphine antinociception. Naunyn Schmiedebergs Arch. Pharmacol. 1982; 318: 368-9.
40. Jia H, Xie YF, Xiao DQ, Tang JS. Involvement of GABAergic modulation of the nucleus submedius (Sm) morphine-induced antinociception. Pain 2004; 108: 28-35.
41. Hara K, Saito Y, Kirihara Y, Yamada Y, Sakura S, Kosaka Y. The interaction of antinociceptive effects of morphine and GABA receptor agonists within the rat spinal cord. Anesth. Analg. 1999; 89: 422-7.
42. A receptors in the central nucleus of amygdala (CeA) affect on pain modulation. Brain Res. 2008; 1241: 36-41.
43. Capogna M, Gahwiler BH, Thompson SM. Mechanism of mu-opioid receptor-mediated presynaptic inhibition in the rat hippocampus in vitro. J. Physiol. 1993; 470: 539-58.
44. Kalyuzhny AE, Wessendorf MW. CNS GABA neurons express the mu-opioid receptor: Immunocytochemical studies. NeuroReport 1997; 8: 3367-72.
45. Kalyuzhny AE, Wessendorf MW. Relationship of mu- and delta-opioid receptors to GABAergic neurons in the central nervous system, including antinociceptive brainstem circuits. J. Comp. Neurol. 1998; 392: 528-47.
46. Vaughan CW, Ingram SL, Connor MA, Christie MJ. How opioids inhibit GABA-mediated neurotransmission. Nature 1997; 390: 611-4.
47. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. Academic Press, San Diego. 1986.
48. Geiger BM, Frank LE, Caldera-Siu AD, Pothos EN. Survivable stereotaxic surgery in rodents. J. Vis. Exp. 2008; 20: 880.
49. D'Amour FE, Smith DL. A method for determining loss of pain sensation. J. Pharmacol. Exp. Ther. 1941; 72: 74-8.