The midbrain periaqueductal gray and fear extinction: Opioid receptor subtype and roles of cyclic AMP, protein kinase A, and mitogen-activated protein kinase

Behavioral Neuroscience

Volumn 119, Issue 4, 2005, Pages 1023-1033

  McNally, Gavan P ^a   Lee, Boo Wahl ^a   Chiem, Janet Y ^a   Choi, Eun A ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

cAMP; Error correction; Extinction; Fear; Opioid

Indexed keywords

AMMONIUM DERIVATIVE; BINALTORPHIMINE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DERIVATIVE; DELTA OPIATE RECEPTOR; DELTA OPIATE RECEPTOR ANTAGONIST; DEXTRO PHENYLALANYLCYSTEINYLTYROSYL DEXTRO TRYPTOPHYLARGINYLTHREONYLPENICILLAMINYLTHREONINAMIDE 2,7 DISULFIDE; ENZYME ACTIVATOR; KAPPA OPIATE RECEPTOR; KAPPA OPIATE RECEPTOR ANTAGONIST; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MU OPIATE RECEPTOR; MU OPIATE RECEPTOR ANTAGONIST; NALTRINDOLE; PHOSPHOROTHIOIC ACID DERIVATIVE;

AMYGDALOID NUCLEUS; ANALGESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ERROR; FEAR; INFUSION; MALE; MESENCEPHALON; MICROINJECTION; NONHUMAN; PERIAQUEDUCTAL GRAY MATTER; RAT; REINFORCEMENT; SIGNAL TRANSDUCTION;

ANALYSIS OF VARIANCE; ANIMALS; BEHAVIOR, ANIMAL; CONDITIONING, CLASSICAL; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ENZYME INHIBITORS; EXTINCTION, PSYCHOLOGICAL; FEAR; FREEZING REACTION, CATALEPTIC; MALE; MICROINJECTIONS; MITOGEN-ACTIVATED PROTEIN KINASES; NARCOTIC ANTAGONISTS; PERIAQUEDUCTAL GRAY; RATS; RATS, WISTAR; RECEPTORS, OPIOID; TIME FACTORS;

EID: 25444461108     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/0735-7044.119.4.1023     Document Type: Article

References (61)

