Corticotrophin Releasing Factor-Induced Synaptic Plasticity in the Amygdala Translates Stress into Emotional Disorders

Journal of Neuroscience

Volumn 24, Issue 14, 2004, Pages 3471-3479

  Rainnie, Donald G ^a   Bergeron, Richard ^b   Sajdyk, Tammy J ^d   Patil, Madhvi ^a   Gehlert, Donald R ^c   Shekhar, Anantha ^d  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^c ELI LILLY AND COMPANY   (United States)

^d INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Anxiety; Basolateral amygdala; in vitro; in vivo; Inhibition; Urocortin

Indexed keywords

CORTICOTROPIN RELEASING FACTOR; CORTICOTROPIN RELEASING FACTOR RECEPTOR; LACTATE SODIUM; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PROTEIN KINASE (CALCIUM,CALMODULIN) II; UROCORTIN;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD PRESSURE; BREATHING RATE; CONTROLLED STUDY; EMOTIONAL DISORDER; HEART RATE; MALE; MENTAL STRESS; NERVE CELL EXCITABILITY; NERVE CELL PLASTICITY; NEUROENDOCRINOLOGY; NEUROMODULATION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PSYCHOPHYSIOLOGY; RAT;

AFFECTIVE SYMPTOMS; AMYGDALA; ANIMALS; ANXIETY; BLOOD PRESSURE; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM; CORTICOTROPIN-RELEASING HORMONE; DRUG ADMINISTRATION ROUTES; DRUG ADMINISTRATION SCHEDULE; EXCITATORY POSTSYNAPTIC POTENTIALS; HEART RATE; MALE; NEURONAL PLASTICITY; NEURONS; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; RECEPTORS, N-METHYL-D-ASPARTATE; SODIUM LACTATE; STRESS; SYNAPTIC TRANSMISSION;

EID: 1842631468     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5740-03.2004     Document Type: Article

References (69)

