Plastic synaptic networks of the amygdala for the acquisition, expression, and extinction of conditioned fear.
The last 10 years have witnessed a surge of interest for the mechanisms underlying the acquisition and extinction of classically conditioned fear responses. In part, this results from the realization that abnormalities in fear learning mechanisms likely participate in the development and/or maintenance of human anxiety disorders. The simplicity and robustness of this learning paradigm, coupled with the fact that the underlying circuitry is evolutionarily well conserved, make it an ideal model to study the basic biology of memory and identify genetic factors and neuronal systems that regulate the normal and pathological expressions of learned fear. Critical advances have been made in determining how modified neuronal functions upon fear acquisition become stabilized during fear memory consolidation and how these processes are controlled in the course of fear memory extinction. With these advances came the realization that activity in remote neuronal networks must be coordinated for these events to take place. In this paper, we review these mechanisms of coordinated network activity and the molecular cascades leading to enduring fear memory, and allowing for their extinction. We will focus on Pavlovian fear conditioning as a model and the amygdala as a key component for the acquisition and extinction of fear responses.
Pape
Hans-Christian
HC
Institute of Physiology, Westfaelische Wilhelms-University, Muenster, Germany; and Rutgers State University, Newark, New Jersey, USA. papechris@ukmuenster.de
Pare
Denis
D
D000679:Amygdala / Q000502:physiology*; D000818:Animals; D001007:Anxiety / Q000503:physiopathology*; D005108:Extinction, Psychological; D005239:Fear / Q000502:physiology*; D006801:Humans; D009415:Nerve Net / Q000502:physiology*; D009473:Neuronal Plasticity / Q000502:physiology*
J Comp Neurol. 1985 Dec 8;242(2):182-213
4086664
Brain Res. 1989 Dec 29;505(2):337-40
2598054
Biol Psychiatry. 2009 Oct 1;66(7):665-73
19482263
J Comp Neurol. 2004 May 17;473(1):137-46
15067724
Neuroscience. 2002;110(4):617-26
11934470
J Neurosci. 2009 Sep 9;29(36):11078-88
19741114
J Neurophysiol. 2001 Dec;86(6):2887-95
11731545
Brain Behav Evol. 2002;60(2):101-16
12373061
Learn Mem. 2008 Oct 02;15(10):792-805
18832566
J Neurosci. 2009 Jan 14;29(2):402-13
19144840
J Comp Neurol. 1994 Feb 15;340(3):405-26
8188859
J Neurochem. 2008 Jul;106(2):889-99
18466342
Nature. 2007 May 10;447(7141):178-82
17468743
Psychiatr Clin North Am. 2009 Mar;32(1):57-69
19248916
CNS Spectr. 2007 Mar;12(3):200-6
17329980
Biol Psychiatry. 2005 Apr 15;57(8):841-7
15820704
Brain Res. 1978 Oct 27;155(2):397-403
688023
Hippocampus. 2000;10(5):527-41
11075823
Proc Natl Acad Sci U S A. 1999 Nov 9;96(23):13438-43
10557339
Learn Mem. 2009 Jan 07;16(1):62-8
19141467
J Neurosci. 1999 Dec 1;19(23):10575-83
10575053
Science. 2004 Jul 2;305(5680):96-9
15232109
Acta Psychol (Amst). 2008 Mar;127(3):567-80
18226795
Learn Mem. 2008 Jan 28;15(2):55-62
18230673
Mol Pharmacol. 2007 Aug;72(2):350-8
17456785
Learn Mem. 2004 Sep-Oct;11(5):540-3
15466305
J Comp Neurol. 1995 Nov 6;362(1):86-108
8576430
Eur J Neurosci. 2000 Jul;12(7):2534-46
10947828
