Effect of D-cycloserine in conjunction with fear extinction training on extracellular signal-regulated kinase activation in the medial prefrontal cortex and amygdala in rat

European Journal of Neuroscience

Volumn 37, Issue 11, 2013, Pages 1811-1822

  Gupta, Subhash C ^a   Hillman, Brandon G ^a   Prakash, Anand ^a,b   Ugale, Rajesh R ^c   Stairs, Dustin J ^a   Dravid, Shashank M ^a  

^a CREIGHTON UNIVERSITY   (United States)

^b BABASAHEB BHIMRAO AMBEDKAR UNIVERSITY   (India)

^c GURU GHASIDAS UNIVERSITY   (India)

Author keywords

Bed nucleus of the stria terminalis intra amygdaloid division; Infralimbic cortex; Ionotropic Glutamate Receptors; Prelimbic cortex; Synaptic plasticity

Indexed keywords

AMPA RECEPTOR; CYCLOSERINE; IONOTROPIC RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN C FOS;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; CELL ACTIVITY; CONTROLLED STUDY; FEAR; HYPOTHALAMUS; LATERAL AMYGDALA; LATERAL HYPOTHALAMUS; MALE; NERVE CELL PLASTICITY; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SYNAPSE;

AMYGDALA; ANIMALS; CARRIER PROTEINS; CYCLOSERINE; EXTINCTION, PSYCHOLOGICAL; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEAR; MALE; NERVE TISSUE PROTEINS; NEURONS; PREFRONTAL CORTEX; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84878517979     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12197     Document Type: Article

References (98)

