title: An update on the connections of the ventral mesencephalic dopaminergic complex.
abstract: This review covers the intrinsic organization and afferent and efferent connections of the midbrain dopaminergic complex, comprising the substantia nigra, ventral tegmental area and retrorubral field, which house, respectively, the A9, A10 and A8 groups of nigrostriatal, mesolimbic and mesocortical dopaminergic neurons. In addition, A10dc (dorsal, caudal) and A10rv (rostroventral) extensions into, respectively, the ventrolateral periaqueductal gray and supramammillary nucleus are discussed. Associated intrinsic and extrinsic connections of the midbrain dopaminergic complex that utilize gamma-aminobutyric acid (GABA), glutamate and neuropeptides and various co-expressed combinations of these compounds are considered in conjunction with the dopamine-containing systems. A framework is provided for understanding the organization of massive afferent systems descending and ascending to the midbrain dopaminergic complex from the telencephalon and brainstem, respectively. Within the context of this framework, the basal ganglia direct and indirect output pathways are treated in some detail. Findings from rodent brain are briefly compared with those from primates, including humans. Recent literature is emphasized, including traditional experimental neuroanatomical and modern gene transfer and optogenetic studies. An attempt was made to provide sufficient background and cite a representative sampling of earlier primary papers and reviews so that people new to the field may find this to be a relatively comprehensive treatment of the subject.
authors.affiliation: Department of Pharmacological and Physiological Science, Saint Louis University School of Medicine, 1402 S. Grand Boulevard, Saint Louis, MO 63104, United States. Electronic address: lyetniko@slu.edu.
authors.forename: L
authors.initials: L
authors.lastname: Yetnikoff
authors.affiliation: Department of Pharmacological and Physiological Science, Saint Louis University School of Medicine, 1402 S. Grand Boulevard, Saint Louis, MO 63104, United States.
authors.forename: H N
authors.initials: HN
authors.lastname: Lavezzi
authors.affiliation: Department of Pharmacological and Physiological Science, Saint Louis University School of Medicine, 1402 S. Grand Boulevard, Saint Louis, MO 63104, United States.
authors.forename: R A
authors.initials: RA
authors.lastname: Reichard
authors.affiliation: Department of Pharmacological and Physiological Science, Saint Louis University School of Medicine, 1402 S. Grand Boulevard, Saint Louis, MO 63104, United States. Electronic address: zahmds@slu.edu.
authors.forename: D S
authors.initials: DS
authors.lastname: Zahm
mesh_terms: D000344:Afferent Pathways / Q000033:anatomy & histology / Q000502:physiology; D000818:Animals; D059290:Dopaminergic Neurons / Q000502:physiology; D004525:Efferent Pathways / Q000033:anatomy & histology / Q000502:physiology; D006801:Humans; D013378:Substantia Nigra / Q000033:anatomy & histology / Q000502:physiology; D013681:Tegmentum Mesencephali / Q000033:anatomy & histology / Q000502:physiology
keywords: compacta; periaqueductal gray; reticulata; retrorubral field; substantia nigra; ventral tegmental area
references.citation: J Comp Neurol. 2011 Apr 15;519(6):1143-64