Science. 2009 Mar 13;323(5920):1492-6
19286560
Annu Rev Neurosci. 2004;27:1-28
15217324
J Comp Neurol. 2007 Jan 20;500(3):513-29
17120289
Nature. 1997 Jul 24;388(6640):377-80
9237754
Nat Neurosci. 2005 Jul;8(7):925-31
15937483
Learn Mem. 2007 Jul 12;14(7):497-503
17626908
Nature. 2008 Jul 31;454(7204):642-5
18615014
Learn Mem. 2008 Aug 26;15(9):657-66
18772253
Neuron. 1997 Sep;19(3):613-24
9331352
J Neurosci. 2009 Dec 16;29(50):15713-20
20016086
Exp Brain Res. 1994;100(3):469-83
7529194
Neuron. 1999 Jun;23(2):227-8
10399929
J Comp Neurol. 1995 Oct 16;361(2):345-68
8543667
Learn Mem. 2009 Feb 17;16(3):167-77
19223600
J Neurosci. 1999 Dec 15;19(24):11027-39
10594083
J Comp Neurol. 1990 Dec 15;302(3):515-28
1702115
J Comp Neurol. 2001 Aug 6;436(4):430-55
11447588
Curr Opin Cell Biol. 2005 Oct;17(5):446-52
16099637
Exp Brain Res. 1987;67(3):493-501
3653311
J Neurophysiol. 1996 Mar;75(3):1301-5
8867138
J Comp Neurol. 1989 Dec 8;290(2):213-42
2592611
Behav Neurosci. 2004 Feb;118(1):5-14
14979778
J Comp Neurol. 1991 Nov 8;313(2):295-325
1765584
PLoS One. 2009 Jun 10;4(6):e5865
19517024
Neuroscience. 2002;115(2):455-62
12421611
Brain Res. 2007 Feb 23;1134(1):87-94
17207780
J Neurosci. 2008 Nov 26;28(48):12682-90
19036961
Neurosci Lett. 1985 Jan 21;53(2):203-7
3885076
Neuroscience. 2006;139(3):821-9
16515842
Neuron. 2008 Jul 31;59(2):298-310
18667157
Cell Mol Life Sci. 2008 Nov;65(22):3525-44
18668205
Brain Res. 2000 Mar 17;859(1):1-14
10720609
Biol Psychiatry. 2004 Aug 1;56(3):151-60
15271583
Nat Neurosci. 2009 Jun;12(6):801-7
19430471
Cereb Cortex. 1993 Nov-Dec;3(6):515-32
7511012
Behav Brain Res. 2000 Sep;114(1-2):145-52
10996055
Neuroscientist. 2005 Feb;11(1):75-88
15632280
Neuroscience. 2006 Nov 17;143(1):15-23
16962716
Hum Mol Genet. 1999 Mar;8(3):387-96
9949198
Neuron. 1998 May;20(5):937-45
9620698
Proc Natl Acad Sci U S A. 2006 Nov 21;103(47):18020-5
17090669
J Neurosci. 2005 Oct 26;25(43):10010-4
16251449
Proc Natl Acad Sci U S A. 2007 Aug 28;104(35):14146-50
17709755
Neuroscience. 2004;128(1):7-14
15450349
Science. 2009 May 15;324(5929):951-5
19342552
J Comp Neurol. 1977 Apr 15;172(4):723-52
838896
J Neurophysiol. 1990 Mar;63(3):473-90
2329357
Brain Res. 2002 Jul 12;943(2):237-44
12101046
Prog Neurobiol. 2003 Jun;70(2):83-244
12927745
Behav Neurosci. 1992 Apr;106(2):274-85
1590953
J Comp Neurol. 1997 Jun 2;382(2):153-75
9183686
Neuroscience. 1998 Apr;83(3):877-89
9483571
Neurosci Res. 1995 Feb;21(4):317-22
7777222
J Neurosci. 2004 May 19;24(20):4796-806
15152040
Behav Neurosci. 2004 Jun;118(3):505-13
15174928
Behav Res Ther. 2005 Mar;43(3):357-71
15680931
Neuron. 2003 May 8;38(3):447-60
12741991
J Comp Neurol. 1998 May 25;395(1):53-72
9590546
J Neurosci. 2002 Jun 15;22(12):5219-29
12077217
Rev Neurosci. 2003;14(3):233-40
14513866
Behav Res Ther. 2002 Feb;40(2):127-49
11814178
Neuron. 2005 Oct 20;48(2):175-87
16242399
Neuroscience. 1991;42(2):335-50
1832750
Neuron. 1995 Nov;15(5):1029-39
7576647
J Comp Neurol. 1992 Oct 8;324(2):180-94
1430328
Brain Res Rev. 2009 Apr;60(1):226-42
19162070
Neuron. 2002 Oct 24;36(3):527-38
12408854
J Comp Neurol. 1993 May 1;331(1):14-36
8320347
Prog Brain Res. 2008;167:171-86
18037014
Eur J Neurosci. 2005 Mar;21(5):1359-69
15813945
Brain Behav Evol. 1986;29(1-2):17-28
