Adult hippocampal neurogenesis: regulation, functional implications, and contribution to disease pathology.
It is now well established that the mammalian brain has the capacity to produce new neurons into adulthood. One such region that provides the proper milieu to sustain progenitor cells and is permissive to neuronal fate determination is located in the dentate gyrus of the hippocampus. This review will discuss in detail the complex process of adult hippocampal neurogenesis, including proliferation, differentiation, survival, and incorporation into neuronal networks. The regulation of this phenomenon by a number of factors is described, including neurotransmitter systems, growth factors, paracrine signaling molecules, neuropeptides, transcription factors, endogenous psychotropic systems, sex hormones, stress, and others. This review also addresses the functional significance of adult born hippocampal granule cells with regard to hippocampal circuitry dynamics and behavior. Furthermore, the relevance of perturbations in adult hippocampal neurogenesis to the pathophysiology of various disease states, including depression, schizophrenia, epilepsy, and diabetes are examined. Finally, this review discusses the potential of using hippocampal neurogenesis as a therapeutic target for these disorders.
Balu
Darrick T
DT
Department of Pharmacology, University of Pennsylvania, Philadelphia, PA, USA.
Lucki
Irwin
I
D000818:Animals; D002453:Cell Cycle / Q000502:physiology; D016923:Cell Death / Q000502:physiology; D003866:Depressive Disorder / Q000503:physiopathology; D003920:Diabetes Mellitus / Q000503:physiopathology; D004827:Epilepsy / Q000503:physiopathology; D006624:Hippocampus / Q000502:physiology* / Q000503:physiopathology*; D006801:Humans; D055495:Neurogenesis / Q000502:physiology*; D009474:Neurons / Q000502:physiology; D012559:Schizophrenia / Q000503:physiopathology; D015398:Signal Transduction / Q000502:physiology; D013234:Stem Cells / Q000502:physiology; D013315:Stress, Psychological / Q000503:physiopathology
Neuron. 1991 Jun;6(6):937-48
2054188
Brain Res. 1990 Dec 10;535(2):195-204
1705855
Nature. 2001 Mar 15;410(6826):372-6
11268214
Biol Psychiatry. 2002 Dec 1;52(11):1057-65
12460689
Hippocampus. 2006;16(3):321-8
16435310
Eur J Neurosci. 2002 Jul;16(1):129-36
12153537
Biol Psychiatry. 2006 Jun 15;59(12):1136-43
16797263
Neuroscience. 2006 Oct 13;142(2):505-14
16889901
Cereb Cortex. 2003 Aug;13(8):845-51
12853371
Nature. 2004 May 13;429(6988):184-7
15107864
Brain. 2007 Dec;130(Pt 12):3321-35
18055496
Brain Pathol. 2004 Jul;14(3):237-48
15446578
J Neurosci. 2004 Mar 3;24(9):2133-42
14999064
Nat Neurosci. 2004 Jul;7(7):726-35
15195095
Mol Psychiatry. 2003 Nov;8(12):974-82
14647395
Br J Psychiatry. 2001 Mar;178:200-6
11230029
Genes Dev. 2002 Mar 1;16(5):548-53
11877374
J Neurosci. 2005 Feb 2;25(5):1089-94
15689544
Proc Natl Acad Sci U S A. 2006 May 23;103(21):8233-8
16702546
J Neuroendocrinol. 2004 Aug;16(8):704-10
15271063