references.pmid: 21344406
references.citation: J Neurosci. 2008 Jun 18;28(25):6309-18
references.pmid: 18562601
references.citation: Trends Neurosci. 1991 Jan;14(1):21-7
references.pmid: 1709528
references.citation: Psychopharmacology (Berl). 2013 Mar;226(1):155-65
references.pmid: 23096770
references.citation: J Gen Physiol. 2012 Jan;139(1):93-6
references.pmid: 22200950
references.citation: J Neurosci. 1995 Nov;15(11):7181-8
references.pmid: 7472472
references.citation: Exp Brain Res. 1989;74(2):227-38
references.pmid: 2466685
references.citation: Neuron. 2012 Nov 21;76(4):826-37
references.pmid: 23177966
references.citation: J Neurosci. 2012 Dec 12;32(50):18035-46
references.pmid: 23238719
references.citation: Trends Neurosci. 1989 Oct;12(10):366-75
references.pmid: 2479133
references.citation: J Neurosci. 1990 Sep;10(9):2996-3013
references.pmid: 1975839
references.citation: Ann N Y Acad Sci. 1995 May 10;757:169-79
references.pmid: 7611672
references.citation: Neuroscience. 1992 Jul;49(2):285-96
references.pmid: 1359451
references.citation: Proc Natl Acad Sci U S A. 2006 Feb 21;103(8):2938-42
references.pmid: 16477003
references.citation: Neuroscience. 1988 Oct;27(1):1-39
references.pmid: 3059226
references.citation: Brain Behav Evol. 1978;15(3):185-234
references.pmid: 99205
references.citation: J Neurosci. 2011 Sep 14;31(37):13078-87
references.pmid: 21917791
references.citation: Eur J Neurosci. 2012 Feb;35(4):527-38
references.pmid: 22330100
references.citation: Synapse. 2007 Feb;61(2):87-95
references.pmid: 17117419
references.citation: J Comp Neurol. 2001 Mar 26;432(1):119-36
references.pmid: 11241381
references.citation: J Neurosci. 2011 May 4;31(18):6891-9
references.pmid: 21543619
references.citation: Neuropsychopharmacology. 2010 Jan;35(1):4-26
references.pmid: 19812543
references.citation: Front Hum Neurosci. 2013 Dec 09;7:854
references.pmid: 24367324
references.citation: Brain Nerve. 2009 Apr;61(4):360-72
references.pmid: 19378805
references.citation: J Comp Neurol. 1989 Dec 8;290(2):213-42
references.pmid: 2592611
references.citation: J Comp Neurol. 1966 Mar;126(3):311-35
references.pmid: 4957032
references.citation: Neuron. 2009 Mar 12;61(5):786-800
references.pmid: 19285474
references.citation: Brain Res. 1995 Dec 24;705(1-2):273-94
references.pmid: 8821759
references.citation: J Comp Neurol. 1995 Nov 20;362(3):400-10
references.pmid: 8576447
references.citation: Brain Res. 1989 Sep 4;496(1-2):373-6
references.pmid: 2804651
references.citation: Am J Anat. 1981 Jul;161(3):323-40
references.pmid: 6168196
references.citation: J Comp Neurol. 2001 Aug 6;436(4):430-55
references.pmid: 11447588
references.citation: Nat Neurosci. 2013 May;16(5):632-8
references.pmid: 23542690
references.citation: Proc Natl Acad Sci U S A. 2006 Mar 28;103(13):5167-72
references.pmid: 16549786
references.citation: Neuroscience. 1995 Feb;64(4):1019-34
references.pmid: 7753373
references.citation: Neuroscience. 1980;5(12):2093-124
references.pmid: 7007911
references.citation: Ann N Y Acad Sci. 1988;537:27-50
references.pmid: 2462395
references.citation: CNS Neurol Disord Drug Targets. 2006 Feb;5(1):79-97
references.pmid: 16613555
references.citation: Prog Brain Res. 1996;107:243-55
references.pmid: 8782523
references.citation: J Comp Neurol. 1989 Jan 8;279(2):249-71
references.pmid: 2563268