3594197
J Comp Neurol. 1986 May 8;247(2):246-71
2424941
J Neurosci. 1999 Dec 15;19(24):RC48
10594092
Neuroscience. 2006 Sep 1;141(3):1599-609
16753264
Neuroscience. 2001;102(2):413-25
11166127
Nat Rev Neurosci. 2004 Nov;5(11):844-52
15496862
Pharmacol Biochem Behav. 2005 May;81(1):139-45
15894071
Hippocampus. 2002;12(5):592-9
12440575
Cereb Cortex. 2009 Feb;19(2):474-82
18562331
Proc Natl Acad Sci U S A. 2007 Dec 26;104(52):20955-60
18165656
J Comp Neurol. 1981 May 1;198(1):121-36
6164704
Learn Mem. 2001 Jul-Aug;8(4):209-19
11533224
Neurobiol Learn Mem. 2007 May;87(4):635-43
17185008
Semin Cell Dev Biol. 2003 Feb;14(1):37-42
12524005
Science. 2009 Sep 4;325(5945):1258-61
19729657
Nat Rev Neurosci. 2004 Dec;5(12):917-30
15550947
J Neurophysiol. 2001 Aug;86(2):717-23
11495945
Nature. 1993 Jan 7;361(6407):31-9
8421494
Neuron. 2007 Sep 6;55(5):786-98
17785185
J Neurophysiol. 2009 Mar;101(3):1494-506
19164102
J Neurosci. 2004 May 19;24(20):4787-95
15152039
Brain Res. 1980 May 5;189(1):49-66
7363097
J Neurosci. 1995 Mar;15(3 Pt 2):2301-11
7891168
J Neurosci. 2005 Jun 15;25(24):5730-9
15958739
Neuron. 2009 Feb 12;61(3):340-50
19217372
Behav Brain Res. 2008 Dec 12;194(2):201-6
18692093
J Neurosci. 1988 Jul;8(7):2517-29
2854842
Neuropsychopharmacology. 2008 Jan;33(1):56-72
17882236
Annu Rev Neurosci. 2004;27:193-222
15217331
Neurobiol Learn Mem. 2007 May;87(4):573-82
17223582
Biol Psychiatry. 2006 Aug 15;60(4):337-43
16712801
J Neurophysiol. 1993 Apr;69(4):1350-62
8492168
J Neurosci. 2007 Aug 29;27(35):9369-79
17728450
Neuroscience. 2006 Sep 15;141(4):2007-18
16820264
Neuron. 2004 Jan 8;41(1):139-51
14715141
J Comp Neurol. 2000 Jan 24;416(4):496-508
10660880
J Comp Neurol. 2006 Jun 10;496(5):655-67
16615120
Neurosci Biobehav Rev. 2006;30(2):188-202
16120461
Neuroscience. 2003;121(1):155-66
12946708
J Neurosci. 2003 Mar 1;23(5):1574-9
12629159
Trends Neurosci. 2004 Jul;27(7):378-83
15219736
J Comp Neurol. 1994 Apr 8;342(2):232-48
7911130
J Neurosci. 1990 Apr;10(4):1062-9
2329367
Trends Neurosci. 2005 Jan;28(1):12-9
15626492
Arch Gen Psychiatry. 2005 Jun;62(6):617-27
15939839
Learn Mem. 2001 Sep-Oct;8(5):229-42
11584069
J Neurosci. 2000 Sep 15;20(18):RC96
10974093
J Comp Neurol. 1947 Aug;87(1):1-16
20256274
J Comp Neurol. 1987 Oct 1;264(1):123-46
2445791
J Neurosci. 2000 Apr 1;20(7):RC68
10729357
Brain Res. 2005 Jul 27;1051(1-2):81-9
15979591
J Comp Neurol. 1994 Jun 1;344(1):33-49
7520456
Neurobiol Learn Mem. 2008 Mar;89(3):225-33
18162421
J Neurosci. 2003 Sep 24;23(25):8800-7
14507980
Neuropharmacology. 2007 Jan;52(1):215-27
16919687
Neuron. 2009 Jan 15;61(1):10-26
19146809
Nat Rev Neurosci. 2002 Feb;3(2):122-31
11836520
Behav Res Ther. 2002 Feb;40(2):169-72
11814180
Nat Neurosci. 2002 Apr;5(4):348-55
11889468
Learn Mem. 2004 Nov-Dec;11(6):727-31
15537738
Learn Mem. 2008 Apr 25;15(5):348-56
18441293
J Neurophysiol. 1997 Jan;77(1):353-63
9120576
J Neurosci. 2009 Mar 18;29(11):3387-94
19295145
Synapse. 1997 Oct;27(2):106-21
9266772
Neuron. 2004 Jun 24;42(6):961-72
15207240
Learn Mem. 2001 May-Jun;8(3):148-55
11390634
Neuropsychopharmacology. 2008 Sep;33(10):2416-26
18046303
J Comp Neurol. 1982 Feb 10;205(1):30-48
7068948
Cell. 2005 Nov 18;123(4):697-709
16286011
J Neurosci. 2008 Feb 6;28(6):1282-90