Eur J Neurosci. 2005 Mar;21(5):1304-14
15813940
Am J Psychiatry. 2000 Jan;157(1):115-8
10618023
Prog Brain Res. 2007;163:529-40
17765736
J Neurosci. 1999 Jun 15;19(12):5034-43
10366636
J Neurosci. 2007 Apr 4;27(14):3845-54
17409249
J Neurosci. 1992 Sep;12(9):3642-50
1527603
Neuroscience. 1998 Jan;82(2):349-54
9466447
Nat Rev Neurosci. 2006 Mar;7(3):179-93
16495940
Am J Pathol. 2001 Feb;158(2):453-68
11159183
Science. 1997 Apr 4;276(5309):66-71
9082987
Methods Cell Biol. 2008;85:243-72
18155466
J Neurosci. 2000 Dec 15;20(24):9104-10
11124987
Neuropsychopharmacology. 2004 Apr;29(4):747-58
14702022
J Neurosci. 1984 Jun;4(6):1429-41
6726341
Neuron. 2005 Sep 15;47(6):803-15
16157276
J Affect Disord. 2002 Apr;68(2-3):261-71
12063154
J Neurochem. 2005 May;93(3):560-70
15836615
Trends Neurosci. 2007 Jan;30(1):1-8
17116335
Proc Natl Acad Sci U S A. 2007 Dec 18;104(51):20558-63
18077357
Neurobiol Aging. 2004 Mar;25(3):361-75
15123342
Mol Psychiatry. 2008 Jul;13(7):717-28
17700577
Neurobiol Dis. 2007 Apr;26(1):174-88
17317195
Exp Brain Res. 2006 Apr;170(4):501-12
16328260
Exp Neurol. 2005 Apr;192(2):348-56
15755552
Eur J Neurosci. 2006 Oct;24(7):1845-9
17067290
Nature. 2005 Oct 6;437(7060):894-7
16208373
Science. 2001 Jun 1;292(5522):1728-31
11387480
J Neurosci. 2007 Jul 18;27(29):7860-8
17634380
Proc Natl Acad Sci U S A. 2008 Jan 29;105(4):1358-63
18172194
Science. 2007 Aug 10;317(5839):819-23
17615305
J Pharmacol Exp Ther. 2001 Nov;299(2):401-7
11602648
J Neurosci. 2006 May 31;26(22):5888-93
16738230
Mol Cell Neurosci. 2003 Sep;24(1):23-40
14550766
Neuroscience. 1993 Dec;57(4):913-22
8309552
Nat Neurosci. 2004 Aug;7(8):841-6
15273691
Nat Neurosci. 1999 Mar;2(3):266-70
10195220
Proc Natl Acad Sci U S A. 2003 Aug 5;100(16):9566-71
12886012
Cell Tissue Res. 2008 Jan;331(1):243-50
17938969
Dev Neurosci. 2007;29(1-2):84-90
17148951
Pharmacol Rep. 2005 Nov-Dec;57(6):845-9
16382206
Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15718-23
9861036
Proc Natl Acad Sci U S A. 2001 May 8;98(10):5874-9
11320217
Neurosci Res. 1997 Jun;28(2):103-10
9220467
Mol Cell Neurosci. 2007 Jun;35(2):261-71
17459722
J Neurobiol. 2003 May;55(2):247-60
12672021
Am J Psychiatry. 2003 Aug;160(8):1516-8
12900317
J Comp Neurol. 1985 Oct 8;240(2):143-52
4056107
J Neurosci. 2008 Feb 6;28(6):1374-84
18256257
Mol Cell Neurosci. 1995 Oct;6(5):474-86
8581317
Neurobiol Dis. 2004 Mar;15(2):196-205
15006689
Eur J Neurosci. 2008 Mar;27(6):1485-93
18336568
Eur J Neurosci. 2004 May;19(9):2377-87
15128392
FASEB J. 2005 Oct;19(12):1704-6
16037095
J Comp Neurol. 1994 Feb 22;340(4):551-65
7911808
J Neurosci. 2000 Apr 15;20(8):2896-903
10751442
Brain Res Bull. 2004 Dec 15;64(4):303-8
15561464
Mol Cell Neurosci. 2003 Jul;23(3):373-82
12837622
J Neurosci. 1993 Jun;13(6):2351-8
7684771
J Neurosci. 2007 Nov 7;27(45):12156-67
17989282
Exp Neurol. 2007 Feb;203(2):320-32
17049346
Neuroscience. 1993 Sep;56(2):337-44
8247264
Brain Res. 2004 Aug 13;1017(1-2):21-31
15261095
