Behavioral and neural analysis of GABA in the acquisition, consolidation, reconsolidation, and extinction of fear memory.
The current review systematically documents the role of gamma-amino-butyric acid (GABA) in different aspects of fear memory-acquisition and consolidation, reconsolidation, and extinction, and attempts to resolve apparent contradictions in the data in order to identify the function of GABA(A) receptors in fear memory. First, numerous studies have shown that pre- and post-training administration of drugs that facilitate GABAergic transmission disrupt the initial formation of fear memories, indicating a role for GABA(A) receptors, possibly within the amygdala and hippocampus, in the acquisition and consolidation of fear memories. Similarly, recent evidence indicates that these drugs are also detrimental to the restorage of fear memories after their reactivation. This suggests a role for GABA(A) receptors in the reconsolidation of fear memories, although the precise neural circuits are yet to be identified. Finally, research regarding the role of GABA in extinction has shown that GABAergic transmission is also disruptive to the formation of newly acquired extinction memories. We argue that contradictions to these patterns are the result of variations in (a) the location of drug infusion, (b) the dosage of the drug and/or (c) the time point of drug administration. The question of whether these GABA-induced memory deficits reflect deficits in retrieval is discussed. Overall, the evidence implies that the processes mediating memory stability consequent to initial fear learning, memory reactivation, and extinction training are dependent on a common mechanism of reduced GABAergic neurotransmission.
Makkar
Steve R
SR
School of Psychology, University of New South Wales, Sydney, NSW, Australia.
Zhang
Shirley Q
SQ
Cranney
Jacquelyn
J
D000818:Animals; D003214:Conditioning, Classical / Q000187:drug effects / Q000502:physiology*; D005108:Extinction, Psychological / Q000187:drug effects / Q000502:physiology*; D005239:Fear; D018682:GABA Agents / Q000494:pharmacology; D006801:Humans; D008568:Memory / Q000187:drug effects / Q000502:physiology*; D008954:Models, Biological; D018079:Receptors, GABA / Q000502:physiology; D005680:gamma-Aminobutyric Acid / Q000378:metabolism*
D018682:GABA Agents; D018079:Receptors, GABA; D005680:gamma-Aminobutyric Acid
Neuropsychopharmacology. 2008 Jan;33(1):56-72
17882236
Hippocampus. 2008;18(1):29-39
17853412
Trends Neurosci. 2003 Feb;26(2):65-72
12536129
Learn Mem. 2008 Dec 02;15(12):876-84
19050159
Behav Brain Res. 2005 Mar 30;158(2):293-300
15698896
J Exp Psychol Anim Behav Process. 1999 Apr;25(2):236-46
10331922
Behav Neurosci. 2007 Feb;121(1):131-9
17324057
Learn Mem. 2009 Jan 07;16(1):53-61
19141466
Learn Mem. 2004 Sep-Oct;11(5):540-3
15466305
Eur J Pharmacol. 1994 May 17;267(3):R3-5
8088363
Behav Neural Biol. 1990 Sep;54(2):156-64
2173543
Cell. 2002 Dec 13;111(6):905-18
12526815
J Neurophysiol. 2004 Jul;92(1):1-9
15212433
Eur J Neurosci. 2006 Sep;24(6):1751-8
17004939
J Neurosci. 2001 Mar 15;21(6):2186-93
11245703
Neuropsychopharmacology. 2008 Nov;33(12):2912-21
18288094
Curr Opin Neurobiol. 2001 Apr;11(2):180-7
11301237
J Neurosci. 2009 Oct 28;29(43):13432-4
19864555
Behav Neural Biol. 1989 Mar;51(2):165-70
2539081
Psychol Bull. 1993 Jul;114(1):80-99
8346330
Learn Mem. 2005 Nov-Dec;12(6):573-8
16322359
Science. 2008 Feb 29;319(5867):1253-6
18258863