18256248
Brain Res. 1983 Oct;287(2):139-71
6357356
Brain Res. 1990 Jun 4;518(1-2):227-43
1697208
Trends Neurosci. 1997 Nov;20(11):517-23
9364666
J Neurosci. 2006 Oct 18;26(42):10888-109898
17050727
J Neurophysiol. 1999 Feb;81(2):930-4
10036290
Ann N Y Acad Sci. 2003 Apr;985:135-49
12724155
J Neurosci. 2004 Nov 3;24(44):9953-61
15525780
Acta Psychiatr Scand Suppl. 2004;(420):21-7
15128384
Science. 1995 Aug 25;269(5227):1115-8
7652558
Neuropsychopharmacology. 2007 Sep;32(9):1929-40
17213844
Science. 1999 Sep 17;285(5435):1870-4
10489359
J Neurosci. 1999 Nov 15;19(22):9698-704
10559379
J Neurosci. 1990 Aug;10(8):2818-24
2388089
J Comp Neurol. 1993 Mar 8;329(2):201-29
8454730
Learn Mem. 2008 Oct 30;15(11):837-43
18984565
Learn Mem. 2005 Nov-Dec;12(6):615-9
16322363
Neuroscience. 2001;106(3):613-20
11591461
Nat Neurosci. 1998 Nov;1(7):595-601
10196567
Neurobiol Learn Mem. 2004 Sep;82(2):159-63
15341801
CNS Spectr. 2009 Jan;14(1 Suppl 1):13-24
19169190
Synapse. 2004 Jan;51(1):32-58
14579424
Behav Neurosci. 1997 Aug;111(4):683-91
9267646
J Comp Neurol. 1978 Mar 15;178(2):255-80
627626
Neuroreport. 2002 Apr 16;13(5):685-91
11973471
J Neurosci. 2006 Nov 29;26(48):12387-96
17135400
Cereb Cortex. 1993 Nov-Dec;3(6):499-514
7511011
J Neurosci. 2003 Jul 30;23(17):6876-83
12890782
J Neurosci. 2003 Feb 1;23(3):748-57
12574403
J Neurosci. 2003 Mar 1;23(5):1966-73
12629202
Neuroscience. 1996 Mar;71(1):55-75
8834392
J Neurosci. 1982 Aug;2(8):1129-49
6286904
Neurosci Lett. 2002 Jul 19;327(2):138-42
12098654
Annu Rev Neurosci. 2001;24:1071-89
11520928
Neuron. 2005 Jan 6;45(1):119-31
15629707
Learn Mem. 2007 Apr 12;14(4):318-24
17522021
J Comp Neurol. 1982 Jul 10;208(4):401-18
7119168
J Neurosci. 2006 Sep 13;26(37):9503-11
16971534
J Neurosci. 1998 Jan 1;18(1):411-8
9412517
Biol Psychiatry. 2007 May 1;61(9):1049-61
17081505
Learn Mem. 2008 Mar 05;15(3):163-71
18323571
Neuroscience. 1992 Oct;50(4):811-30
1333061
Annu Rev Cell Dev Biol. 2002;18:601-35
12142283
Nat Neurosci. 2005 May;8(5):635-41
15852010
Ann Med. 2008;40(2):92-109
18293140
J Neurosci. 1998 Jan 1;18(1):388-98
9412515
Neuropsychopharmacology. 2009 Jan;34(2):509-21
18580872
J Neurosci. 1981 Nov;1(11):1242-59
6171630
Brain Res Bull. 1986 Sep;17(3):321-33
2429740
Neuroscience. 2000;97(4):693-702
10842014
Learn Mem. 2005 Mar-Apr;12(2):130-7
15774944
Neuron. 2009 Mar 26;61(6):917-29
19324000
J Mol Neurosci. 2006;30(1-2):133-5
17192659
Eur J Neurosci. 1998 Mar;10(3):853-67
9753153
Brain Res. 1990 Jul 23;523(2):347-50
2400920
Nature. 2001 Jun 14;411(6839):801-5
11459059
Learn Mem. 2004 Sep-Oct;11(5):536-9
15466304
Eur J Neurosci. 2006 Aug;24(3):876-84
16930415
Science. 2000 Jan 14;287(5451):248-51
10634773
Nat Rev Neurosci. 2008 May;9(5):387
18401345
Behav Brain Res. 2001 Nov 1;125(1-2):195-204
11682111
J Neurosci. 1990 Apr;10(4):1043-54
2158523
Eur J Neurosci. 2002 Feb;15(3):545-52
11876782
Neuroscience. 2001;107(4):641-52
11720787
Learn Mem. 2009 Aug 25;16(9):520-9
19706835
Nature. 1999 Aug 12;400(6745):671-5
10458162
Eur J Neurosci. 2007 Dec;26(12):3631-44
18088283
Nature. 2000 Aug 17;406(6797):722-6
10963596
J Comp Neurol. 1994 Feb 1;340(1):43-64
7513719
J Comp Neurol. 1999 Sep 6;411(4):613-42
10421872
J Comp Neurol. 1987 Dec 1;266(1):45-55