J Neural Transm (Vienna). 1998;105(2-3):317-27
9660110
Epilepsia. 2003 May;44(5):647-58
12752463
Proc Natl Acad Sci U S A. 2001 Sep 11;98(19):10910-7
11526209
Neuropsychopharmacology. 2003 Sep;28(9):1562-71
12838272
Mol Cell Neurosci. 2003 Nov;24(3):603-13
14664811
J Neurosci. 2006 Apr 12;26(15):4095-103
16611826
Nat Neurosci. 2008 Mar;11(3):277-84
18297065
Brain Res. 2006 Sep 19;1110(1):221-5
16876769
Neuroscience. 2005;135(3):803-13
16129565
Stress. 1998 Jul;2(3):171-81
9787265
Nat Neurosci. 2006 Jun;9(6):729-31
16648847
Genes Cells. 2006 Oct;11(10):1145-59
16999735
J Neurosci. 1997 May 15;17(10):3727-38
9133393
Eur J Neurosci. 2001 Nov;14(10):1603-12
11860455
Eur J Neurosci. 2003 May;17(10):2042-6
12786970
Proc Natl Acad Sci U S A. 2008 Jan 15;105(2):751-6
18178625
Nat Neurosci. 2003 Jan;6(1):21-7
12469128
Brain Res. 1993 May 21;611(2):342-6
8392896
Mol Cell Biol. 2005 Mar;25(5):1869-78
15713641
Neuroscience. 2005;136(2):381-6
16216425
J Neurosci. 2001 Sep 1;21(17):6718-31
11517261
J Neurosci. 2002 Feb 1;22(3):635-8
11826092
FASEB J. 2008 Jul;22(7):2253-62
18263701
J Comp Neurol. 1965 Jun;124(3):319-35
5861717
J Neurosci. 2005 Nov 2;25(44):10074-86
16267214
Brain Res. 2006 Feb 23;1075(1):48-59
16460708
Neurobiol Dis. 2007 Apr;26(1):47-55
17270453
Proc Natl Acad Sci U S A. 2000 Jun 20;97(13):7579-84
10840056
Proc Natl Acad Sci U S A. 2002 Sep 3;99(18):11946-50
12181492
Proc Natl Acad Sci U S A. 2004 Sep 14;101(37):13648-53
15347806
Biol Psychiatry. 2006 Apr 1;59(7):619-24
16325782
Eur J Neurosci. 2006 Jul;24(2):586-94
16903860
Metabolism. 2005 May;54(5 Suppl 1):20-3
15877308
J Neurosci. 2007 Dec 26;27(52):14317-25
18160639
Biochem Biophys Res Commun. 2003 Nov 28;311(4):1019-25
14623284
Am J Psychiatry. 2000 Nov;157(11):1738-51
11058466
Curr Biol. 2002 Apr 2;12(7):606-8
11937032
J Neurosci. 1995 Mar;15(3 Pt 1):1768-77
7891134
J Clin Invest. 2005 Nov;115(11):3104-16
16224541
Genes Dev. 1999 Jun 15;13(12):1501-12
10385618
Biol Psychiatry. 2006 Jun 15;59(12):1116-27
16631126
Neuroscience. 2001;107(4):603-13
11720784
Learn Mem. 2007 May 10;14(5):368-75
17522028
Exp Brain Res. 1988;72(2):399-406
2465172
Nature. 2002 May 2;417(6884):39-44
11986659
J Comp Neurol. 2004 Oct 25;478(4):359-78
15384070
Nature. 2008 Feb 21;451(7181):1004-7
18235445
J Comp Neurol. 2001 Sep 3;437(4):496-504
11503148
Trends Neurosci. 2000 Nov;23(11):542-9
11074263
J Neurophysiol. 2005 Dec;94(6):4528-32
16033936
Cell Mol Neurobiol. 2006 Jul-Aug;26(4-6):943-57
16807785
Prog Brain Res. 2007;163:697-722
17765746
Nat Neurosci. 2008 Mar;11(3):309-17
18278039
Neurosci Lett. 2004 Aug 5;366(1):107-11
15265600
Proc Natl Acad Sci U S A. 1993 Mar 1;90(5):2074-7
8446631
Nature. 2006 Aug 24;442(7105):929-33
16906136
Epilepsia. 2002;43 Suppl 5:68-73
12121298
Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):3168-71
9501234
Neurosci Lett. 2000 Sep 8;291(1):17-20
10962143
Proc Natl Acad Sci U S A. 1983 Apr;80(8):2390-4
6572982
Neuroendocrinology. 2001 Aug;74(2):135-42
11474221