1. Akirav, I., Raizel, H. & Maroun, M. (2006) Enhancement of conditioned fear extinction by infusion of the GABA (A) agonist muscimol into the rat prefrontal cortex and amygdala. Eur. J. Neurosci., 23, 758-764.
2. Amano, T., Unal, C.T. & Pare, D. (2010) Synaptic correlates of fear extinction in the amygdala. Nat. Neurosci., 13, 489-494.
3. Aupperle, R.L., Hale, L.R., Chambers, R.J., Cain, S.E., Barth, F.X., Sharp, S.C., Denney, D.R. & Savage, C.R. (2009) An fMRI study examining effects of acute D-cycloserine during symptom provocation in spider phobia. CNS Spectr., 14, 556-571.
4. Baker, J.D. & Azorlosa, J.L. (1996) The NMDA antagonist MK-801 blocks the extinction of Pavlovian fear conditioning. Behav. Neurosci., 110, 618-620.
5. Barrett, D., Shumake, J., Jones, D. & Gonzalez-Lima, F. (2003) Metabolic mapping of mouse brain activity after extinction of a conditioned emotional response. J. Neurosci., 23, 5740-5749.
6. Bauer, E.P., Schafe, G.E. & LeDoux, J.E. (2002) NMDA receptors and L-type voltage-gated calcium channels contribute to long-term potentiation and different components of fear memory formation in the lateral amygdala. J. Neurosci., 22, 5239-5249.
7. Berlau, D.J. & McGaugh, J.L. (2006) Enhancement of extinction memory consolidation: the role of the noradrenergic and GABAergic systems within the basolateral amygdala. Neurobiol. Learn. Mem., 86, 123-132.
8. Bertotto, M.E., Bustos, S.G., Molina, V.A. & Martijena, I.D. (2006) Influence of ethanol withdrawal on fear memory: effect of D-cycloserine. Neuroscience, 142, 979-990.
9. Bouton, M.E. & King, D.A. (1983) Contextual control of the extinction of conditioned fear: tests for the associative value of the context. J. Exp. Psychol. Anim. B., 9, 248-265.
10. Brambilla, R., Gnesutta, N., Minichiello, L., White, G., Roylance, A.J., Herron, C.E., Ramsey, M., Wolfer, D.P., Cestari, V., Rossi-Arnaud, C., Grant, S.G., Chapman, P.F., Lipp, H.P., Sturani, E. & Klein, R. (1997) A role for the ras signalling pathway in synaptic transmission and long-term memory. Nature, 390, 281-286.
11. Bullitt, E. (1990) Expression of c-fos-like protein as a marker for neuronal activity following noxious stimulation in the rat. J. Comp. Neurol., 296, 517-530.
12. 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. Learn. Memory, 11, 625-632.
13. Chang, C.H. & Maren, S. (2011) Medial prefrontal cortex activation facilitates re-extinction of fear in rats. Learn. Memory, 18, 221-225.
14. Chang, C.H., Berke, J.D. & Maren, S. (2010) Single-unit activity in the medial prefrontal cortex during immediate and delayed extinction of fear in rats. PLoS ONE, 5, e11971.
15. Chen, X., Garelick, M.G., Wang, H., Lil, V., Athos, J. & Storm, D.R. (2005) PI3 kinase signaling is required for retrieval and extinction of contextual memory. Nat. Neurosci., 8, 925-931.
16. Corcoran, K.A., Desmond, T.J., Frey, K.A. & Maren, S. (2005) Hippocampal inactivation disrupts the acquisition and contextual encoding of fear extinction. J. Neurosci., 25, 8978-8987.
17. Cox, J. & Westbrook, R.F. (1994) The NMDA receptor antagonist MK-801 blocks acquisition and extinction of conditioned hypoalgesic responses in the rat. Q. J. Exp. Psychol.-B., 47, 187-210.
18. Dalton, G.L., Wu, D.C., Wang, Y.T., Floresco, S.B. & Phillips, A.G. (2012) NMDA GluN2A and GluN2B receptors play separate roles in the induction of LTP and LTD in the amygdala and in the acquisition and extinction of conditioned fear. Neuropharmacology, 62, 797-806.
19. Davis, M. & Myers, K.M. (2002) The role of glutamate and gamma-aminobutyric acid in fear extinction: clinical implications for exposure therapy. Biol. Psychiat., 52, 998-1007.
