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Review on Amygdala Neural Circuitry of Antinociception: On Actions of Opioids and Endocannabinoids

The Korean Journal of Cognitive and Biological Psychology / The Korean Journal of Cognitive and Biological Psychology, (P)1226-9654; (E)2733-466X
2010, v.22 no.3, pp.387-404
https://doi.org/10.22172/cogbio.2010.22.3.008

Abstract

Organisms encountering a threatening environment often express various fear responses including antinociception, or hypoalgesia. Main brian structures or regions responsible for antinociception are the PAG, the RVM and the amygdala that primarily compose the amygdala-brain stem circuitry. Regarding antinociceptive mechanisms of the amygdala that is important for processing negative emotional information, the author has previously suggested a potent neural model mainly focusing on actions by opioid systems. On the other hand, a considerable amount of recent empirical data have shown important contributions of endocannabinoids released in the antinociceptive system including the amygdala to controlling pain in organisms facing environmental stressors. Hence, the present review was processed to reflect this trend of neuropsychology and present a more comprehensive neural model. Important points of the present discussions are as follows. First, activation of neurons in the central nucleus of the amygdala (CeA) that project to the brain stem is the critical factor for producing antinociception from the amygdala, and the activity of the CeA cells is determined by a neural integration between inhibitory and excitatory inputs given from the basolateral complex of the amygdala (BLA). Second, these inhibitory and excitatory inputs are currently suggested to be regulated by opioids and endocannabinoids that are both released in the BLA under stress, respectively. Third, the present new neural model of amygdala antinociceptive actions gives comprehensive accounts for a variety of characteristics shared by opioids and endocannabinoids, such as functional similarities, synergistic actions and interactions.

keywords
antinociception, pain control, amygdala, (endo)cannabinoid, opioid, neural circuitry, 항유해 작용, 통각 조절, 편도체, 카나비노이드, 아편물질, 신경회로

Reference

1.

서동오, 이연경, 최준식 (2006). 공포의 생성과 소멸: 파블로프 공포조건화의 뇌회로를 중심으로. 한국심리학회지:실험, 18(1), 1-19.

2.

신맹식 (2008). 뇌의 항유해작용 기제에 관한 개관: 편도체-뇌간 회로를 중심으로. 한국심리학회지: 실험, 20(2), 73-94.

3.

Atweh, S. F., & Kuhar, M. J. (1977). Autoradiographic localization of opiate receptors in rat brain III. The telencephalon. Brain Research, 134, 393-405.

4.

Basbaum, A. I., & Fields, H. L. (1978). Endogenous pain control mechanisms: Review and hypothesis. Annals of Neurology, 4, 451-462.

5.

Basbaum, A. I., & Fields, H. L. (1984). Endogenous pain control systems: Brainstem spinal pathways and endorphin circuitry. Annual Review of Neuroscience, 7, 309-338.

6.

Behbehani, M. M., & Pert, A. (1984). A mechanism for the analgesic effect of neurotensin as revealed by behavioral and electrophysiological techniques. Brain Research, 324, 35-42.

7.

Bellgowan, P. S., & Helmstetter, F. J. (1998). The role of mu and kappa opioid receptors within the periaqueductal gray in the expression of conditional hypoalgesia. Brain Research, 279, 83-89.

8.

Butler, R. K., Rea, K., Lang, Y., Gavin, A. M., & Finn, D. P. (2008). Endocannabinoid- mediated enhancement of fear-conditioned analgesia in rats: opioid receptor dependency and molecular correlates. Pain, 140, 491-500.

9.

Cannich, A., Wotjak, C.T., Kamprath, K., Hermann, H., Lutz, B., & Marsicano, G. (2004). CB1 cannabinoid receptors modulate kinase and phosphatase activity during extinction of conditioned fear in mice. Learning and Memory, 11, 625-632.

10.

Carlson, N. R. (2002). Foundations of Physiological Psychology (5th Ed.), pp. 355-395. Allyn and Bacon, MA: A Person Education Company.

11.

Collins, D. R., & Pare, D. (1999). Reciprocal changes in the firing probabilities lateral and central medial amygdala neurons. Journal of Neuroscience, 19(2), 836-844.