3429715
J Comp Neurol. 1978 Mar 15;178(2):225-54
627625
Eur J Neurosci. 2007 Feb;25(4):1205-11
17331216
Brain Res. 1997 Jul 25;763(2):247-54
9296566
J Neurosci. 1995 Jan;15(1 Pt 1):47-60
7823151
Synapse. 2006 Sep 15;60(4):280-7
16786530
J Neurophysiol. 1998 Jan;79(1):217-26
9425193
Hippocampus. 2006;16(2):174-82
16358312
J Neurosci. 2001 Mar 15;21(6):RC135
11245704
Exp Brain Res. 1984;54(2):203-11
6327347
Cell Calcium. 1999 Dec;26(6):289-99
10668567
Acta Neurobiol Exp (Wars). 1972;32(4):835-48
4660612
Neurosci Biobehav Rev. 2004 Nov;28(7):675-85
15555677
J Neurosci. 2004 Mar 31;24(13):3281-8
15056707
Neuroscience. 1993 Jan;52(2):281-94
8450947
Behav Neurosci. 1996 Jun;110(3):618-20
8889007
J Comp Neurol. 2006 Jan 1;494(1):108-41
16304682
J Comp Neurol. 1996 Oct 14;374(2):291-313
8906500
J Comp Neurol. 1998 Feb 9;391(2):164-79
9518267
Science. 2005 Apr 1;308(5718):83-8
15746389
J Neurosci. 1998 Apr 1;18(7):2592-601
9502818
J Neurosci. 2001 Sep 1;21(17):6889-96
11517276
J Neurophysiol. 1997 Jan;77(1):341-52
9120575
Eur J Neurosci. 2003 Jun;17(12):2703-15
12823477
Neuron. 1998 May;20(5):947-57
9620699
Neuron. 1998 Jul;21(1):169-78
9697861
J Neurosci. 2000 Apr 1;20(7):2701-10
10729351
J Neurosci. 2009 Sep 2;29(35):10802-8
19726637
Science. 2000 Oct 27;290(5492):754-8
11052932
Brain Res. 1983 Dec 12;288(1-2):13-9
6198023
Neuroscience. 2002;111(1):133-49
11955718
Eur J Neurosci. 2005 Jul;22(1):201-11
16029210
J Comp Neurol. 1989 Mar 8;281(2):320-33
2468696
Science. 2004 May 7;304(5672):881-3
15131309
J Comp Neurol. 2006 Sep 1;498(1):142-61
16856165
Mol Neurobiol. 2007 Aug;36(1):92-101
17952654
Br J Pharmacol. 1994 Nov;113(3):1029-35
7858845
Neuron. 2002 Nov 14;36(4):727-38
12441060
Annu Rev Neurosci. 2009;32:289-313
19400714
Neuroscience. 1999;89(4):1025-39
10362292
Learn Mem. 2008 May 05;15(5):304-14
18463174
Mol Pharmacol. 2006 Jan;69(1):299-308
16219906
Brain Res. 2005 Feb 21;1035(1):32-40
15713274
J Abnorm Psychol. 1986 Nov;95(4):365-72
3805500
Learn Mem. 2001 Jan-Feb;8(1):11-9
11160759
Science. 2007 Apr 20;316(5823):457-60
17446403
Behav Res Ther. 2002 Feb;40(2):173-84
11814181
Nat Rev Neurosci. 2004 Jan;5(1):45-54
14708003
Synapse. 1992 Aug;11(4):310-8
1354397
J Neurosci. 2003 Nov 12;23(32):10283-91
14614087
Nat Rev Neurosci. 2009 Mar;10(3):224-34
19229241
J Comp Neurol. 1998 Aug 31;398(3):431-58
9714153
J Comp Neurol. 1977 Apr 15;172(4):687-722
838895
Nature. 1997 Dec 11;390(6660):604-7
9403688
Brain Res. 1982 Apr 29;238(2):457-62
7093668
Nat Neurosci. 2006 Apr;9(4):481-3
16547510
Neurobiol Learn Mem. 2006 Mar;85(2):192-7
16290195
J Psychiatr Res. 2008 Jun;42(7):515-20
18313695
J Neurosci. 2009 Aug 5;29(31):9700-3
19657022
Nat Neurosci. 2009 Mar;12(3):256-8
19219038
J Clin Psychiatry. 2009;70 Suppl 2:4-9
19371500
Mol Psychiatry. 2007 Feb;12(2):120-50
17160066
Neuron. 2003 Dec 4;40(5):1013-22
14659099
Genes Brain Behav. 2006;5 Suppl 2:34-47
16681799
Front Neural Circuits. 2008 Nov 24;2:3
19104668
Behav Neurosci. 1992 Jun;106(3):569-574
1352104
Eur J Neurosci. 1999 Apr;11(4):1217-22
10103117
Eur J Neurosci. 2003 Dec;18(11):3080-8
14656303
J Comp Neurol. 1993 May 8;331(2):199-224
7685361
Nature. 2002 May 16;417(6886):282-7
12015602
Eur J Neurosci. 2008 Dec;28(11):2299-309
19019199