20. Farinelli, M., Deschaux, O., Hugues, S., Thevenet, A. & Garcia, R. (2006) Hippocampal train stimulation modulates recall of fear extinction independently of prefrontal cortex synaptic plasticity and lesions. Learn. Memory, 13, 329-334.
21. Fischer, A., Radulovic, M., Schrick, C., Sananbenesi, F., Godovac-Zimmermann, J. & Radulovic, J. (2007) Hippocampal Mek/Erk signaling mediates extinction of contextual freezing behavior. Neurobiol. Learn. Mem., 87, 149-158.
22. Gabbott, P.L., Warner, T.A., Jays, P.R., Salway, P. & Busby, S.J. (2005) Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J. Comp. Neurol., 492, 145-177.
23. Ganasen, K.A., Ipser, J.C. & Stein, D.J. (2010) Augmentation of cognitive behavioral therapy with pharmacotherapy. Psychiat. Clin. N. Am., 33, 687-699.
24. Gisquet-Verrier, P. & Delatour, B. (2006) The role of the rat prelimbic/infralimbic cortex in working memory: not involved in the short-term maintenance but in monitoring and processing functions. Neuroscience, 141, 585-596.
25. Gourley, S.L., Kedves, A.T., Olausson, P. & Taylor, J.R. (2009) A history of corticosterone exposure regulates fear extinction and cortical NR2B, GluR2/3, and BDNF. Neuropsychopharmacol., 34, 707-716.
26. Hampson, D.R., Huang, X.P., Oberdorfer, M.D., Goh, J.W., Auyeung, A. & Wenthold, R.J. (1992) Localization of AMPA receptors in the hippocampus and cerebellum of the rat using an anti-receptor monoclonal antibody. Neuroscience, 50, 11-22.
27. 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. J. Neurosci., 22, 577-583.
28. Herry, C. & Mons, N. (2004) Resistance to extinction is associated with impaired immediate early gene induction in medial prefrontal cortex and amygdala. Eur. J. Neurosci., 20, 781-790.
29. Herry, C., Trifilieff, P., Micheau, J., Luthi, A. & Mons, N. (2006) Extinction of auditory fear conditioning requires MAPK/ERK activation in the basolateral amygdala. Eur. J. Neurosci., 24, 261-269.
30. Heynen, A.J., Quinlan, E.M., Bae, D.C. & Bear, M.F. (2000) Bidirectional, activity-dependent regulation of glutamate receptors in the adult hippocampus in vivo. Neuron, 28, 527-536.
31. Ho, Y.J., Hsu, L.S., Wang, C.F., Hsu, W.Y., Lai, T.J., Hsu, C.C. & Tsai, Y.F. (2005) Behavioral effects of d-cycloserine in rats: the role of anxiety level. Brain Res., 1043, 179-185.
32. Hofmann, S.G., Pollack, M.H. & Otto, M.W. (2006) Augmentation treatment of psychotherapy for anxiety disorders with D-cycloserine. CNS Drug Rev., 12, 208-217.
33. Hollingsworth, E.B., McNeal, E.T., Burton, J.L., Williams, R.J., Daly, J.W. & Creveling, C.R. (1985) Biochemical characterization of a filtered synaptoneurosome preparation from guinea pig cerebral cortex: cyclic adenosine 3′:5′-monophosphate-generating systems, receptors, and enzymes. J. Neurosci., 5, 2240-2253.
34. Hugues, S. & Garcia, R. (2007) Reorganization of learning-associated prefrontal synaptic plasticity between the recall of recent and remote fear extinction memory. Learn. Memory, 14, 520-524.
35. Hugues, S., Deschaux, O. & Garcia, R. (2004) Postextinction infusion of a mitogen-activated protein kinase inhibitor into the medial prefrontal cortex impairs memory of the extinction of conditioned fear. Learn. Memory, 11, 540-543.
36. Hugues, S., Chessel, A., Lena, I., Marsault, R. & Garcia, R. (2006) Prefrontal infusion of PD098059 immediately after fear extinction training blocks extinction-associated prefrontal synaptic plasticity and decreases prefrontal ERK2 phosphorylation. Synapse, 60, 280-287.
37. Jacome, L.F., Burket, J.A., Herndon, A.L. & Deutsch, S.I. (2011) D-Cycloserine enhances social exploration in the Balb/c mouse. Brain Res. Bull., 85, 141-144.