1. Ai, W., Gong, I., & Yu, L. (1999). MAP kinase activation by μ-opioid receptor involves phosphatidylinositol 3-kinase but not the cAMP/PKA pathway. FEBS Letters, 456, 196-200.
2. Arntz, A., Merkelbach, H., & de Jong, P. (1993). Opioid antagonist affects behavioral effects of exposure in vivo. Journal of Consulting and Clinical Psychology, 61, 865-870.
3. Bailey, C. H., Bartsch, D., & Kandel, E. R. (1996). Toward a molecular definition of long-term memory storage. Proceedings of the National Academy of Sciences, USA, 93, 13445-13452.
4. Chieng, B., & Christie, M. J. (1994). Inhibition by opioids acting on μ-receptors of GABAergic and glutamatergic postsynaptic potentials in single rat periaqueductal gray neurones in vitro. British Journal of Pharmacology, 113, 303-309.
5. Commons, K. G. (2003). Translocation of presynaptic delta opioid receptors in the ventrolateral periaqueductal gray after swim stress. Journal of Comparative Neurology, 464, 197-207.
6. 2+ channel currents of acutely dissociated rat periaqueductal grey neurons. Journal of Physiology, 509, 47-58.
7. Davis, M. (1992). The role of the amygdala in fear and anxiety. Annual Review of Neuroscience, 15, 353-375.
8. Davis, M. (2002). Role of NMDA receptors and MAP kinase in the amygdala in extinction of fear: Clinical implications for exposure therapy. European Journal of Neuroscience, 16, 395-398.
9. Davis, M. I., Ronesi, J., & Lovinger, D. M. (2003). A predominant role for inhibition of adenylate cyclase/protein kinase A pathway in ERK activation by cannabinoid 1 receptor 1 in N1E-115 neuroblastoma cells. Journal of Biological Chemistry, 278, 48973-48980.
10. Delamater, A. R. (2004). Experimental extinction in Pavlovian conditioning: Behavioural and neuroscience perspectives. Quarterly Journal of Experimental Psychology: Journal of Comparative and Physiological Psychology, 57(B), 97-132.
11. Egan, K. J., Carr, J. E., Hunt, D. D., & Adamson, R. (1988). Endogenous opiate system and systematic desensitization. Journal of Consulting and Clinical Psychology, 56, 287-291.
12. Eitan, S., Bryant, C. D., Saliminejad, N., Yang, Y. C., Vojdani, E., Keith, D., et al. (2003). Brain region-specific mechanisms for acute morphine-induced mitogen-activated protein kinase modulation and distinct patterns of activation during analgesic tolerance and locomotor sensitisation. Journal of Neuroscience, 23, 8360-8369.
13. Falls, W. A., Miserendino, M. J., & Davis, M. (1992). Extinction of fear-potentiated startle: Blockade by infusion of an NMDA antagonist into the amygdala. Journal of Neuroscience, 12, 854-863.
14. Fanselow, M. S., Kim, J. J., Young, S. L., Calcagnetti, D. J., DeCola, J. P., Helmstetter, F. J., & Landeira-Fernandez, J. (1991). Differential effects of selective opioid peptide antagonists on the acquisition of Pavlovian fear conditioning. Peptides, 12, 1033-1037.
15. Fanselow, M. S., & LeDoux, J. E. (1999). Why we think plasticity underlying Pavlovian fear conditioning occurs in the basolateral amygdala. Neuron, 23, 229-232.
16. Fendt, M., & Fanselow, M. S. (1999). The neuroanatomical and neurochemical basis of conditioned fear. Neuroscience & Biobehavioral Reviews, 23, 743-760.
17. Fields, H. (2004). State-dependent opioid control of pain. Nature Reviews Neuroscience, 5, 565-575.
18. Fukuda, K., Kato, S., Morikawa, H., Shoda, T., & Mori, K. (1996). Functional coupling of the delta-, mu-, and kappa-opioid receptors to mitogen-activated protein kinase and arachidonate release in Chinese hamster ovary cells. Journal of Neurochemistry, 67, 1309-1316.
19. Hammer, G. D., & Kapp, B. S. (1986). The effects of naloxone administered into the periaqueductal gray on shock-elicited freezing behavior in the rat. Behavioral and Neural Biology, 46, 189-195.
20. Herry, C., & Garcia, R. (2002). Prefrontal cortex long-term potentiation, but not long-term depression, is associated with the maintenance of extinction of learned fear in mice. Journal of Neuroscience, 22, 577-583.