12.

Connell, K., Bolton, N., Olsen, D., Piomelli, D., & Hohmann A.G. (2006). Role of the basolateral nucleus of the amygdala in endocannabinoid-mediated stress-induced analgesia. Neuroscience Letters, 397, 180-184.

13.

De Olmos, J., Alheid, G.F., & Beltramino, C.A (1985). Amygdala, in G. Paxinos (Eds.), The rat nervous system: I. Forebrain and midbrain, Academic Press, New York.

14.

Dodd, J., Kelly, J. S., & Said, S. I. (1979). Excitation of CA1 neurons of the rat hippocampus by the octapeptide vasoactive intestinal polypeptide (VIP). British Journal of Pharmacology, 66(1), 125.

15.

Elphick, M. R., & Egartova, M. (2001). The neurobiology and evolution of cannabinoid signalling. Philosophical Transactions of the Royal Society of Lond, Series B, Biological Sciences, 356, 381-408.

16.

Fields, H. L., Heinricher, M. M., & Mason, P. (1991). Neurotransmitters in nociceptive modulatory circuits. Annual Review of Neuroscience, 14, 219-245.

17.

Gray, T. S., Cassell, M. D., & Williams, T. H. (1982). Synaptology of three peptidergic neuron types in the central nucleus of the rat amygdala. Peptides, 3, 273-281.

18.

Gray, T. S., & Magnuson, D. J. (1992). Peptide immunoreactive neurons in the amygdala and the bed nucleus of the stria terminalis project to the midbrain central gray in the rat. Peptides, 13, 451-460.

19.

Hasanein, P., Parviz., M., Keshavarz., M., & Javanmardi., K. (2007). CB1 receptor activation in the basolateral amygdala produces antinociception in animal models of acute and tonic nociception. Clinical and Experimental Pharmacology & Physiology, 34, 439-449.

20.

Helmstetter, F. J., & Bellgowan, P. S. (1994). Hypoalgesia in response to sensitization during acute noise stress. Behavioral Neuroscience, 108(1), 177-185.

21.

Helmstetter, F. J., Bellgowan, P. S. F,. & Poore, L. H. (1995). Microinfusion of mu but not delta or kappa agonists into the basolateral amygdala results in inhibition of the tail flick reflex in pentobarbital-anesthetized rats. Journal of Pharmacology & Experimental Therapeutics, 275, 381-388.

22.

Helmstetter, F. J., & Tershner, S. A. (1994). Lesions of the periaqueductal gray and rostral ventromedial medulla disrupt antinociception but not cardiovascular aversive conditional responses. Journal of Neuroscience, 14(11), 7099-7108.

23.

Helmstetter, F. J., Tershner, S. A., Poore, L. H., & Bellgowan, P. S. F. (1998). Antinociception following opioid stimulation of the basolateral amygdala is expressed through the periaqueductal gray and rostral ventromedial medulla. Brain Research, 779, 104-118.

24.

Herkenham, M, Lynn, A.B., Johnson, M.R., Melvin, L.S., De Costa, B.R, & Rice, K.C. (1991). Characterization and lateralization of cannabinoid receptors in the rat brain: A quantitative in vitro autoradiographic study. Journal of Neuroscience, 11, 563-583.

25.

Hohmann, A. G., Martin, W. J., Tsou, K., & Walker, J. M. (1995). Inhibition of noxious stimulus-evoked activity of spinal cord dorsal horn neurons by the cannabinoid WIN 55, 212-2. Life Sciences, 56, 2111-2118.

26.

Hohmann, A. G., Suplita, R. L., Bolton, N. M., Neely, M. H., Fegley, D., Mangieri, R., Krey, J. F., Walker, M., Holmes, P.V., Crystal, J. D., Duranti, A., Tontini, A., Mor, M., Tarzia, G., & Piomelli,D.(2005). An endocannabinoid mechanism for stress-induced analgesia. Nature, 435, 1108-1112.

27.

Hopkins, D. A., & Holstege, G. (1978). Amygdaloid projections to the mesencephalon, pons and medulla oblongata in the cat. Experimental Brain Research, 32, 529-547.

28.