references.citation: J Neurosci. 2004 Mar 10;24(10):2566-74
references.pmid: 15014132
references.citation: Brain Res Brain Res Rev. 2005 Dec 15;50(2):336-60
references.pmid: 16278019
references.citation: Nature. 1980 Jun 12;285(5765):476-8
references.pmid: 6105617
references.citation: J Comp Neurol. 1984 Feb 1;222(4):543-59
references.pmid: 6365985
references.citation: Nature. 2010 Jul 29;466(7306):622-6
references.pmid: 20613723
references.citation: J Neurosci. 1997 Aug 1;17(15):5738-46
references.pmid: 9221772
references.citation: J Neurosci. 2006 Mar 8;26(10):2788-97
references.pmid: 16525058
references.citation: Annu Rev Neurosci. 2011;34:441-66
references.pmid: 21469956
references.citation: J Comp Neurol. 1979 Sep 1;187(1):85-98
references.pmid: 489779
references.citation: Synapse. 2006 Jul;60(1):20-31
references.pmid: 16575850
references.citation: J Comp Neurol. 2009 Apr 20;513(6):597-621
references.pmid: 19235223
references.citation: J Comp Neurol. 1992 Dec 22;326(4):595-622
references.pmid: 1484125
references.citation: Neuron. 2012 Jun 7;74(5):858-73
references.pmid: 22681690
references.citation: Nature. 2012 Dec 20;492(7429):452-6
references.pmid: 23178810
references.citation: Nature. 2012 Jan 18;482(7383):85-8
references.pmid: 22258508
references.citation: J Neurosci. 1987 Jan;7(1):279-90
references.pmid: 2879896
references.citation: Adv Neurol. 1990;53:17-29
references.pmid: 1978514
references.citation: J Chem Neuroanat. 2009 Dec;38(4):273-81
references.pmid: 19467322
references.citation: Prog Brain Res. 1991;87:81-99
references.pmid: 1678193
references.citation: J Neurosci. 2005 Jun 29;25(26):6076-83
references.pmid: 15987937
references.citation: Physiol Behav. 2010 Jul 14;100(5):419-28
references.pmid: 20338186
references.citation: J Comp Neurol. 1993 Jul 1;333(1):118-33
references.pmid: 8101849
references.citation: Brain Res. 1990 Mar 12;511(1):173-6
references.pmid: 1970510
references.citation: Neuroscience. 2011 Dec 15;198:112-37
references.pmid: 21939738
references.citation: J Neurosci Res. 2010 Apr;88(5):981-91
references.pmid: 19885830
references.citation: Neuropsychopharmacology. 2013 Apr;38(5):715-28
references.pmid: 23303055
references.citation: J Neurosci. 2012 Oct 24;32(43):15076-85
references.pmid: 23100428
references.citation: J Neurophysiol. 1998 Jul;80(1):1-27
references.pmid: 9658025
references.citation: J Neurosci. 1998 Oct 1;18(19):8003-15
references.pmid: 9742167
references.citation: Neuroscience. 2008 Apr 9;152(4):1024-31
references.pmid: 18355970
references.citation: Proc Natl Acad Sci U S A. 1985 Dec;82(24):8780-4
references.pmid: 3909155
references.citation: Neuroscience. 1984 Feb;11(2):425-35
references.pmid: 6201780
references.citation: J Comp Neurol. 1994 Jul 22;345(4):562-78
references.pmid: 7962700
references.citation: J Comp Neurol. 2003 Oct 6;465(1):1-10
references.pmid: 12926012
references.citation: Nature. 2005 Feb 24;433(7028):873-6
references.pmid: 15729344
references.citation: Neuron. 2013 Sep 4;79(5):1011-24
references.pmid: 23932490
references.citation: Brain Res Rev. 2008 Aug;58(2):322-39
references.pmid: 18055018
references.citation: J Comp Neurol. 1993 Apr 15;330(3):381-404
references.pmid: 8385679
references.citation: Nat Neurosci. 2012 Feb 12;15(4):613-9
references.pmid: 22327472