New Biol. 1991 Mar;3(3):259-69
1715184
Neurosci Lett. 2000 Oct 27;293(2):91-4
11027841
J Neurosci. 2006 Jan 11;26(2):609-21
16407559
Proc Natl Acad Sci U S A. 1996 Apr 30;93(9):3908-13
8632988
Mol Cell Neurosci. 1998 Jul;11(4):234-45
9675054
Mol Cell Neurosci. 2008 Feb;37(2):402-11
18086533
J Neurosci. 1997 Apr 1;17(7):2492-8
9065509
J Pharmacol Sci. 2007 Mar;103(3):299-308
17341843
Ann Neurol. 2006 Jan;59(1):81-91
16261566
Biol Psychiatry. 2004 Oct 15;56(8):570-80
15476686
Eur J Pharmacol. 2001 Jan 5;411(1-2):67-70
11137860
Nature. 1998 May 28;393(6683):382-6
9620803
Eur J Neurosci. 2004 Jun;19(12):3219-26
15217378
Science. 1999 Oct 15;286(5439):548-52
10521353
Eur J Neurosci. 2003 Oct;18(7):1828-36
14622216
Eur J Neurosci. 2003 Nov;18(10):2803-12
14656329
Hippocampus. 2002;12(5):578-84
12440573
Eur J Neurosci. 2007 Oct;26(7):1765-79
17883411
Eur J Neurosci. 2005 Jan;21(2):513-21
15673450
Mol Psychiatry. 2004 Mar;9(3):278-86, 224
14699428
J Neural Transm (Vienna). 2004 Jan;111(1):91-100
14714218
J Comp Neurol. 2002 Dec 9;454(2):105-14
12412137
Development. 2003 Jan;130(2):391-9
12466205
Neuroscience. 2007 Feb 9;144(3):855-64
17157994
Eur J Neurosci. 2002 Nov;16(10):2008-12
12453065
Eur J Pharmacol. 2008 Mar 31;583(1):115-27
18289522
Neuropsychopharmacology. 2004 Jul;29(7):1230-8
15085089
Nat Rev Neurosci. 2002 Jan;3(1):24-33
11823802
Cell. 2007 Sep 21;130(6):1146-58
17825401
Nature. 2006 Feb 2;439(7076):589-93
16341203
Hippocampus. 2005;15(6):722-38
15986407
Neuroscience. 1999;89(4):999-1002
10362289
Biol Psychiatry. 2000 Jun 15;47(12):1043-9
10862803
Brain Res Dev Brain Res. 2005 Jun 9;157(1):42-57
15939084
Brain Res. 2001 Feb 2;890(2):261-71
11164792
Proc Natl Acad Sci U S A. 2007 Oct 23;104(43):17169-73
17940008
J Neurochem. 1998 Mar;70(3):1327-30
9489757
Eur J Neurosci. 2000 Jan;12(1):391-6
10651896
J Comp Neurol. 2003 Dec 22;467(4):455-63
14624480
Neuron. 1999 Jun;23(2):247-56
10399932
Nature. 2003 May 22;423(6938):409-14
12717450
Biol Psychiatry. 2005 Dec 1;58(11):871-8
16043138
J Neurosci. 2007 Aug 29;27(35):9400-7
17728453
J Neurosci Res. 2004 Jul 15;77(2):155-65
15211583
J Neurosci. 1999 Jul 15;19(14):5792-801
10407020
J Clin Pharm Ther. 2006 Dec;31(6):523-34
17176358
Brain Res. 2007 Oct 3;1172:10-20
17803978
Dev Neurobiol. 2007 Sep 1;67(10):1321-33
17638384
Science. 2005 Oct 28;310(5748):679-83
16254185
J Neurosci. 1996 Apr 1;16(7):2365-72
8601816
Nat Neurosci. 2005 Sep;8(9):1179-87
16116450
Nat Neurosci. 2007 Sep;10(9):1110-5
17726477
Neuroscience. 1994 Jul;61(2):203-9
7969902
Prog Brain Res. 2007;163:399-415
17765731
Mol Pharmacol. 2004 Aug;66(2):204-8
15266010
Neuropsychopharmacology. 2008 Aug;33(9):2251-62
17987063
Science. 2007 Nov 9;318(5852):980-5
17991865
J Neurosci. 2002 Nov 15;22(22):9868-76
12427843
Nat Neurosci. 1999 Mar;2(3):260-5
10195219
Nat Neurosci. 2004 Nov;7(11):1233-41
15494728
Neuroscience. 2006 Aug 25;141(2):827-836
16735094
J Comp Neurol. 1999 Apr 19;406(4):449-60
10205022