38. Kandel, E.R. (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science, 294, 1030-1038.
39. Kelleher, R.J. 3rd., Govindarajan, A., Jung, H.Y., Kang, H. & Tonegawa, S. (2004) Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell, 116, 467-479.
40. Kim, J., Lee, S., Park, K., Hong, I., Song, B., Son, G., Park, H., Kim, W.R., Park, E., Choe, H.K., Kim, H., Lee, C., Sun, W., Kim, K., Shin, K. & Choi, S. (2007) Amygdala depotentiation and fear extinction. Proc. Natl. Acad. Sci. USA, 104, 20955-20960.
41. Kim, J.H., Hamlin, A.S. & Richardson, R. (2009) Fear extinction across development: the involvement of the medial prefrontal cortex as assessed by temporary inactivation and immunohistochemistry. J. Neurosci., 29, 10802-10808.
42. Kim, S.C., Jo, Y.S., Kim, I.H., Kim, H. & Choi, J.S. (2010) Lack of medial prefrontal cortex activation underlies the immediate extinction deficit. J. Neurosci., 30, 832-837.
43. Kinon, B.J. & Lieberman, J.A. (1996) Mechanisms of action of atypical antipsychotic drugs: a critical analysis. Psychopharmacology, 124, 2-34.
44. Knapska, E. & Maren, S. (2009) Reciprocal patterns of c-fos expression in the medial prefrontal cortex and amygdala after extinction and renewal of conditioned fear. Learn. Memory, 16, 486-493.
45. Kontkanen, O., Lakso, M., Wong, G. & Castren, E. (2002) Chronic antipsychotic drug treatment induces long-lasting expression of fos and jun family genes and activator protein 1 complex in the rat prefrontal cortex. Neuropsychopharmacol., 27, 152-162.
46. Laroche, S., Davis, S. & Jay, T.M. (2000) Plasticity at hippocampal to prefrontal cortex synapses: dual roles in working memory and consolidation. Hippocampus, 10, 438-446.
47. Laurent, V. & Westbrook, R.F. (2009) Inactivation of the infralimbic but not the prelimbic cortex impairs consolidation and retrieval of fear extinction. Learn. Memory, 16, 520-529.
48. Laurent, V., Marchand, A.R. & Westbrook, R.F. (2008) The basolateral amygdala is necessary for learning but not relearning extinction of context conditioned fear. Learn. Memory, 15, 304-314.
49. Ledgerwood, L., Richardson, R. & Cranney, J. (2003) Effects of D-cycloserine on extinction of conditioned freezing. Behav. Neurosci., 117, 341-349.
50. Ledgerwood, L., Richardson, R. & Cranney, J. (2004) D-cycloserine and the facilitation of extinction of conditioned fear: consequences for reinstatement. Behav. Neurosci., 118, 505-513.
51. LeDoux, J.E. (2000) Emotion circuits in the brain. Annu. Rev. Neurosci., 23, 155-184.
52. Likhtik, E., Popa, D., Apergis-Schoute, J., Fidacaro, G.A. & Pare, D. (2008) Amygdala intercalated neurons are required for expression of fear extinction. Nature, 454, 642-645.
53. Lin, C.H., Lee, C.C. & Gean, P.W. (2003) Involvement of a calcineurin cascade in amygdala depotentiation and quenching of fear memory. Mol. Pharmacol., 63, 44-52.
54. Lin, H.C., Mao, S.C., Su, C.L. & Gean, P.W. (2010) Alterations of excitatory transmission in the lateral amygdala during expression and extinction of fear memory. Int. J. Neuropsychop., 13, 335-345.
55. Lu, K.T., Walker, D.L. & Davis, M. (2001) Mitogen-activated protein kinase cascade in the basolateral nucleus of amygdala is involved in extinction of fear-potentiated startle. J. Neurosci., 21, RC162.
56. Mao, S.C., Hsiao, Y.H. & Gean, P.W. (2006) Extinction training in conjunction with a partial agonist of the glycine site on the NMDA receptor erases memory trace. J. Neurosci., 26, 8892-8899.
57. Maren, S. & Quirk, G.J. (2004) Neuronal signalling of fear memory. Nat. Rev. Neurosci., 5, 844-852.