references.citation: J Comp Neurol. 1984 Jul 20;227(1):92-103
references.pmid: 6147361
references.citation: Histol Histopathol. 1987 Jul;2(3):251-63
references.pmid: 2908792
references.citation: Eur J Neurosci. 2008 Nov;28(10):2028-40
references.pmid: 19046384
references.citation: Brain Res. 1988 Sep 27;461(1):127-42
references.pmid: 3224272
references.citation: Synapse. 1998 Aug;29(4):363-70
references.pmid: 9661254
references.citation: J Comp Neurol. 2006 Feb 20;494(6):863-75
references.pmid: 16385486
references.citation: Neuron. 2011 Jun 9;70(5):855-62
references.pmid: 21658580
references.citation: Prog Neurobiol. 1995 Jun;46(2-3):131-97
references.pmid: 7568912
references.citation: Mo Med. 2010 Jul-Aug;107(4):276-80
references.pmid: 20806841
references.citation: J Neurosci. 2013 Apr 24;33(17):7583-94
references.pmid: 23616563
references.citation: J Neurophysiol. 2013 Nov;110(10):2287-94
references.pmid: 24004527
references.citation: Neuroscience. 1992;46(3):711-20
references.pmid: 1372117
references.citation: Synapse. 2009 Oct;63(10):895-906
references.pmid: 19582784
references.citation: J Neurosci. 2008 Sep 3;28(36):8908-13
references.pmid: 18768684
references.citation: Neuropeptides. 1988 Apr;11(3):95-100
references.pmid: 3133572
references.citation: F1000 Biol Rep. 2010 Jan 18;2:
references.pmid: 20948813
references.citation: J Neurochem. 2004 Mar;88(6):1398-405
references.pmid: 15009640
references.citation: Life Sci. 1965 Jul;4(13):1275-9
references.pmid: 5849269
references.citation: J Neurosci. 2000 May 15;20(10):3864-73
references.pmid: 10804226
references.citation: J Neurosci. 2013 Jul 10;33(28):11668-76
references.pmid: 23843534
references.citation: Ann N Y Acad Sci. 1988;537:415-34
references.pmid: 2462397
references.citation: J Neurosci. 1995 Apr;15(4):3092-103
references.pmid: 7722648
references.citation: Eur J Neurosci. 2006 Jul;24(1):116-34
references.pmid: 16882012
references.citation: J Neurosci. 2011 Aug 10;31(32):11457-71
references.pmid: 21832176
references.citation: J Neurosci. 1984 Jun;4(6):1626-38
references.pmid: 6374062
references.citation: Brain Res. 1997 Jan 30;747(1):173-9
references.pmid: 9042545
references.citation: J Comp Neurol. 2002 Dec 2;454(1):15-33
references.pmid: 12410615
references.citation: J Neurosci. 2011 May 25;31(21):7811-6
references.pmid: 21613494
references.citation: J Comp Neurol. 1989 Jan 15;279(3):415-35
references.pmid: 2918078
references.citation: Neuroscience. 2007 Mar 30;145(3):1059-76
references.pmid: 17270353
references.citation: Neurosci Res. 2002 Jun;43(2):111-7
references.pmid: 12067746
references.citation: Neurosci Biobehav Rev. 2006;30(2):126-47
references.pmid: 16183121
references.citation: Exp Brain Res. 1994;100(3):395-406
references.pmid: 7813678
references.citation: J Comp Neurol. 1961 Feb;116:27-69
references.pmid: 13774738
references.citation: Brain Res. 1987 Dec 1;435(1-2):71-83
references.pmid: 2892580
references.citation: Brain Res. 1983 Mar 7;262(2):334-8
references.pmid: 6839161
references.citation: Neuroscience. 1998 Sep;86(2):353-87
references.pmid: 9881853
references.citation: Neurosci Lett. 1991 Dec 16;134(1):62-6
references.pmid: 1687702
references.citation: Nat Rev Neurosci. 2004 Jun;5(6):483-94
references.pmid: 15152198
references.citation: Neuroscience. 1984 Dec;13(4):1189-215
references.pmid: 6152036