21. Ignatova, E. G., Belcheva, M. M., Bohn, L. M., Neuman, M. C., & Coscia, C. J. (1999). Requirement of receptor internalization for opioid stimulation of mitogen-activated protein kinase: Biochemical and immunofluorescence confocal microscopic evidence. Journal of Neuroscience, 19, 56-63.
22. Ingram, S. L., Vaughan, C. W., Bagley, E. E., Connor, M., & Christie, M. J. (1998). Enhanced opioid efficacy in opioid dependence is caused by an altered signal transduction pathway. Journal of Neuroscience, 18, 10269-10276.
23. h via adenylyl cyclase. Neuron, 13, 179-186.
24. Kandel, E. R. (2001, November 2). The molecular biology of memory storage: A dialogue between genes and synapses. Science, 294, 1030-1038.
25. Kramer, H. K., & Simon, E. J. (2000). Mu and delta-opioid receptor agonists induce mitogen-activated protein kinase (MAPK) activation in the absence of receptor internalization. Neuropharmacology, 39, 1707-1719.
26. Li, L. Y., & Chang, K. J. (1996). The stimulatory effect of opioids on mitogen-activated protein kinase in Chinese hamster ovary cells transfected to express mu-opioid receptors. Molecular Pharmacology, 50, 599-602.
27. Lin, C. H., Yen, S. H., & Gean, P. W. (2003). The similarities and diversities of signal pathways leading to consolidation of conditioning and consolidation of extinction of fear memory. Journal of Neuroscience, 23, 8310-8317.
28. Lovibond, P. F., Davis, N. R., & O'Flaherty, A. S. (2000). Protection from extinction in human fear conditioning. Behavior Research & Therapy, 38, 967-983.
29. Lu, K. T., Walker, D. L., & Davis, M. (2001). Mitogen-activated protein kinase cascade in the basolateral nucleus of the amygdala is involved in extinction of fear-potentiated startle. Journal of Neuroscience, 21, RC162.
30. Mansour, A., Hoversten, M. T., Taylor, L. P., Watson, S. J., & Akil, H. (1995). The cloned μ, δ, and κ receptors and their endogenous ligands: Evidence for two opioid peptide recognition cores. Brain Research, 700, 89-98.
31. Maren, S. (2001). Neurobiology of Pavlovian fear conditioning. Annual Review of Neuroscience, 24, 897-931.
32. McNally, G. P., & Akil, H. (2002). Opioid peptides and their receptors: Overview and function in pain modulation. In K. Davis, D. Charney, J. T. Coyle, & C. Nemeroff (Eds.), Neuropsychopharmacology: A fifth generation of progress (pp. 35-46). New York: Lippincott Williams & Wilkins.
33. McNally, G. P., Pigg, M., & Weidemann, G. (2004a). Blocking, unblocking and overexpectation of fear: Opioid receptors regulate Pavlovian association formation. Behavioral Neuroscience, 118, 111-120.
34. McNally, G. P., Pigg, M., & Weidemann, G. (2004b). Opioid receptors in the midbrain periaqueductal gray regulate extinction of Pavlovian fear conditioning. Journal of Neuroscience, 24, 6912-6919.
35. McNally, G. P., & Westbrook, R. F. (2003). Opioid receptors regulate the extinction of Pavlovian fear conditioning. Behavioral Neuroscience, 117, 1292-1301.
36. Merluzzi, T. V., Taylor, C. B., Boltwood, M., & Götestam, K. G. (1991). Opioid antagonist impedes exposure. Journal of Consulting and Clinical Psychology, 59, 425-430.
37. Milad, M. R., & Quirk, G. J. (2002, November 7). Neurons in medial prefrontal cortex signal memory for fear extinction. Nature, 420, 70-74.
38. Myers, K. M., & Davis, M. (2002). Behavioral and neural analysis of extinction. Neuron, 36, 567-584.
39. National Institutes of Health. (1986). Guide for the care and use of laboratory animals {Publication No. 86-23). Institute of Laboratory Animal Resources Commission on Life Sciences, National Research Council. Washington, DC: National Academy Press.
40. O'Brien, R. G., & Kaiser, M. K. (1985). MANOVA method for analyzing repeated measures designs: An extensive primer. Psychological Bulletin, 97, 316-333.
41. Ozaki, S., Narita, M., Ozaki, M., Khotib, J., & Suzuki, T. (2004). Role of extracellular signal-regulated kinase in the ventral tegmental area in the suppression of the morphine-induced rewarding effect in mice with sciatic nerve ligation. Journal of Neurochemistry, 88, 1389-1397.