Front Horm Res. 2006;35:157-168
16809931
Philos Trans R Soc Lond B Biol Sci. 2006 Sep 29;361(1473):1477-97
16939970
J Neurosci. 2006 Feb 22;26(8):2326-34
16495460
Proc Natl Acad Sci U S A. 1999 Apr 27;96(9):5263-7
10220454
Neuroscience. 2003;119(3):635-42
12809684
Neuroscience. 2004;127(4):881-91
15312900
J Neurosci. 1999 Jun 1;19(11):4508-19
10341251
Curr Pharm Biotechnol. 2007 Jun;8(3):147-65
17584088
Proc Natl Acad Sci U S A. 1995 Sep 26;92(20):9225-9
7568106
Curr Diab Rep. 2006 Dec;6(6):431-8
17118225
Neuropsychopharmacology. 2004 Jun;29(6):1063-9
15010699
Exp Gerontol. 2005 May;40(5):450-3
15885957
Trends Neurosci. 2004 Aug;27(8):447-52
15271491
Science. 1977 Sep 9;197(4308):1092-4
887941
Stem Cells. 2007 Oct;25(10):2396-407
17600108
Ann N Y Acad Sci. 2002 May;962:226-41
12076978
Proc Natl Acad Sci U S A. 1997 Sep 16;94(19):10432-7
9294228
Psychopharmacology (Berl). 2008 Oct;200(2):231-42
18512047
J Neurobiol. 2002 May;51(2):115-28
11932953
J Comp Neurol. 1969 Dec;137(4):433-57
5361244
Nature. 1965 Aug 28;207(5000):953-6
5886931
J Neurosci. 2004 Aug 25;24(34):7477-81
15329394
Brain Res. 2002 Nov 15;955(1-2):264-7
12419546
Exp Neurol. 2008 Apr;210(2):359-67
18190910
Eur J Neurosci. 2005 Oct;22(7):1570-80
16197497
Brain Res. 1998 Apr 20;790(1-2):52-9
9593820
J Neurosci. 2002 Apr 15;22(8):3262-8
11943827
J Neurosci. 2000 Aug 15;20(16):6144-58
10934264
Biochem J. 1998 Oct 1;335 ( Pt 1):1-13
9742206
J Med Genet. 2003 May;40(5):325-32
12746393
Neuron. 2007 Sep 6;55(5):712-25
17785179
Acta Neurol Scand. 2008 Mar;117(3):205-10
17854417
Science. 2003 Dec 5;302(5651):1760-5
14615545
Neuropsychopharmacology. 2005 Feb;30(2):231-41
15536491
Nat Med. 1998 Nov;4(11):1313-7
9809557
J Neurosci. 1995 Jun;15(6):4687-92
7790933
Learn Mem. 2006 May-Jun;13(3):307-15
16705139
Br Med J. 1968 Aug 3;3(5613):285-7
4385601
Neurobiol Dis. 2005 Apr;18(3):523-7
15755679
Nature. 2002 Feb 28;415(6875):1030-4
11875571
Brain Res. 2004 Mar 12;1000(1-2):195-9
15053968
Synapse. 2004 Dec 15;54(4):200-6
15472930
Neuroscience. 2006 Sep 15;141(4):1793-800
16797852
J Neurosci Res. 2002 Jul 1;69(1):72-9
12111817
Neurosci Lett. 1998 May 29;248(2):73-6
9654345
Eur J Neurosci. 2005 Aug;22(4):785-92
16115202
Nat Neurosci. 2006 Jun;9(6):723-7
16732202
Eur J Neurosci. 2004 Aug;20(4):885-95
15305857
Neuroscience. 2006;137(1):83-92
16289354
Hippocampus. 2006;16(3):233-8
16411244
J Neurosci. 2001 Sep 1;21(17):6706-17
11517260
Science. 2001 Dec 7;294(5549):2127-30
11739948
J Comp Neurol. 1998 Apr 27;394(1):91-105
9550144
Eur J Neurosci. 2005 Feb;21(4):871-8
15787693
Mol Psychiatry. 2002;7(3):254-75
11920153
J Comp Neurol. 1999 Oct 11;413(1):146-54
10464376
J Neurosci. 2007 May 2;27(18):4894-901
17475797
J Neurosci. 2001 Sep 15;21(18):7153-60
11549726
Radiat Res. 2004 Jul;162(1):39-47
15222778
Neurobiol Dis. 2004 Dec;17(3):473-90
15571983
Proc Natl Acad Sci U S A. 2006 Nov 14;103(46):17501-6
17088541
J Neurosci. 2006 Jul 5;26(27):7272-80
16822985
Annu Rev Cell Dev Biol. 2001;17:387-403