references.citation: Neuropsychopharmacology. 2006 Jul;31(7):1356-61
references.pmid: 16319915
references.citation: Peptides. 1985;6 Suppl 2:113-22
references.pmid: 2417207
references.citation: Neuron. 2013 Nov 20;80(4):1039-53
references.pmid: 24267654
references.citation: Nature. 1976 Mar 18;260(5548):258-60
references.pmid: 1256567
references.citation: Eur J Neurosci. 2009 Oct;30(7):1239-50
references.pmid: 19788571
references.citation: Neuroscience. 1994 Apr;59(3):609-23
references.pmid: 7516505
references.citation: J Comp Neurol. 1996 Jan 08;364(2):254-66
references.pmid: 8788248
references.citation: Acta Physiol Scand. 1966 Jul-Aug;67(3):306-12
references.pmid: 5967596
references.citation: Nat Neurosci. 2012 Jun;15(6):816-8
references.pmid: 22544310
references.citation: Adv Neurol. 1997;74:83-96
references.pmid: 9348404
references.citation: J Neurosci. 1995 Sep;15(9):5859-69
references.pmid: 7666171
references.citation: Neurosci Lett. 1989 May 22;100(1-3):215-20
references.pmid: 2761771
references.citation: Neuroscience. 1989;30(2):405-21
references.pmid: 2568603
references.citation: Cereb Cortex. 1993 May-Jun;3(3):199-222
references.pmid: 8100725
references.citation: J Comp Neurol. 2004 Feb 16;469(4):581-607
references.pmid: 14755537
references.citation: Cell Metab. 2009 Aug;10(2):89-98
references.pmid: 19656487
references.citation: Exp Brain Res. 1987;68(2):277-89
references.pmid: 3319664
references.citation: Neuropsychopharmacology. 2013 Apr;38(5):701-14
references.pmid: 23232445
references.citation: Brain Res Rev. 2008 Aug;58(2):265-71
references.pmid: 18343506
references.citation: Nat Neurosci. 2011 Jan;14(1):22-4
references.pmid: 21131952
references.citation: Nature. 2001 Jul 5;412(6842):79-83
references.pmid: 11452310
references.citation: J Neurosci. 1999 Jun 1;19(11):4682-94
references.pmid: 10341266
references.citation: Brain Res Brain Res Rev. 1998 Dec;28(3):309-69
references.pmid: 9858756
references.citation: Arch Neurol. 1986 Oct;43(10):1074-8
references.pmid: 3753266
references.citation: Cell Tissue Res. 1978 Jul 10;190(3):383-407
references.pmid: 688339
references.citation: Neuron. 2012 Mar 22;73(6):1184-94
references.pmid: 22445345
references.citation: Neurosci Lett. 1980 Jun;18(2):125-31
references.pmid: 7052484
references.citation: Annu Rev Neurosci. 1992;15:285-320
references.pmid: 1575444
references.citation: J Comp Neurol. 1989 Nov 8;289(2):189-201
references.pmid: 2478598
references.citation: Brain Behav Evol. 1972;6(1):484-523
references.pmid: 4662205
references.citation: J Comp Neurol. 1989 Nov 1;289(1):36-52
references.pmid: 2572613
references.citation: Eur J Neurosci. 2006 Jul;24(1):188-96
references.pmid: 16882016
references.citation: Crit Rev Neurobiol. 1997;11(4):241-61
references.pmid: 9336713
references.citation: Brain Res. 1975 Feb 28;85(2):295-300
references.pmid: 234280
references.citation: Peptides. 2006 Oct;27(10):2364-84
references.pmid: 16934369
references.citation: J Neurosci. 2011 Aug 31;31(35):12593-603
references.pmid: 21880920
references.citation: Eur J Pharmacol. 1992 Feb 18;211(3):295-303
references.pmid: 1319909
references.citation: Neuropsychopharmacology. 2014 Jan;39(2):254-62
references.pmid: 24121188
references.citation: Nature. 1984 Oct 4-10;311(5985):461-4
references.pmid: 6207434
references.citation: Nature. 2013 Apr 11;496(7444):224-8