1. Adolphs R, Tranel D, Damasio AR (1998) The human amygdala in social judgment. Nature 393:470-474.
2. Ali AB, Rossier J, Staiger JF, Audinat E (2001) Kainate receptors regulate unitary IPSCs elicited in pyramidal cells by fast-spiking interneurons in the neocortex. J Neurosci 21:2992-2999.
3. Arborelius L, Owens MJ, Plotsky PM, Nemeroff CB (1999) The role of corticotropin-releasing factor in depression and anxiety disorders. J Endocrinol 160:1-12.
4. 3H](2S,4R)-4-methylglutamate autoradiography. Eur J Pharmacol 431:305-310.
5. Bale TL, Contarino A, Smith GW, Chan R, Gold LH, Sawchenko PE, Koob GF, Vale WW, Lee KF (2000) Mice deficient for corticotropin-releasing hormone receptors display anxiety-like behaviour and are hypersensitive to stress. Nat Genet 24:410-414.
6. Bedford FK, Kittler JT, Muller E, Thomas P, Uren JM, Merlo D, Wisden W, Triller A, Smart TG, Moss SJ (2001) GABA(A) receptor cell surface number and subunit stability are regulated by the ubiquitin-like protein Plic-1. Nat Neurosci 4:908-916.
7. Behr J, Gebhardt C, Heinemann U, Mody I (2002) Kindling enhances kainite receptor-mediated depression of GABAergic inhibition in rat granule cells. Eur J Neurosci 16:861-867.
8. Brandon NJ, Delmas P, Kittler JT, McDonald BJ, Sieghart W, Brown DA, Smart TG, Moss SJ (2000) GABAA receptor phosphorylation and functional modulation in cortical neurons by a protein kinase C-dependent pathway. J Biol Chem 275:38856-38862.
9. Britton KT, Lee G, Vale W, Rivier J, Koob GF (1986) Corticotropin releasing factor (CRF) receptor antagonist blocks activating and "anxiogenic" actions of CRF in the rat. Brain Res 369:303-306.
10. Callahan PM, Paris JM, Cunningham KA, Shinnick-Gallagher P (1991) Decrease of GABA-immunoreactive neurons in the amygdala after electrical kindling in the rat. Brain Res 555:335-339.
11. Casasola C, Bargas J, Arias-Montano JA, Calixto E, Montiel T, Galarraga E, Brailowsky S (2001) Hippocampal hyperexcitability induced by GABA withdrawal is due to down-regulation of GABA(A) receptors. Epilepsy Res 47:257-271.
12. Churn SB, Rana A, Lee K, Parsons JT, De Blas A, Delorenzo RJ (2002) Calcium/calmodulin-dependent kinase II phosphorylation of the GABAA receptor alpha1 subunit modulates benzodiazepine binding. J Neurochem 82:1065-1076.
13. Clugnet MC, LeDoux JE (1990) Synaptic plasticity in fear conditioning circuits: induction of LTP in the lateral nucleus of the amygdala by stimulation of the medial geniculate body. J Neurosci 10:2818-2824.
14. Cratty MS, Ward HE, Johnson EA, Azzaro AJ, Birkle DL (1995) Prenatal stress increases corticotropin-releasing factor (CRF) content and release in rat amygdala minces. Brain Res 675:297-302.
15. Crestani F, Lorez M, Baer K, Essrich C, Benke D, Laurent JP, Belzung C, Fritschey JM, Lüscher B, Mohler H (1999) Decreased GABAA-receptor clustering results in enhanced anxiety and a bias for threat cues. Nat Neurosci 2:833-839.
16. Critchley HD, Mathias CJ, Dolan RJ (2002) Fear conditioning in humans: the influence of awareness and autonomic arousal on functional neuroanatomy. Neuron 33:653-663.
17. Davis M, Whalen PJ (2001) The amygdala: vigilance and emotion. Mol Psychiatry 6:13-34.
18. Dube T, Brunson T, Nehlig A, Baram TZ (2000) Activation of specific neuronal circuits by corticotropin releasing hormone as indicated by c-fos expression and glucose metabolism. J Cereb Blood Flow Metab 20:1414-1424.
19. Dunn AJ, File SE (1987) Corticotropin-releasing factor has an anxiogenic action in the social interaction test. Horm Behav 21:193-202.
20. Everitt BJ, Parkinson JA, Olmstead MC, Arroyo M, Robledo P, Robbins TW (1999) Associative processes in addiction and reward. The role of amygdala-ventral striatal subsystems. Ann NY Acad Sci 877:412-438.
21. File SE (1990) One-trial tolerance to the anxiolytic effects of chlordiazepoxide in the plus-maze. Psychopharmacology (Berl) 100:281-282.
22. Furmark T, Fischer H, Wik G, Larsson M, Fredrikson M (1997) The amygdala and individual differences in human fear conditioning. NeuroReport 8:3957-3960.
