Cell-type specific deletion of GABA(A) α1 in corticotropin-releasing factor-containing neurons enhances anxiety and disrupts fear extinction

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 40, 2012, Pages 16330-16335

  Gafford, Georgette M ^a   Guo, Ji Dong ^a   Flandreau, Elizabeth I ^b   Hazra, Rimi ^a   Rainnie, Donald G ^a   Ressler, Kerry J ^a,c  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Central amygdala; HPA axis; Knockout; Plasticity; Short term synaptic depression

Indexed keywords

3 (6 DIMETHYLAMINO 4 METHYL 3 PYRIDINYL) 7 DIPROPYLAMINO 2,5 DIMETHYLPYRAZOLO[1,5 A]PYRIMIDINE; 4 AMINOBUTYRIC ACID A RECEPTOR ALPHA1; BENZODIAZEPINE; CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; MESSENGER RNA; ZOLPIDEM;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY DISORDER; ARTICLE; BED NUCLEUS OF THE STRIA TERMINALIS; BRAIN NERVE CELL; CONDITIONING; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DEPRESSION; FEAR; GENE DELETION; GENE EXPRESSION; HORMONE DETERMINATION; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; KNOCKOUT GENE; LOCOMOTION; MAZE TEST; MOUSE; NERVE CELL PLASTICITY; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; PAIN; PRIORITY JOURNAL; REINFORCEMENT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STRIA TERMINALIS; TRANSGENIC MOUSE;

ANALYSIS OF VARIANCE; ANIMALS; ANXIETY; CONDITIONING (PSYCHOLOGY); CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; DNA PRIMERS; EXTINCTION, PSYCHOLOGICAL; FEAR; IN SITU HYBRIDIZATION; IN SITU HYBRIDIZATION, FLUORESCENCE; MAZE LEARNING; MICE; MICE, TRANSGENIC; NEURONS; PATCH-CLAMP TECHNIQUES; PYRIDINES; PYRIMIDINES; RECEPTORS, GABA-A; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

MUS; MUS MUSCULUS;

EID: 84867091896     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1119261109     Document Type: Article

References (44)