references.pmid: 23515155
references.citation: Mol Neurobiol. 2004 Jun;29(3):243-59
references.pmid: 15181237
references.citation: Brain Res. 1985 May 6;333(2):271-84
references.pmid: 2986775
references.citation: Neuroscience. 2001;104(3):807-27
references.pmid: 11440812
references.citation: Science. 2013 Sep 27;341(6153):1521-5
references.pmid: 24072923
references.citation: J Neurosci. 2004 Sep 22;24(38):8198-204
references.pmid: 15385602
references.citation: Neuropsychopharmacology. 2008 Nov;33(12):3010-20
references.pmid: 18256592
references.citation: Brain Res. 1995 Jun 5;682(1-2):215-21
references.pmid: 7552315
references.citation: J Comp Neurol. 1984 May 10;225(2):212-27
references.pmid: 6202728
references.citation: Neuroscience. 1995 Apr;65(3):709-30
references.pmid: 7609871
references.citation: Synapse. 2011 Aug;65(8):695-707
references.pmid: 21638336
references.citation: Acta Physiol Scand Suppl. 1964;:SUPPL 232:1-55
references.pmid: 14229500
references.citation: Neuroscience. 2000;96(3):451-74
references.pmid: 10717427
references.citation: Neuroscience. 2008 Jul 31;155(1):203-20
references.pmid: 18562124
references.citation: J Comp Neurol. 1978 Aug 1;180(3):545-80
references.pmid: 659674
references.citation: Neuron. 2012 Mar 8;73(5):978-89
references.pmid: 22405207
references.citation: J Neurosci. 1981 Nov;1(11):1242-59
references.pmid: 6171630
references.citation: Neuroimage. 2007 Feb 1;34(3):965-84
references.pmid: 17140815
references.citation: Adv Anat Embryol Cell Biol. 1991;121:1-132
references.pmid: 2053466
references.citation: Neuroscience. 2010 Jun 16;168(1):263-72
references.pmid: 20363297
references.citation: J Comp Neurol. 1979 Sep 1;187(1):117-43
references.pmid: 489776
references.citation: Neuropsychopharmacology. 2010 Jan;35(1):27-47
references.pmid: 19675534
references.citation: Brain Res Rev. 2008 Aug;58(2):290-302
references.pmid: 18042492
references.citation: Eur J Neurosci. 2009 Jan;29(2):340-58
references.pmid: 19200238
references.citation: J Neurosci. 1983 Feb;3(2):383-8
references.pmid: 6822869
references.citation: J Neurosci. 1981 Dec;1(12):1361-8
references.pmid: 6172572
references.citation: J Neurosci. 2013 Nov 20;33(47):18531-9
references.pmid: 24259575
references.citation: Neuroscience. 2007 May 25;146(3):1259-74
references.pmid: 17391856
references.citation: J Comp Neurol. 1978 Mar 15;178(2):225-54
references.pmid: 627625
references.citation: Neuroscience. 1989;29(3):503-37
references.pmid: 2472578
references.citation: J Chem Neuroanat. 2003 Dec;26(4):317-30
references.pmid: 14729134
references.citation: J Comp Neurol. 2006 Oct 10;498(5):581-92
references.pmid: 16917821
references.citation: Brain Res Brain Res Rev. 2002 Sep;39(2-3):107-40
references.pmid: 12423763
references.citation: Neuroscience. 1998 Feb;82(3):767-80
references.pmid: 9483534
references.citation: Neurosci Biobehav Rev. 2006;30(2):148-72
references.pmid: 16125239
references.citation: Neuron. 2010 Jun 24;66(6):896-907
references.pmid: 20620875
references.citation: Brain Res. 1992 Mar 20;575(2):341-6
references.pmid: 1349255
references.citation: Neuropharmacology. 2014 Jan;76 Pt B:351-9
references.pmid: 23578393
references.citation: J Comp Neurol. 1990 Dec 15;302(3):437-46
references.pmid: 1702109
references.citation: Neuroscience. 2000;97(3):479-94