58. McDonald, A.J. (1996) Localization of AMPA glutamate receptor subunits in subpopulations of non-pyramidal neurons in the rat basolateral amygdala. Neurosci. Lett., 208, 175-178.
59. McDonald, A.J. (1998) Cortical pathways to the mammalian amygdala. Prog. Neurobiol., 55, 257-332.
60. Milad, M.R. & Quirk, G.J. (2002) Neurons in medial prefrontal cortex signal memory for fear extinction. Nature, 420, 70-74.
61. Miserendino, M.J., Sananes, C.B., Melia, K.R. & Davis, M. (1990) Blocking of acquisition but not expression of conditioned fear-potentiated startle by NMDA antagonists in the amygdala. Nature, 345, 716-718.
62. Morgan, M.A., Romanski, L.M. & LeDoux, J.E. (1993) Extinction of emotional learning: contribution of medial prefrontal cortex. Neurosci. Lett., 163, 109-113.
63. Morgan, M.A., Schulkin, J. & LeDoux, J.E. (2003) Ventral medial prefrontal cortex and emotional perseveration: the memory for prior extinction training. Behav. Brain Res., 146, 121-130.
64. Myers, K.M. & Carlezon, W.A. Jr. (2012) D-cycloserine effects on extinction of conditioned responses to drug-related cues. Biol. Psychiat., 71, 947-955.
65. Papp, M. & Moryl, E. (1996) Antidepressant-like effects of 1-aminocyclopropanecarboxylic acid and D-cycloserine in an animal model of depression. Eur. J. Pharmacol., 316, 145-151.
66. Pare, D., Quirk, G.J. & Ledoux, J.E. (2004) New vistas on amygdala networks in conditioned fear. J. Neurophysiol., 92, 1-9.
67. Park, J. & Choi, J.S. (2009) Long-term synaptic changes in two input pathways into the lateral nucleus of the amygdala underlie fear extinction. Learn. Memory, 17, 23-34.
68. Paxinos, G. & Watson, C. (2005) The Rat Brain in Stereotaxic Coordinates, 5th Edn. Academic Press, Salt Lake City.
69. Peters, J., Kalivas, P.W. & Quirk, G.J. (2009) Extinction circuits for fear and addiction overlap in prefrontal cortex. Learn. Memory, 16, 279-288.
70. Phelps, E.A. & LeDoux, J.E. (2005) Contributions of the amygdala to emotion processing: from animal models to human behavior. Neuron, 48, 175-187.
71. Quirk, G.J., Likhtik, E., Pelletier, J.G. & Pare, D. (2003) Stimulation of medial prefrontal cortex decreases the responsiveness of central amygdala output neurons. J. Neurosci., 23, 8800-8807.
72. Quirk, G.J., Garcia, R. & Gonzalez-Lima, F. (2006) Prefrontal mechanisms in extinction of conditioned fear. Biol. Psychiat., 60, 337-343.
73. Ressler, K.J., Rothbaum, B.O., Tannenbaum, L., Anderson, P., Graap, K., Zimand, E., Hodges, L. & Davis, M. (2004) Cognitive enhancers as adjuncts to psychotherapy: use of D-cycloserine in phobic individuals to facilitate extinction of fear. Arch. Gen. Psychiat., 61, 1136-1144.
74. Richardson, R., Ledgerwood, L. & Cranney, J. (2004) Facilitation of fear extinction by D-cycloserine: theoretical and clinical implications. Learn. Memory, 11, 510-516.
75. Robertson, G.S. & Fibiger, H.C. (1992) Neuroleptics increase c-fos expression in the forebrain: contrasting effects of haloperidol and clozapine. Neuroscience, 46, 315-328.
76. Romcy-Pereira, R. & Pavlides, C. (2004) Distinct modulatory effects of sleep on the maintenance of hippocampal and medial prefrontal cortex LTP. Eur. J. Neurosci., 20, 3453-3462.
77. Rosenkranz, J.A. & Grace, A.A. (2001) Dopamine attenuates prefrontal cortical suppression of sensory inputs to the basolateral amygdala of rats. J. Neurosci., 21, 4090-4103.
78. Rosenkranz, J.A., Moore, H. & Grace, A.A. (2003) The prefrontal cortex regulates lateral amygdala neuronal plasticity and responses to previously conditioned stimuli. J. Neurosci., 23, 11054-11064.
79. Royer, S. & Pare, D. (2002) Bidirectional synaptic plasticity in intercalated amygdala neurons and the extinction of conditioned fear responses. Neuroscience, 115, 455-462.