Howlett, A. C., Blume, L. C., & Dalton, G. D. (2010). CB1 cannabinoid receptors and their associated proteins. Current Medicinal Chemistry, 17(14), 1382-1393.

29.

Kalivas, P. W., Gau, B. A., Nemeroff, C. B., & Prange, A. J., Jr. (1982). Antinociception after microinjection of neurotensin into the central amygdaloid nucleus of the rat. Brain Research, 243, 279-286.

30.

Kalyuzhny, A. E., & Wessendorf, M. W. (1998). Relationship of mu- and delta-opioid receptors to GABAergic neurons in the central nervous system, including antinociceptive brainstem circuits. The Journal of Comparative Neurology, 392, 528-547.

31.

Katona, I., Rancz, E.A., Acsady, L., Ledent, C., Mackie, K., Hajos, N., & Freund, T.F. (2001). Distribution of CB1 cannabinoid receptors in the amygdala and their role in the control of GABAergic transmission. The Journal of Neuroscience, 21(23), 9506-9518.

32.

Kurjak M., Hamel A. M., Allescher H.D., Schucdziarra V., & Storr M. (2008). Differential stimulatory effects of cannabinoids on VIP release and NO synthase activity in synaptosomal fractions from rat ileum. Neuropeptides, 42(5-6), 623-632.

33.

Li, A. H., Hwang, H.M., Tan, P. P., Wu, T., & Wang, H. L. (2001). Neurotensin excites periaqueductal gray neurons projecting to the rostral ventromedial medulla. Journal of Neurophysiology, 85(4), 1479-1488.

34.

Manning, B. H. (1998). A lateralized deficit in morphine antinociception after unilateral inactivation of the central amygdala. Journal of Neuroscience, 18(22), 9453-70.

35.

Manning, B. H., Martin, W. J., & Meng, I. D. (2003). The rodent amygdala contributes to the production of cannabinoid-induced antinociception. Neuroscience, 120, 1157-1170.

36.

Mansour A., Khachaturian H., Lewis M. E., Akil H., & Watson S. J. (1987). Autoradiographic differentiation of mu, delta and kappa opioid receptors in the rat forebrain and midbrain. Journal of Neuroscience, 7, 2445-2464.

37.

Manzanares, J., Corchero, J., Romero, J., Fernandez-Ruiz, J. J., Ramos, A., Fuentes, J. A. (1999). Pharmacological and biochemical interaction between opioids and cannabinoids. Tends in Pharmacological Sciences, 20, 287-294.

38.

Massi, P. Vaccani, A., Romorini, S. & Parolaro, D. (2001). Comparative characterization in the rat of the interaction between cannabinoids and opiates for their immunosopressive and analgesic effects. Journal of Neuroimmunology, 117(1-2), 116-124.

39.

McGaraughty, S., Farr, D.A., & Heinricher, M. M. (2004). Lesions of the periaqueductal gray disrupt input to the rostral ventromedial medulla following microinjections of morphine into the medial or basolateral nuclei of the amygdala. Brain Research, 1009, 223-227.

40.

Niteckam L., & Frotsch, M. (1988). Organization and synaptic interconnections of GABAergic and cholinergic elements in the rat amygdaloid nuclei: Single and double- immunolabelling studies. The Journal of Comparative Neurology, 279, 470-488.

41.

Pan, Z. Z (1998). Mu-opposing actions of the kappa-opioid receptor. Trends in Pharmacology and Sciences, 19, 94-98.

42.

Pare, D., & Smith, Y. (1993). The intercalated cell masses project to the central and medial nuclei of the amygdala in cats. Neuroscience, 57, 1077-1090.

43.

Reichling, D. B., Kwiat, G. C., & Basbaum, A. I. (1988). Anatomy, physiology and pharmacology of the periaqueductal gray contribution to antinociceptive controls. Progress in Brain Research, 77, 31-46.

44.

Pertwee, R. G. (2001). Cannabinoid receptors and pain. Progress in Neurobiology, 63(5), 569-611.

45.

Phillis, J. W., Kirkpatrick, J. R., & Said, S. I. (1978). Vasoactive intestinal peptide excitation of central neurons. Canadian Journal of Physiology & Pharmacology, 56, 337-340.