23. Gallagher M, Schoenbaum G (1999) Functions of the amygdala and related forebrain areas in attention and cognition. Ann NY Acad Sci 877:397-411.
24. Gean PW, Chang FC (1992) Ketamine suppresses synchronized discharges in the disinhibited amygdala slice. Brain Res Bull 26:923-927.
25. Gray TS, Bingaman EW (1996) The amygdala: corticotropin-releasing factor, steroids, and stress. Crit Rev Neurobiol 10:155-168.
26. Heinrichs SC, Pich EM, Miczek KA, Britton KT, Koob GF (1992) Corticotropin-releasing factor antagonist reduces emotionality in socially defeated rats via direct neurotropic action. Brain Res 581:190-197.
27. Heinrichs SC, Lapsansky J, Lovenberg TW, De Souza EB, Chalmers DT (1997) Corticotropin-releasing factor CRF1, but not CRF2, receptors mediate anxiogenic-like behavior. Regul Pept 71:15-21.
28. Kawaguchi SY, Hirano T (2002) Signaling cascade regulating long-term potentiation of GABA(A) receptor responsiveness in cerebellar Purkinje neurons. J Neurosci 22:3969-3976.
29. LeDoux JE (2000) The amygdala: second edition a functional analysis (Aggleton JP, ed), pp 289-310. Oxford: Oxford UP.
30. Lee Y, Schulkin J, Davis M (1994) Effect of corticosterone on the enhancement of the acoustic startle reflex by corticotropin releasing factor (CRF). Brain Res 666:93-98.
31. Li XF, Phillips R, LeDoux JE (1995) NMDA and non-NMDA receptors contribute to synaptic transmission between the medial geniculate body and the lateral nucleus of the amygdala. Exp Brain Res 105:87-100.
32. Lisman J, Schulman H, Cline H (2002) The molecular basis of CaMKII function in synaptic and behavioral memory. Nat Rev Neurosci 3:175-190.
33. Maddock RJ (2001) The lactic acid response to alkalosis in panic disorder: an integrative review. J Neuropsychiatry Clin Neurosci 13:22-34.
34. Mahanty NK, Sah P (1999) Excitatory synaptic inputs to pyramidal neurons of the lateral amygdala. Eur J Neurosci 11:1217-1222.
35. Malinow R, Schulman H, Tsien RW (1989) Inhibition of post-synaptic PKC or CaMKII blocks induction but not expression of LTP. Science 245:862-866.
36. Maren S (2003) What the amygdala does and doesn't do in aversive learning. Learn Mem 10:306-308.
37. McGaugh JL, Roozendaal B (2002) Role of adrenal, stress hormones in forming lasting memories in the brain. Curr Opin Neurobiol 12:205-210.
38. McIntyre CK, Power AE, Roozendaal B, McGaugh JL (2003) Role of the basolateral amygdala in memory consolidation. Ann NY Acad Sci 985:273-293.
39. Merlo Pich E, Lorang M, Yeganeh M, Rodriguez de Fonseca F, Raber J, Koob GF, Weiss F (1995) Increase of extracellular corticotropin-releasing factor-like immunoreactivity levels in the amygdala of awaked rats during restraint stress and ethanol withdrawal as measured by microdialysis. J Neurosci 15:5439-5447.
40. Palkovits M, Brownstein MJ, Vale W (1983) Corticotropin releasing factor (CRF) immunoreactivity in hypothalamic and extrahypothalamic nuclei of sheep brain. Neuroendocrinology 37:302-305.
41. Rainnie DG (1999) Serotonergic modulation of neurotransmission in the rat basolateral amygdala. J Neurophysiol 82:69-85.
42. Rainnie DG, Asprodini EK, Shinnick-Gallagher P (1991a) Excitatory transmission in the basolateral amygdala. J Neurophysiol 66:986-998.
43. Rainnie DG, Asprodini EK, Shinnick-Gallagher P (1991b) Inhibitory transmission in the basolateral amygdala. J Neurophysiol 66:999-1009.
44. Rainnie DG, Fernhout BJ, Shinnick-Gallagher P (1992a) Differential actions of corticotropin releasing factor on basolateral and central amygdaloid neurons, in vitro. J Pharmacol Exp Ther 263:846-858.
45. Rainnie DG, Asprodini EK, Shinnick-Gallagher P (1992b) Kindling-induced long-lasting changes in synaptic transmission in the basolateral amygdala. J Neurophysiol 67:443-454.
46. Rainnie DG, Asprodini EK, Shinnick-Gallagher P (1993) Intracellular recordings from morphologically identified neurons of the basolateral amygdala. J Neurophysiol 69:1350-1362.
47. Reul JM, Holsboer F (2002) Corticotropin-releasing factor receptors 1 and 2 in anxiety and depression. Curr Opin Pharmacol 2:23-33.
48. Robbins TW, Everitt BJ (2002) Limbic-striatal memory systems and drug addiction. Neurobiol Learn Mem 78:625-636.