11687494
Neuroscience. 2004;129(3):593-601
15541881
Neurosci Lett. 2005 Sep 2;385(1):70-5
15967575
Eur J Neurosci. 2006 Oct;24(7):1850-6
17040481
Proc Natl Acad Sci U S A. 1994 May 10;91(10):4214-8
7514300
Proc Natl Acad Sci U S A. 2005 Sep 27;102(39):14052-7
16172381
J Cell Biol. 2004 Oct 25;167(2):209-13
15504908
Eur J Neurosci. 2001 Nov;14(9):1417-24
11722603
Eur J Neurosci. 2004 Jan;19(2):234-46
14725617
Nature. 2005 Oct 27;437(7063):1370-5
16251967
J Neurosci. 1997 Aug 1;17(15):5820-9
9221780
PLoS One. 2008 Apr 09;3(4):e1959
18509506
Proc Natl Acad Sci U S A. 2007 Mar 13;104(11):4647-52
17360578
Cell. 1999 Jun 11;97(6):703-16
10380923
Eur Arch Psychiatry Clin Neurosci. 2007 Aug;257(5):250-60
17401728
Neurobiol Aging. 2003 Mar-Apr;24(2):273-84
12498961
Science. 2003 Aug 8;301(5634):805-9
12907793
Eur J Neurosci. 2006 Mar;23(6):1539-46
16553617
Proc Natl Acad Sci U S A. 1999 May 11;96(10):5768-73
10318959
J Biol Chem. 2001 Oct 19;276(42):38349-52
11533044
Exp Neurol. 2003 Oct;183(2):298-310
14552871
J Neurochem. 2002 Feb;80(3):438-47
11908465
Rev Neurosci. 2007;18(2):93-114
17593874
Psychopharmacology (Berl). 2008 Jan;195(4):547-57
17891380
J Neurosci. 2006 Jan 4;26(1):3-11
16399667
Annu Rev Neurosci. 1999;22:105-22
10202533
Neuroscience. 2007 Jan 5;144(1):77-87
17055658
J Neurosci. 2002 Jun 1;22(11):4372-80
12040043
Hippocampus. 1996;6(4):347-470
8915675
Ann Med. 2006;38(6):439-48
17008307
Neuropharmacology. 2003 Jun;44(8):1013-21
12763094
Neuroscience. 2004;124(1):3-10
14960334
J Comp Neurol. 1985 Sep 1;239(1):117-25
4044929
Endocrinology. 1998 Jul;139(7):3112-8
9645683
Hum Mol Genet. 2000 May 22;9(9):1415-23
10814723
J Neural Transm (Vienna). 2007 Sep;114(9):1107-19
17510734
Mol Psychiatry. 2006 May;11(5):514-22
16415915
Proc Natl Acad Sci U S A. 2003 Nov 11;100(23):13632-7
14581618
Eur J Neurosci. 2004 Nov;20(10):2491-8
15548194
J Cell Biol. 2005 Jan 31;168(3):415-27
15684031
Cancer Res. 2005 May 15;65(10):3980-5
15899785
Diabetologia. 2002 May;45(5):642-50
12107744
Proc Natl Acad Sci U S A. 2003 Nov 25;100(24):14385-90
14614143
Neuroscience. 1991;42(3):777-91
1956515
Neuroscience. 2005;130(4):843-52
15652983
Hippocampus. 2006;16(3):296-304
16411241
Proc Natl Acad Sci U S A. 2001 Oct 23;98(22):12796-801
11675510
Genes Dev. 1999 Nov 15;13(22):2905-27
10579998
Neuropsychopharmacology. 2004 Mar;29(3):450-60
14872203
Eur J Neurosci. 2005 Jan;21(2):493-500
15673448
Biol Psychiatry. 2007 Sep 1;62(5):381-90
17239352
J Neurosci. 2003 Mar 1;23(5):1759-68
12629180
J Neurosci. 2003 Oct 15;23(28):9357-66
14561863
Nature. 1990 Oct 25;347(6295):768-70
1700301
J Neurosci. 2007 Dec 5;27(49):13481-90
18057206
J Neurosci. 2002 May 1;22(9):3673-82
11978843
Hippocampus. 2006;16(3):329-43
16435309
Science. 1994 May 13;264(5161):977-9
8178158
Proc Natl Acad Sci U S A. 2000 Sep 26;97(20):11032-7
11005874
J Comp Neurol. 2008 Apr 20;507(6):1860-70
18271024
Anat Rec. 1963 Apr;145:573-91
14012334
J Neurochem. 2002 Sep;82(6):1367-75
12354284