46.

Poore, L. H., & Helmstetter, F. J. (1994). Forebrain modulation of nociceptive reflex: Effects of GABA antagonists in the amygdala. Society for Neuroscience Abstracts, 20, 767.

47.

Reche, I., Fuentes J. A., & Ruiz-Gayo, M. (1996). Potentiation of delta 9-tetrahydrocannabinol- induced analgesia by morphine in mice: involvement of mu- and kappa-opioid receptors. European Journal of Pharmacology, 318(1), 11-16.

48.

Rizvi, T. A., Ennis, M., Behbehani, M. M., & Shipley, M. T. (1991). Connections between the central nucleus of the amygdala and the midbrain periaqueductal gray: Topography and reciprocity. The Journal of Comparative Neurology, 303, 121-131.

49.

Roberts, G. W., & Woodhams, P. L., Polak, J. M., & Crow, T. L. (1982). Distribution of neuropeptides in the limbic system of the rat: The amygdaloid complex. Neuroscience, 7,(1), 99-131.

50.

Shin, M.-S. (2002). Neuropeptide circuitry of the amygdala related to antinociception. Dissertation for Ph. D. at University of Wisconsin- Milwaukee.

51.

Shin, M.-S. (2005). Vasoactive intestinal peptide in the amygdala inhibits tail flick reflexes in rats. Brain Research, 1040, 197-201.

52.

Shin M. -S., Bailey, D. J., Hillard, C. J., & Helmstetter, F. J. (2008). Down regulating mu receptors in the basolateral complex of amygdala prevents antinociception in the rat. The Korean Journal of Experimental Psychology, 20(4), 285-301.

53.

Shin, M.-S., & Helmstetter, F. J. (1998). Effects of selective down-regulation of mu receptors in the basolateral amygdala with antisense oligonucleotides on antinociception. Society for Neuroscience Abstracts, 24, 447.1.

54.

Shin, M.-S, & Helmstetter, F. J. (2000). Pretreatment of the central, but not the basolateral, amygdala with muscimol blocks induction of mu-related antinociception following application of DAMGO. Society for Neuroscience Abstracts, 26, 244.12.

55.

Shin, M.-S., & Helmstetter, F. J. (2001). Vasoactive intestinal peptide interactions with mu opioids in the basolateral amygdala during antinociception. Society for Neuroscience Abstracts, 27, 509.16.

56.

Shin, M.-S., & Helmstetter, F. J. (2005). Antinociception following application of DAMGO to the basolateral amygdala results from a direct interaction of DAMGO with mu opioid receptors in the amygdala. Brain Research, 1064, 56-65.

57.

Smith, F. L., Cichewicz, D., Martin, Z. L., & Welch, S. P. (1998). The enhancement of morphine antinociception in mice by delta 9-tetrahydrocannabinol. Pharmacology, Biochemistry, and Behavior, 60(2), 559-566.

58.

Tershner, S. A., & Helmstetter, F. J. (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 Research, 865(1), 17-26.

59.

Young, W. S., & Kuhar, M. J. (1981). Neurotensin receptor localization by light microscopic autoradiography in rat brain. Brain Research, 206, 273-285.

60.

Vigano, D. Rubino, T. R., & Parolaro, D. (2005). Molecular and cellular basis of cannabinoid and opioid interactions. Pharmacology, Biochemistry and Behavior, 81, 360-368.

61.

Walker, J. M., & Huang, S. M. (2002). Endocannabinoids in pain modulation. Prostaglandins, Leukotrienes and Essential Fatty Acids, 66(2-3), 235-242.

62.

Zhu, P. J. & Lovinger, D. M. (2005). Retrograde cannabinoid signaling in a postsynaptic neuron/synaptic bouton preparation from basolateral amygdala. The Journal of Neuroscience, 25(26), 6199-6207.

63.

Zubieta, J-K., Smith, Y. R., Bueller, J. A., Xu, Y., Kilbourn, M. R., Jewett, D.M., Meyer, C. R., Koeppe, R. A., Stohler, C.S. (2001). Regional mu opioid receptor regulation of sensory and affective dimensions of pain. Science, 293, 311-315.

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