49. Roozendaal B, Brunson KL, Holloway BL, McGaugh JL, Baram TZ (2002) Involvement of stress-released corticotropin-releasing hormone in the basolateral amygdala in regulating memory consolidation. Proc Natl Acad Sci USA 99:13908-13913.
50. Sajdyk TJ, Gehlert DR (2000) Astressin, a corticotropin releasing factor antagonist, reverses the anxiogenic effects of urocortin when administered into the basolateral amygdala. Brain Res 877:226-234.
51. Sajdyk TJ, Shekhar A (1997) Excitatory amino acid receptors in the basolateral amygdala regulate anxiety responses in the social interaction test. Brain Res 764:262-264.
52. Sajdyk TJ, Schober DA, Gehlert DR, Shekhar A (1999) Role of corticoptropin-releasing factor and urocortin within the basolateral amygdala of rats in anxiety and panic responses. Behav Brain Res 100:207-215.
53. Sanders SK, Morzorati SL, Shekhar A (1995) Priming of experimental anxiety by repeated subthreshold GABA blockade in the rat amygdala. Brain Res 699:250-259.
54. Shekhar A (1993) GABA receptors in the region of the dorsomedial hypothalamus of rats regulate anxiety in the elevated plus-maze test. I. Behavioral measures. Brain Res 627:9-16.
55. Smagin GN, Heinrichs SC, Dunn AJ (2001) The role of CRH in behavioral responses to stress. Peptides 22:713-724.
56. Smith BN, Dudek FE (1996) Amino acid-mediated regulation of spontaneous synaptic activity patterns in the rat basolateral amygdala. J Neurophysiol 76:1958-1967.
57. Smith GW, Aubry JM, Dellu F, Contarino A, Bilezikjian LM, Gold LH, Chen R, Marchuk Y, Hauser C, Bentley CA, Sawchenko PE, Koob GF, Vale W, Lee KF (1998) Corticotropin releasing factor 1-deficient mice display decreased anxiety, impaired stress response, and aberrant neuroendocrine development. Neuron 20:1093-1102.
58. Smith SS, Gong QH, Hsu FC, Markowitz RS, ffrench-Mullen JM, Li X (1998) GABA(A) receptor alpha4 subunit suppression prevents withdrawal properties of an endogenous steroid. Nature 392:926-930.
59. Stenzel-Poore MP, Duncan JE, Rittenberg MB, Bakke A, Heinrichs SC (1996) CRH overproduction in transgenic mice: behavioral and immune system modulation. Ann NY Acad Sci 780:36-48.
60. Sutton RE, Koob GF, Le Moal M, Rivier J, Vale W (1982) Corticotropin releasing factor produces behavioural activation in rats. Nature 297:331-333.
61. Swerdlow NR, Geyer MA, Vale WW, Koob GF (1986) Corticotropin-releasing factor potentiates acoustic startle in rats: blockade by chlordiazepoxide. Psychopharmacology (Berl) 88:147-152.
62. Tan S-E, Liang K-C (1997) Inhibitory avoidance learning alters the amygdala calcium/calmodulin-dependent protein kinase KK activity in rats. Brain Res 748:227-233.
63. Tillfors M, Furmark T, Marteinsdottir I, Fischer H, Pissiota A, Langstrom B, Fredrikson M (2001) Cerebral blood flow in subjects with social phobia during stressful speaking tasks: a positron emission tomography study. Am J Psychiatry 158:1220-1226.
64. Timpl P, Spanagel R, Sillaber I, Kresse A, Reul JM, Stalla GK, Blanquet V, Steckler T, Holsboer F, Wurst W (1998) Impaired stress response and reduced anxiety in mice lacking functional corticotropin-releasing hormone receptor 1. Nat Genet 19:162-166.
65. Vale W, Spiess J, Rivier C, Rivier J (1981) Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and beta-endorphin. Science 213:1394-1397.
66. Van Pett K, Viau V, Bittencourt JC, Chan RK, Li HY, Arias C, Prins GS, Perrin M, Vale W, Sawchenko PE (2000) Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J Comp Neurol 428:191-212.
67. Vaughan J, Donaldson C, Bittencourt J, Perrin MH, Lewis K, Sutton S, Chan R, Turnbull AV, Lovejoy D, Rivier C, Sawchenko PE, Vale W (1995) Urocortin, a mammalian neuropeptide related to fish urotensin I and to corticotropin-releasing factor. Nature 378:287-292.
68. Walker DL, Davis M (2002) The role of amygdala glutamate receptors in fear learning, fear-potentiated startle, and extinction. Pharmacol Biochem Behav 71:379-392.
69. Yehuda R (2001) Biology of posttraumatic stress disorder. J Clin Psychiatry 62[Suppl 17]:41-46.