42. Paxinos, G., & Watson, C. (1998). The rat brain in stereotaxic coordinates (4th ed.). New York: Academic Press.
43. Punch, L. J., Self, D. W., Nestler, E. J., & Taylor, J. R. (1997). Opposite modulation of opiate withdrawal behaviors on microinfusion of a protein kinase A inhibitor versus activator into the locus coeruleus or periaqueductal gray. Journal of Neuroscience, 17, 8520-8527.
44. Quirk, G. J., Russo, G. K., Barron, J. L., & Lebron, K. (2000). The role of the ventromedial prefrontal cortex in the recovery of extinguished fear. Journal of Neuroscience, 20, 6225-6231.
45. Rescorla, R. A. (2000). Extinction can be enhanced by a concurrent excitor. Journal of Experimental Psychology: Animal Behavior Processes, 26, 251-260.
46. Rescorla, R. A. (2001). Experimental extinction. In R. R. Mowrer & S. B Klein (Eds.), Handbook of contemporary learning theories (pp. 119-154). Hillsdale, NJ: Erlbaum.
47. Rescorla, R. A. (2003). Protection from extinction. Learning & Behavior, 31, 124-132.
48. Rescorla, R. A. (2004). Spontaneous recovery. Learning & Memory, 11, 501-509.
49. Rescorla, R. A., & Wagner, A. R. (1972). A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. In A. H. Black & W. F. Prokasy (Eds.), Classical conditioning II: Current research and theory (pp. 64-99). New York: Appleton-Century-Crofts.
50. Ressler, K. J., Rothbaum, B. O., Tannenbaum, L., Anderson, P., Graap, K., Zimand, E., et al. (2004). Cognitive enhancers as adjuncts to psychotherapy: Use of D-cycloserine in phobic individuals to facilitate extinction of fear. Archives of General Psychiatry, 61, 1136-1144.
51. Schafe, G. E., Atkins, C. M., Swank, M. W., Bauer, E. P., Sweatt, J. D., & Le Doux, J. E. (2000). Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of Pavlovian fear conditioning. Journal of Neuroscience, 20, 8177-8187,
52. Sharma, S. K., & Carew, T. J. (2004). The roles of MAPK cascades in synaptic plasticity and memory in Aplyisa: Facilitatory effects and inhibitory constraints. Learning & Memory, 11, 373-378.
53. Szapiro, G., Vianna, M. R., McGaugh, J. L., Medina, J. H., & Izquierdo, I. (2003). The role of NMDA glutamate receptors, PKA, MAPK, and CAMKII in the hippocampus in extinction of conditioned fear. Hippocampus, 13, 53-58.
54. Thomas, B. L., & Ayres, J. J. B. (2004). Use of the ABA fear renewal paradigm to assess the effects of extinction with co-present fear inhibitors or excitors: Implications for theories of extinction and for treating human fears and phobias. Learning and Motivation, 35, 22-52.
55. Vaughan, C. W., & Christie, M. J. (1997). Presynaptic inhibitory action of opioids on synaptic transmission in the rat periaqueductal grey in vitro. Journal of Physiology, 498, 463-472.
56. Vaughan, C. W., Ingram, S. L., Connor, M. A., & Christie, M. J. (1997, December 11). How opioids inhibit GABA-mediated neurotransmission. Nature. 390, 611-614.
57. Wagner, A. R. (1969). Stimulus selection and modified contiguity theory. In G. H. Bower & J. T. Spence (Eds.), The psychology of learning and motivation (Vol 3., pp. 1-41). New York: Academic Press.
58. Wagner, A. R., & Rescorla, R. A. (1972). Inhibition in Pavlovian conditioning: Application of a theory. In R. A. Boakes & M. S. Halliday (Eds.), Inhibition and learning (pp. 301-336). New York: Academic Press.
59. Walker, D. L., Ressler, K. J., Lu, K. T., & Davis, M. (2002). Facilitation of conditioned fear extinction by systemic administration or intra-amygdala infusions of D-cycloserine as assessed with fear-potentiated startle in rats. Journal of Neuroscience, 22, 2343-2351.
60. Williams, J. T., Christie, M. J., & Manzoni, O. (2001). Cellular and synaptic adaptations mediating opioid dependence. Physiological Reviews, 81, 299-343.
61. Young, S. L., & Fanselow, M. S. (1992). Associative regulation of Pavlovian fear conditioning: Unconditional stimulus intensity, incentive shifts, and latent inhibition. Journal of Experimental Psychology: Animal Behavior Processes, 18, 400-413.