1. 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. (Pubitemid 29044562)
2. Regev L, et al. (2011) Prolonged and site-specific over-expression of corticotropin-releasing factor reveals differential roles for extended amygdala nuclei in emotional regulation. Mol Psychiatry 16:714-728.
3. Regev L, Tsoory M, Gil S, Chen A (2012) Site-specific genetic manipulation of amygdala corticotropin-releasing factor reveals its imperative role in mediating behavioral response to challenge. Biol Psychiatry 71:317-326.
4. Kapcala LP, Dicke JA (1992) Brain corticotropin-releasing hormone receptors on neurons and astrocytes. Brain Res 589:143-148.
5. Sawchenko PE, Swanson LW (1985) Localization, colocalization, and plasticity of corti-cotropin- releasing factor immunoreactivity in rat brain. Fed Proc 44:221-227. (Pubitemid 15170678)
6. Shekhar A, Truitt W, Rainnie D, Sajdyk T (2005) Role of stress, corticotrophin releasing factor (CRF) and amygdala plasticity in chronic anxiety. Stress 8:209-219. (Pubitemid 43163254)
7. Bagosi Z, Jászberényi M, Szabó G, Telegdy G (2008) The effects of CRF and the urocortins on [3H]GABA release from the rat amygdala - An in vitro superfusion study. Brain Res Bull 75:15-17. (Pubitemid 350297637)
8. Nie Z, et al. (2004) Ethanol augments GABAergic transmission in the central amygdala via CRF1 receptors. Science 303:1512-1514. (Pubitemid 38314419)
9. Rainnie DG, et al. (2004) Corticotrophin releasing factor-induced synaptic plasticity in the amygdala translates stress into emotional disorders. J Neurosci 24:3471-3479. (Pubitemid 38481103)
10. Vinkers CH, et al. (2012) Lifelong CRF overproduction is associated with altered gene expression and sensitivity of discrete GABA(A) and mGlu receptor subtypes. Psychopharmacology (Berl) 219:897-908.
11. Sajdyk TJ, Schober DA, Gehlert DR, Shekhar A (1999) Role of corticotropin-releasing factor and urocortin within the basolateral amygdala of rats in anxiety and panic responses. Behav Brain Res 100:207-215. (Pubitemid 29130255)
12. Sanders SK, Shekhar A (1995) Regulation of anxiety by GABAA receptors in the rat amygdala. Pharmacol Biochem Behav 52:701-706. (Pubitemid 3005245)
13. Kash TL, Winder DG (2006) Neuropeptide Y and corticotropin-releasing factor bi-directionally modulate inhibitory synaptic transmission in the bed nucleus of the stria terminalis. Neuropharmacology 51:1013-1022. (Pubitemid 44528607)
14. Sakanaka M, Shibasaki T, Lederis K (1986) Distribution and efferent projections of corticotropin-releasing factor-like immunoreactivity in the rat amygdaloid complex. Brain Res 382:213-238. (Pubitemid 16001730)
15. Lee Y, Davis M (1997) Role of the hippocampus, the bed nucleus of the stria terminalis, and the amygdala in the excitatory effect of corticotropin-releasing hormone on the acoustic startle reflex. J Neurosci 17:6434-6446. (Pubitemid 27329915)
16. Sahuque LL, et al. (2006) Anxiogenic and aversive effects of corticotropin-releasing factor (CRF) in the bed nucleus of the stria terminalis in the rat: Role of CRF receptor subtypes. Psychopharmacology (Berl) 186:122-132. (Pubitemid 43668318)
17. Sajdyk T, Johnson P, Fitz S, ShekharA (2008) Chronic inhibition of GABA synthesis in the bed nucleus of the stria terminalis elicits anxiety-like behavior. J Psychopharmacol 22:633-641.
18. Radley JJ, Gosselink KL, Sawchenko PE (2009) A discrete GABAergic relay mediates medial prefrontal cortical inhibition of the neuroendocrine stress response. J Neurosci 29:7330-7340.
19. Heldt SA, Ressler KJ (2007) Training-induced changes in the expression of GABAA-associated genes in the amygdala after the acquisition and extinction of Pavlovian fear. Eur J Neurosci 26:3631-3644. (Pubitemid 350243541)
20. Wiltgen BJ, et al. (2009) The alpha1 subunit of the GABA(A) receptor modulates fear learning and plasticity in the lateral amygdala. Front Behav Neurosci 3:37.
21. Marowsky A, Fritschy JM, Vogt KE (2004) Functional mapping of GABA A receptor subtypes in the amygdala. Eur J Neurosci 20:1281-1289. (Pubitemid 39233581)
22. Heldt SA, Ressler KJ (2007) Forebrain and midbrain distribution of major benzodi-azepine- sensitive GABAA receptor subunits in the adult C57 mouse as assessed with in situ hybridization. Neuroscience 150:370-385. (Pubitemid 350198707)
23. Martin EI, et al. (2010) A novel transgenic mouse for gene-targeting within cells that express corticotropin-releasing factor. Biol Psychiatry 67:1212-1216.
24. Nemeroff CB, Vale WW (2005) The neurobiology of depression: Inroads to treatment and new drug discovery. J Clin Psychiatry 66(Suppl 7):5-13. (Pubitemid 41345489)
25. Bale TL (2005) Sensitivity to stress: Dysregulation of CRF pathways and disease development. Horm Behav 48:1-10.
26. Cai W-H, Blundell J, Han J, Greene RW, Powell CM (2006) Postreactivation glucocorticoids impair recall of established fear memory. J Neurosci 26:9560-9566. (Pubitemid 44396869)
27. Yang YL, Chao PK, Lu KT (2006) Systemic and intra-amygdala administration of glucocorticoid agonist and antagonist modulate extinction of conditioned fear. Neuropsychopharmacology 31:912-924.
28. Abrari K, Rashidy-Pour A, Semnanian S, Fathollahi Y (2008) Administration of corticosterone after memory reactivation disrupts subsequent retrieval of a contextual conditioned fear memory: Dependence upon training intensity. Neurobiol Learn Mem 89:178-184. (Pubitemid 350235967)
29. Blundell J, Blaiss CA, Lagace DC, Eisch AJ, Powell CM (2011) Block of glucocorticoid synthesis during re-activation inhibits extinction of an established fear memory. Neurobiol Learn Mem 95:453-460.
30. McGaugh JL, Roozendaal B (2002) Role of adrenal stress hormones in forming lasting memories in the brain. Curr Opin Neurobiol 12:205-210. (Pubitemid 34518341)
31. Merali Z, et al. (2004) Dysregulation in the suicide brain: mRNA expression of corti-cotropin- releasing hormone receptors and GABA(A) receptor subunits in frontal cortical brain region. J Neurosci 24:1478-1485. (Pubitemid 38223000)
32. Sieghart W (1995) Structure and pharmacology of gamma-aminobutyric acidA receptor subtypes. Pharmacol Rev 47:181-234.
33. Whiting PJ, McKernan RM, Wafford KA (1995) Structure and pharmacology of vertebrate GABAA receptor subtypes. Int Rev Neurobiol 38:95-138. (Pubitemid 3005336)
34. Kralic JE, et al. (2002) GABA(A) receptor alpha-1 subunit deletion alters receptor subtype assembly, pharmacological and behavioral responses to benzodiazepines and zolpidem. Neuropharmacology 43:685-694. (Pubitemid 35279576)
35. Sur C, et al. (2001) Loss of the major GABA(A) receptor subtype in the brain is not lethal in mice. J Neurosci 21:3409-3418. (Pubitemid 32422806)
36. Dobrunz LE, Stevens CF (1997) Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18:995-1008. (Pubitemid 27274617)
37. Tsodyks MV, Markram H (1997) The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc Natl Acad Sci USA 94: 719-723. (Pubitemid 27053700)
38. Rudolph U, et al. (1999) Benzodiazepine actions mediated by specific gamma-aminobutyric acid(A) receptor subtypes. Nature 401:796-800.
39. Vicini S, et al. (2001) GABA(A) receptor alpha1 subunit deletion prevents developmental changes of inhibitory synaptic currents in cerebellar neurons. J Neurosci 21:3009-3016. (Pubitemid 32323482)
40. Heldt SA, Ressler KJ (2010) Amygdala-specific reduction of alpha1-GABAA receptors disrupts the anticonvulsant, locomotor, and sedative, but not anxiolytic, effects of benzodiazepines in mice. J Neurosci 30:7139-7151.
41. Paxinos G (2001) The Mouse Brain in Stereotaxic Coordinates (Academic, San Diego) 2nd ed.
42. Ressler KJ, Paschall G, Zhou XL, Davis M (2002) Regulation of synaptic plasticity genes during consolidation of fear conditioning. J Neurosci 22:7892-7902. (Pubitemid 35379094)
43. Hazra R, et al. (2011) A transcriptomic analysis of type I-III neurons in the bed nucleus of the stria terminalis. Mol Cell Neurosci 46:699-709.
44. Guo JD, et al. (2012) Presynaptic muscarinic M(2) receptors modulate glutamatergic transmission in the bed nucleus of the stria terminalis. Neuropharmacology 62:1671-1683.