Brain Res. 1998 Jun 15;796(1-2):132-42
9689463
J Comp Neurol. 2000 Oct 23;426(3):441-67
10992249
Science. 2007 Aug 31;317(5842):1230-3
17761885
J Comp Neurol. 1982 Apr 1;206(2):159-79
7085926
Neuroscience. 1993 Dec;57(4):1061-76
8309543
Nature. 2003 Apr 3;422(6931):518-22
12673250
J Physiol. 2007 Nov 15;585(Pt 1):117-34
17916608
Neuron. 1999 Jun;23(2):229-32
10399930
Prog Brain Res. 2008;169:27-40
18394466
Z Zellforsch Mikrosk Anat. 1972;134(4):439-58
4638299
Mol Cell Neurosci. 2007 Jun;35(2):356-67
17482476
J Comp Neurol. 1995 Sep 18;360(2):185-212
8522643
J Neurophysiol. 2001 Feb;85(2):714-23
11160506
J Neurosci. 2004 Sep 1;24(35):7654-62
15342732
Neuron. 2005 Sep 15;47(6):783-6
16157273
J Abnorm Psychol. 2000 May;109(2):290-8
10895567
Brain Res. 1981 Jul 27;217(1):150-4
7260612
Learn Mem. 2009 Jul 24;16(8):486-93
19633138
J Neurophysiol. 1998 Jan;79(1):205-16
9425192
Learn Mem. 2009 May 27;16(6):395-405
19474217
Science. 2004 Oct 15;306(5695):487-91
15486301
J Comp Neurol. 1986 Apr 22;246(4):478-99
2422231
J Neurosci. 2002 Sep 15;22(18):7892-902
12223542
J Neurosci. 2000 Nov 1;20(21):8177-87
11050141
J Neurosci. 2005 Jan 12;25(2):502-6
15647495
Proc Natl Acad Sci U S A. 2009 Jul 14;106(28):11737-41
19567836
Prog Neurobiol. 1998 Jun;55(3):257-332
9643556
Neuroscientist. 2005 Aug;11(4):323-33
16061519
Hippocampus. 2003;13(1):53-8
12625457
J Neurophysiol. 2004 Sep;92(3):1285-94
15128752
Eur J Neurosci. 2007 Mar;25(6):1823-31
17408428
Neurobiol Learn Mem. 2007 Jan;87(1):149-58
16979915
Nature. 1998 Aug 13;394(6694):683-7
9716132
J Neurosci. 2002 Jan 1;22(1):324-37
11756516
J Neurosci. 2004 Apr 14;24(15):3810-5
15084662
Neurosci Lett. 1995 Dec 29;202(1-2):45-8
8787827
J Neurosci. 1996 May 15;16(10):3334-50
8627370
Learn Mem. 2008 Oct 02;15(10):747-55
18832561
Eur J Neurosci. 1999 Jan;11(1):187-203
9987023
J Neurosci. 2005 Aug 10;25(32):7366-76
16093387
Eur J Neurosci. 2004 Jul;20(2):549-56
15233764
Neuron. 2008 Nov 26;60(4):683-97
19038224
Neuron. 2008 Sep 25;59(6):914-31
18817731
Nat Neurosci. 2006 Jul;9(7):870-2
16783370
Learn Mem. 2009 Jun 24;16(7):421-5
19553379
J Neurosci. 1996 May 1;16(9):3056-66
8622135
Nature. 2008 Jul 31;454(7204):600-6
18615015
Kaibogaku Zasshi. 1996 Oct;71(5):523-40
8953850
J Neurosci. 2002 Jun 15;22(12):5239-49
12077219
Neuroscience. 2001;105(3):681-93
11516833
Nat Neurosci. 2000 Jan;3(1):74-9
10607398
Science. 2001 Nov 2;294(5544):1030-8
11691980
Neurobiol Learn Mem. 2008 Mar;89(3):324-37
17977027
Mol Brain. 2009 Mar 05;2:7
19265511
Neuroreport. 2007 Jul 16;18(11):1107-11
17589308
Eur J Neurosci. 2004 Aug;20(3):781-90
15255988
J Neurosci. 1994 Apr;14(4):2200-24
8158266
Nature. 1997 Nov 20;390(6657):281-6
9384379
J Clin Psychiatry. 2009;70 Suppl 2:15-9
19371502
Prog Neurobiol. 2000 Aug;61(6):611-48
10775799
Physiol Behav. 1979 Dec;23(6):1109-17
542522
J Neurosci. 2003 Apr 1;23(7):2549-56
12684439
EMBO J. 2006 Jun 21;25(12):2867-77
16710293
Proc Natl Acad Sci U S A. 2003 Apr 1;100(7):4287-92
12646704
J Comp Neurol. 1980 Jun 15;191(4):545-56
7419733
J Neurosci. 2000 Dec 1;20(23):8909-15
11102501
Behav Neurosci. 1993 Oct;107(5):757-769
8280386
J Neurosci. 1998 Oct 15;18(20):8444-54
9763487
Nat Rev Neurosci. 2009 Jun;10(6):423-33
19469026
Neuropsychopharmacology. 2006 Feb;31(2):278-86