Yakubutsu Seishin Kodo. 1987 Jun;7(2):307-12
3687243
Behav Neurosci. 2004 Jun;118(3):563-8
15174933
Psychopharmacology (Berl). 1979 Mar 14;61(1):25-8
35806
Genes Brain Behav. 2003 Feb;2(1):3-10
12882314
Eur J Neurosci. 2006 Apr;23(7):1853-9
16623842
Learn Mem. 2006 Jan-Feb;13(1):27-34
16452651
Pharmacol Biochem Behav. 2009 Apr;92(2):319-26
19171164
Behav Neurosci. 2004 Jun;118(3):505-13
15174928
Brain Res. 1989 May 15;487(1):105-12
2752279
Brain Res. 1993 Oct 29;626(1-2):63-70
7904228
Neuron. 2002 Oct 24;36(3):527-38
12408854
Nat Rev Neurosci. 2004 Nov;5(11):844-52
15496862
J Neurosci. 2003 Dec 3;23(35):11054-64
14657162
Learn Mem. 2000 Mar-Apr;7(2):73-84
10753974
J Neurosci. 2004 May 19;24(20):4787-95
15152039
Science. 2003 Aug 22;301(5636):1102-4
12934010
Behav Brain Res. 2007 Jun 18;180(2):113-8
17403545
Neurobiol Learn Mem. 2006 Sep;86(2):133-43
16504549
Brain Res. 1990 Feb 5;508(2):225-33
2306613
J Med Chem. 2004 Apr 22;47(9):2176-9
15084116
J Neurosci. 2003 Sep 24;23(25):8800-7
14507980
Memory. 2004 Jul;12(4):416-27
15487538
Behav Neural Biol. 1989 Sep;52(2):170-9
2552976
Neuroscience. 2009 Jan 23;158(2):387-401
19015009
Science. 1992 May 1;256(5057):675-7
1585183
J Exp Psychol Anim Behav Process. 2006 Apr;32(2):135-44
16634656
Neurobiol Learn Mem. 2006 Sep;86(2):144-9
16540353
Psychol Rev. 1973 Jan;80(1):69-79
4347561
Exp Brain Res. 2001 Jul;139(1):39-52
11482842
Nature. 1993 Dec 9;366(6455):565-9
7504783
Behav Neurosci. 1997 Aug;111(4):683-91
9267646
Science. 1971 Oct 15;174(4006):292
4330303
Science. 2000 Oct 6;290(5489):131-4
11021797
Behav Neurosci. 2008 Dec;122(6):1295-305
19045949
Psychopharmacology (Berl). 2001 Jun;156(1):92-7
11465639
Learn Motiv. 1996 Nov;27(4):335-61
8979936
Science. 2000 Jan 14;287(5451):248-51
10634773
Br J Anaesth. 2002 Oct;89(4):614-21
12393364
Memory. 2004 Jul;12(4):389-402
15487536
Behav Brain Res. 1988 Sep 1;30(1):31-6
2844205
Toxicology. 2006 Jan 16;217(2-3):147-54
16213647
Neurobiol Learn Mem. 1999 Jul;72(1):1-7
10371710
J Neurosci. 2002 Jul 1;22(13):5572-80
12097508
Neurobiol Learn Mem. 2004 Jul;82(1):52-6
15183170
Eur J Neurosci. 2006 Jul;24(1):249-60
16882021
Learn Mem. 2007 Jul 18;14(7):504-11
17644752
Eur J Neurosci. 2007 Dec;26(12):3631-44
18088283
Eur Arch Psychiatry Neurol Sci. 1989;238(5-6):294-301
2569974
Nature. 2000 Aug 17;406(6797):722-6
10963596
Curr Opin Pharmacol. 2006 Feb;6(1):18-23
16376150
Hippocampus. 2006;16(2):174-82
16358312
Neuropsychopharmacology. 2007 Mar;32(3):542-50
16541088
Behav Neurosci. 1990 Apr;104(2):264-7
2346621
Psychopharmacologia. 1972;23(4):375-85
5025579
Neurobiol Learn Mem. 2006 Sep;86(2):123-32
16458544
Behav Neurosci. 2004 Apr;118(2):389-94
15113265
J Neurosci. 2006 Aug 23;26(34):8800-3
16928868
Neurosci Lett. 2009 Feb 6;450(3):270-4
19047011
Pharmacol Biochem Behav. 1999 May;63(1):55-61
10340524
Psychopharmacology (Berl). 1979 Jun 28;64(1):125-6
39313
J Neurosci. 2005 Sep 28;25(39):8978-87
16192388
Mol Psychiatry. 2007 Feb;12(2):120-50
17160066
Neuron. 2002 Nov 14;36(4):567-84
12441048
Pharmacol Ther. 1996;69(3):173-98
8783370
Neuroscience. 2006;139(3):831-42
16542779
Nat Rev Neurosci. 2009 Mar;10(3):224-34
19229241
Behav Neural Biol. 1990 Sep;54(2):105-9
2173541
Brain Res. 2000 Mar 10;858(2):440-5
10708699
Learn Mem. 2009 Jul 24;16(8):486-93
19633138
Brain Res. 1999 Jul 24;835(2):340-5
10415392
J Neurosci. 1999 Feb 1;19(3):1106-14
9920672
J Neurosci. 2005 Jan 12;25(2):502-6
15647495