80. Santini, E., Muller, R.U. & Quirk, G.J. (2001) Consolidation of extinction learning involves transfer from NMDA-independent to NMDA-dependent memory. J. Neurosci., 21, 9009-9017.
81. Santini, E., Ge, H., Ren, K., Pena de Ortiz, S. & Quirk, G.J. (2004) Consolidation of fear extinction requires protein synthesis in the medial prefrontal cortex. J. Neurosci., 24, 5704-5710.
82. Santini, E., Quirk, G.J. & Porter, J.T. (2008) Fear conditioning and extinction differentially modify the intrinsic excitability of infralimbic neurons. J. Neurosci., 28, 4028-4036.
83. Schafe, G.E., Atkins, C.M., Swank, M.W., Bauer, E.P., Sweatt, J.D. & LeDoux, J.E. (2000) Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of pavlovian fear conditioning. J. Neurosci., 20, 8177-8187.
84. Sesack, S.R., Deutch, A.Y., Roth, R.H. & Bunney, B.S. (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J. Comp. Neurol., 290, 213-242.
85. Sierra-Mercado, D. Jr., Corcoran, K.A., Lebron-Milad, K. & Quirk, G.J. (2006) Inactivation of the ventromedial prefrontal cortex reduces expression of conditioned fear and impairs subsequent recall of extinction. Eur. J. Neurosci., 24, 1751-1758.
86. Sierra-Mercado, D., Padilla-Coreano, N. & Quirk, G.J. (2011) Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacol., 36, 529-538.
87. Sotres-Bayon, F. & Quirk, G.J. (2010) Prefrontal control of fear: more than just extinction. Curr. Opin. Neurobiol., 20, 231-235.
88. Sotres-Bayon, F., Bush, D.E. & LeDoux, J.E. (2007) Acquisition of fear extinction requires activation of NR2B-containing NMDA receptors in the lateral amygdala. Neuropsychopharmacol., 32, 1929-1940.
89. Thomas, G.M. & Huganir, R.L. (2004) MAPK cascade signalling and synaptic plasticity. Nat. Rev. Neurosci., 5, 173-183.
90. Thompson, B.M., Baratta, M.V., Biedenkapp, J.C., Rudy, J.W., Watkins, L.R. & Maier, S.F. (2010) Activation of the infralimbic cortex in a fear context enhances extinction learning. Learn. Memory, 17, 591-599.
91. Trifilieff, P., Herry, C., Vanhoutte, P., Caboche, J., Desmedt, A., Riedel, G., Mons, N. & Micheau, J. (2006) Foreground contextual fear memory consolidation requires two independent phases of hippocampal ERK/CREB activation. Learn. Memory, 13, 349-358.
92. Tronson, N.C., Schrick, C., Guzman, Y.F., Huh, K.H., Srivastava, D.P., Penzes, P., Guedea, A.L., Gao, C. & Radulovic, J. (2009) Segregated populations of hippocampal principal CA1 neurons mediating conditioning and extinction of contextual fear. J. Neurosci., 29, 3387-3394.
93. Villasana, L.E., Klann, E. & Tejada-Simon, M.V. (2006) Rapid isolation of synaptoneurosomes and postsynaptic densities from adult mouse hippocampus. J. Neurosci. Meth., 158, 30-36.
94. 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. J. Neurosci., 22, 2343-2351.
95. Wu, S.L., Hsu, L.S., Tu, W.T., Wang, W.F., Huang, Y.T., Pawlak, C.R. & Ho, Y.J. (2008) Effects of D-cycloserine on the behavior and ERK activity in the amygdala: role of individual anxiety levels. Behav. Brain Res., 187, 246-253.
96. Xu, T. & Pandey, S.C. (2000) Cellular localization of serotonin(2A) (5HT(2A)) receptors in the rat brain. Brain Res. Bull., 51, 499-505.
97. Yadav, R., Gupta, S.C., Hillman, B.G., Bhatt, J.M., Stairs, D.J. & Dravid, S.M. (2012) Deletion of glutamate delta-1 receptor in mouse leads to aberrant emotional and social behaviors. PLoS ONE, 7, e32969.
98. Yang, Y.L. & Lu, K.T. (2005) Facilitation of conditioned fear extinction by d-cycloserine is mediated by mitogen-activated protein kinase and phosphatidylinositol 3-kinase cascades and requires de novo protein synthesis in basolateral nucleus of amygdala. Neuroscience, 134, 247-260.