15988467
J Neurophysiol. 1995 Sep;74(3):1179-91
7500142
J Neurosci. 2007 Feb 21;27(8):2045-57
17314300
J Comp Neurol. 2006 Jan 1;494(1):142-78
16304685
J Physiol. 1970 Apr;207(2):61P
5511138
J Neurosci. 2002 Mar 1;22(5):1618-28
11880492
Neuron. 2007 Mar 15;53(6):871-80
17359921
Learn Mem. 2005 May-Jun;12(3):277-84
15930506
Nat Neurosci. 2007 Apr;10(4):414-6
17351634
Mol Cell Neurosci. 2008 Nov;39(3):491-8
18790060
J Comp Neurol. 1995 May 29;356(2):288-310
7629320
Biol Psychiatry. 2007 Sep 1;62(5):446-54
17217927
J Neurosci. 2004 Jun 23;24(25):5704-10
15215292
J Neurosci. 2006 Dec 13;26(50):12977-83
17167087
J Exp Psychol Anim Behav Process. 1975 Jan;1(1):88-96
1151290
Nat Neurosci. 2003 Jun;6(6):587-92
12740581
Behav Neurosci. 1991 Feb;105(1):126-33
1673846
Learn Mem. 2000 Mar-Apr;7(2):97-103
10753976
Synapse. 1999 Sep 1;33(3):218-29
10420169
J Physiol. 2003 Oct 15;552(Pt 2):483-97
14561831
J Neurosci. 2001 Mar 1;21(5):1720-6
11222661
Neuron. 2002 Aug 15;35(4):605-23
12194863
J Neurosci. 2001 Nov 15;21(22):9009-17
11698611
Nature. 1990 Jun 21;345(6277):716-8
1972778
Nat Rev Neurosci. 2005 Feb;6(2):119-30
15685217
Nat Neurosci. 2004 Jun;7(6):635-42
15133516
J Neurosci. 2008 Dec 24;28(52):14202-12
19109502
J Comp Neurol. 2008 Feb 20;506(6):943-59
18085591
J Neurosci. 2009 Aug 12;29(32):10131-43
19675247
J Neurobiol. 1999 Sep 5;40(3):343-55
10440734
Brain Struct Funct. 2007 Sep;212(2):149-79
17717690
Neuron. 2009 Jun 25;62(6):757-71
19555645
J Neurosci. 2004 Feb 25;24(8):1962-6
14985438
Neuron. 2004 Sep 30;44(1):75-91
15450161
Nature. 2002 Aug 1;418(6897):530-4
12152079
Ann N Y Acad Sci. 2006 Jul;1071:67-79
16891563
Mol Pharmacol. 2003 Jan;63(1):44-52
12488535
J Neurosci. 2005 Aug 10;25(32):7429-37
16093394
Neuroscience. 1995 Nov;69(2):567-83
8552250
J Neurosci. 2003 Jan 1;23(1):52-63
12514201
Neuroscience. 2005;134(1):247-60
15951121
Nat Rev Neurosci. 2007 Jun;8(6):413-26
17514195
Proc Natl Acad Sci U S A. 1999 Jan 5;96(1):5-7
9874760
J Neurosci. 2001 Aug 15;21(16):RC162
11473133
J Neurosci. 2008 Feb 27;28(9):2089-98
18305243
Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11668-73
11573004
J Exp Psychol Anim Behav Process. 1979 Oct;5(4):368-78
528893
Nature. 2002 Nov 7;420(6911):70-4
12422216
J Neurosci. 2006 Jun 14;26(24):6573-82
16775145
Neuron. 2005 Apr 7;46(1):141-51
15820700
Nature. 1999 Sep 2;401(6748):63-9
10485705
PLoS Biol. 2008 Dec 23;6(12):2698-706
19108606
Neuroscience. 1997 Apr;77(3):767-81
9070751
J Neurosci. 2007 Jan 24;27(4):840-4
17251424
J Neurosci. 2005 Oct 19;25(42):9680-5
16237172
Neuron. 2002 Apr 11;34(2):289-300
11970870
J Neurosci. 2002 Oct 15;22(20):9113-21
12388619
Behav Brain Res. 1985 Aug;16(2-3):117-33
4041212
Ann N Y Acad Sci. 2000 Jun;911:369-91
10911886
J Neurophysiol. 2000 Jun;83(6):3509-18
10848566
J Neurosci. 2003 Sep 10;23(23):8310-7
12967993
J Neurosci. 2002 Mar 15;22(6):2343-51
11896173
Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):15130-5
18815362
Learn Mem. 2004 Sep-Oct;11(5):598-603
15466314
J Neurosci. 2007 Oct 10;27(41):10947-56
17928436
Pharmacol Biochem Behav. 2002 Mar;71(3):393-400
11830173
Biol Psychiatry. 2002 Nov 15;52(10):958-75
12437937
J Neurosci. 1999 Feb 1;19(3):955-63
9920659
Learn Mem. 2001 May-Jun;8(3):156-63