Learn Mem. 2004 Sep-Oct;11(5):572-8
15466311
Nature. 1986 Jun 26-Jul 2;321(6073):864-6
3724846
Psychol Rep. 1977 Jun;40(3 Pt 2):783-6
17136
J Trauma Stress. 2000 Oct;13(4):539-88
11109232
Neurobiol Learn Mem. 2008 Oct;90(3):576-9
18657626
Behav Res Ther. 2000 Apr;38(4):319-45
10761279
J Neurosci. 2004 Oct 20;24(42):9269-75
15496662
Horm Behav. 1994 Dec;28(4):537-44
7729823
J Med Chem. 2004 Nov 18;47(24):5829-32
15537339
Psychopharmacologia. 1973 May 21;30(2):173-84
4711374
Trends Pharmacol Sci. 2001 Apr;22(4):188-94
11282419
Mol Pharmacol. 1993 Apr;43(4):609-25
8386310
Neuroscience. 1992 Jul;49(1):1-6
1407540
Science. 2001 Nov 2;294(5544):1030-8
11691980
Nature. 2006 Nov 23;444(7118):486-9
17108970
Psychopharmacology (Berl). 1998 Nov;140(1):105-15
9862409
Eur J Neurosci. 2006 Feb;23(3):758-64
16487156
Behav Neural Biol. 1990 Jul;54(1):27-41
1974134
Cell. 2007 Oct 5;131(1):160-73
17923095
Neuron. 2007 Mar 15;53(6):871-80
17359921
Behav Res Ther. 2000 Jun;38(6):601-10
10846808
Nature. 1999 Oct 21;401(6755):796-800
10548105
J Neurosci. 2004 Jun 23;24(25):5704-10
15215292
Proc Natl Acad Sci U S A. 1992 Aug 1;89(15):6726-30
1323116
Biol Psychiatry. 2007 Sep 1;62(5):446-54
17217927
Psychol Bull. 1979 Sep;86(5):1054-83
386401
J Neurosci. 2001 Mar 1;21(5):1720-6
11222661
Nat Rev Neurosci. 2007 Apr;8(4):262-75
17342174
Nat Neurosci. 2001 Aug;4(8):813-8
11477427
J Neurosci. 2009 Jul 1;29(26):8474-82
19571138
Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11642-7
10500230
Nature. 2002 Aug 1;418(6897):530-4
12152079
Eur J Neurosci. 2003 Nov;18(9):2605-10
14622162
Nature. 2002 Nov 7;420(6911):70-4
12422216
Neuropsychobiology. 1995;32(1):31-6
7566520
Psychopharmacologia. 1971;20(2):186-90
5090537
Pharmacol Rev. 1995 Jun;47(2):181-234
7568326
Neuropharmacology. 1996 Mar;35(3):347-57
8783210
Brain Res. 1997 Mar 28;752(1-2):197-202
9106457
Learn Mem. 2006 Jul-Aug;13(4):451-7
16882861
Proc Natl Acad Sci U S A. 2002 Jun 25;99(13):8980-5
12084936
Brain Res. 1986 Mar 12;368(1):125-33
3955350
Brain Res. 1991 Jun 14;551(1-2):104-9
1913142
Life Sci. 1993;52(24):1935-45
8389411
Cleve Clin J Med. 1990 Jul-Aug;57(5):481-91
2164898
Eur J Neurosci. 2005 Jan;21(1):283-9
15654867
Behav Neural Biol. 1993 Jul;60(1):84-7
8105777
Neuron. 2007 Sep 20;55(6):942-57
17880897
Behav Res Ther. 1972 Nov;10(4):367-70
4637492
Behav Neurosci. 1990 Feb;104(1):44-55
2317285
Brain Res Brain Res Rev. 1999 Apr;29(2-3):196-217
10209232
Behav Neurosci. 2009 Jun;123(3):641-9
19485571
J Neurosci. 2008 Jan 9;28(2):369-75
18184779
Neuropsychopharmacology. 2009 Jan;34(2):446-57
18509330
J Neurosci. 2006 Sep 27;26(39):10051-6
17005868
Neuroscience. 2004;129(2):267-72
15501585
J Neurophysiol. 2009 Jan;101(1):341-9
19004994
Learn Mem. 2006 Mar-Apr;13(2):216-23
16585797
Behav Brain Res. 2010 Mar 17;208(1):1-11
19931568
Behav Neurosci. 2006 Feb;120(1):40-8
16492115
Behav Neurosci. 1989 Feb;103(1):202-5
2923673
Eur J Neurosci. 2004 Oct;20(7):1928-36
15380015
Behav Neural Biol. 1994 Mar;61(2):150-5
8204080
Neurosci Behav Physiol. 2008 Oct;38(8):775-9
18802774
Eur J Neurosci. 2007 Jun;25(12):3702-12
17610589
Biol Psychiatry. 2002 Nov 15;52(10):998-1007
12437940
Neuropsychopharmacology. 2008 Aug;33(9):2117-30
17987061
J Pharmacol Exp Ther. 1985 Mar;232(3):831-7
2857789
J Neurosci. 2005 Feb 23;25(8):1935-42
15728833
Behav Neurosci. 1998 Feb;112(1):183-92
9517826
Neuroscience. 2000;101(4):815-50
11113332
Proc Natl Acad Sci U S A. 2005 Jun 28;102(26):9347-52
15947076