11390635
J Comp Neurol. 2004 Jan 6;468(2):277-98
14648685
Neuroscience. 1995 Jun;66(4):959-82
7651623
Nat Neurosci. 2006 Aug;9(8):1028-35
16819521
J Neurosci. 2001 Jun 1;21(11):4090-103
11356897
J Neurosci. 1998 Sep 15;18(18):7452-61
9736664
Exp Brain Res. 1990;82(3):606-16
1705519
J Neurophysiol. 1991 Sep;66(3):999-1009
1684384
Ann N Y Acad Sci. 2006 Jul;1071:324-34
16891581
J Neurosci. 2008 Jan 9;28(2):369-75
18184779
Mol Cell Neurosci. 2006 Sep;33(1):57-67
16861000
Nat Neurosci. 2007 Aug;10(8):1012-9
17632506
Neurobiol Learn Mem. 2008 Jul;90(1):36-43
18226933
J Neurosci. 2000 Sep 1;20(17):6317-25
10964936
Brain Res Mol Brain Res. 2001 Oct 19;94(1-2):15-24
11597761
Brain Res Bull. 1992 Feb;28(2):179-85
1375860
Annu Rev Neurosci. 2000;23:155-84
10845062
J Neurosci. 2004 Oct 27;24(43):9507-12
15509737
Synapse. 2000 Nov;38(2):124-37
11018786
Learn Mem. 2006 Mar-Apr;13(2):216-23
16585797
Nature. 1997 Dec 11;390(6660):607-11
9403689
Neuron. 2008 Jun 12;58(5):662-71
18549779
J Biol Chem. 2002 Nov 29;277(48):46720-9
12351629
Neuroscience. 2005;132(4):943-53
15857700
J Comp Neurol. 1989 Jan 15;279(3):470-88
2918082
J Neurosci. 2005 Feb 16;25(7):1847-55
15716421
Exp Brain Res. 1978 Aug 15;32(4):529-47
689127
Cell. 1994 Oct 7;79(1):59-68
7923378
J Neurosci. 2007 Jan 17;27(3):553-63
17234587
Nat Rev Neurosci. 2003 Nov;4(11):923-6
14595403
J Neurosci. 2000 Dec 15;20(24):9017-24
11124977
Br J Pharmacol. 2008 Mar;153 Suppl 1:S35-43
18026130
J Neurobiol. 1999 Oct;41(1):108-18
10504198
Hippocampus. 2007;17(9):749-58
17604353
J Neurosci. 2006 Jun 21;26(25):6677-86
16793875
Eur J Neurosci. 2006 Jul;24(1):261-9
16882022
Neurosci Lett. 2004 Nov 23;371(2-3):152-7
15519747
Neuroscience. 1993 Dec;57(3):697-715
8309532
J Comp Neurol. 2006 Jan 1;494(1):75-107
16304681
Neuron. 2005 Dec 22;48(6):1025-37
16364905
J Neurosci. 2008 Oct 22;28(43):10803-13
18945888
Neuroscience. 1993 Dec;57(4):1077-90
8309544
Nat Neurosci. 2002 Jun;5(6):573-9
12006982
J Neurosci. 1992 Oct;12(10):4066-79
1403101
Learn Mem. 1998 Sep-Oct;5(4-5):274-88
10454354
Nature. 2003 Dec 18;426(6968):841-5
14685239
Cogn Affect Behav Neurosci. 2001 Mar;1(1):66-82
12467104
J Neurosci. 1992 Mar;12(3):854-63
1347562
Nat Neurosci. 2002 Sep;5(9):837-8
12172550
Prog Brain Res. 2008;169:117-43
18394471
Cell. 2004 Dec 29;119(7):1041-54
15620361
Annu Rev Neurosci. 2008;31:25-46
18275283
J Neurosci. 2001 Dec 1;21(23):9506-18
11717385
Mol Psychiatry. 2008 Oct;13(10):970-9
17712315
Eur J Neurosci. 2002 May;15(9):1535-41
12028364
Exp Brain Res. 2000 Oct;134(4):520-32
11081834
J Comp Neurol. 2006 Feb 1;494(4):635-50
16374802
Curr Opin Pharmacol. 2007 Feb;7(1):39-47
17088105
Nat Neurosci. 2001 Jul;4(7):724-31
11426229
Trends Neurosci. 1998 Jun;21(6):240-1
9641534
Neuron. 2001 Sep 13;31(5):841-51
11567621
Behav Pharmacol. 2003 Dec;14(8):649-52
14665982
Hippocampus. 2005;15(7):874-80
16158424
Learn Mem. 2009 Feb 23;16(3):193-7
19237641
Mol Pharmacol. 2004 May;65(5):1286-92
15102957
J Hirnforsch. 1975;16(3):175-201
1214051
J Neurosci. 2000 Dec 15;20(24):9034-9
11124979
Proc Natl Acad Sci U S A. 2008 Jul 1;105(26):9087-92
18579781
Science. 2003 Aug 8;301(5634):846-50
12907806
Neuron. 1995 Jul;15(1):127-36
7619517
J Neurophysiol. 1992 Aug;68(2):551-69
1527575