references.pmid: 10828531
references.citation: Nat Neurosci. 2003 Sep;6(9):974-80
references.pmid: 12925855
references.citation: J Comp Neurol. 2001 Oct 8;439(1):104-26
references.pmid: 11584811
references.citation: Brain Res. 1988 Jul 5;455(1):88-98
references.pmid: 3046712
references.citation: Front Comput Neurosci. 2013 Oct 10;7:135
references.pmid: 24133443
references.citation: N Engl J Med. 1998 Oct 8;339(15):1044-53
references.pmid: 9761807
references.citation: Neuroscience. 1999;91(3):891-909
references.pmid: 10391469
references.citation: J Neurosci. 2009 Mar 18;29(11):3613-26
references.pmid: 19295165
references.citation: Neuropsychopharmacology. 2010 Jan;35(1):48-69
references.pmid: 19776734
references.citation: Cereb Cortex. 2012 Feb;22(2):327-36
references.pmid: 21666135
references.citation: Brain Res Bull. 1982 Jul-Dec;9(1-6):321-53
references.pmid: 6816390
references.citation: J Clin Invest. 2006 Dec;116(12):3229-39
references.pmid: 17060947
references.citation: Proc Natl Acad Sci U S A. 2002 Oct 29;99(22):14488-93
references.pmid: 12388773
references.citation: J Comp Neurol. 1975 Aug 15;162(4):487-504
references.pmid: 50334
references.citation: Neuron. 2012 Mar 22;73(6):1173-83
references.pmid: 22445344
references.citation: Neuropsychopharmacology. 2008 Oct;33(11):2688-700
references.pmid: 18094667
references.citation: Neuron. 2008 Nov 26;60(4):720-9
references.pmid: 19038227
references.citation: J Comp Neurol. 2009 Apr 20;513(6):566-96
references.pmid: 19235216
references.citation: J Neurosci. 2002 Jul 1;22(13):5442-51
references.pmid: 12097496
references.citation: J Neurosci. 2007 May 23;27(21):5730-43
references.pmid: 17522317
references.citation: Eur J Neurosci. 2007 Jan;25(1):106-18
references.pmid: 17241272
references.citation: Prog Brain Res. 1996;107:225-42
references.pmid: 8782522
references.citation: J Comp Neurol. 1990 Jul 8;297(2):182-200
references.pmid: 2370319
references.citation: Basal Ganglia. 2011 Nov;1(4):191-200
references.pmid: 22163100
references.citation: Biol Psychiatry. 2012 Sep 1;72(5):343-5
references.pmid: 22872011
references.citation: Neuroscience. 2001;104(3):841-51
references.pmid: 11440814
references.citation: Prog Neuropsychopharmacol Biol Psychiatry. 1997 Jan;21(1):1-22
references.pmid: 9075256
references.citation: J Neurochem. 1991 Mar;56(3):961-7
references.pmid: 1993900
references.citation: J Neurosci. 1990 Dec;10(12):3889-95
references.pmid: 1980132
references.citation: Acta Physiol Scand Suppl. 1971;367:1-48
references.pmid: 4109331
references.citation: Neuroscience. 2009 Dec 15;164(3):1068-83
references.pmid: 19729052
references.citation: Neuroscience. 1996 Nov;75(1):5-12
references.pmid: 8923517
references.citation: J Neurosci. 2011 Jan 26;31(4):1183-92
references.pmid: 21273403
references.citation: Brain Res. 1975 Sep 5;94(3):507-22
references.pmid: 1171714
references.citation: Neuron. 2012 May 10;74(3):475-81
references.pmid: 22578499
references.citation: J Comp Neurol. 1990 Dec 8;302(2):305-21
references.pmid: 1981215
references.citation: Neuroscience. 1989;32(2):297-321
references.pmid: 2479881
references.citation: Prog Neurobiol. 1980;14(2-3):69-97
references.pmid: 6999537
references.citation: J Neurosci. 2005 Jan 12;25(2):291-8
references.pmid: 15647472
references.citation: J Comp Neurol. 1996 Oct 28;374(4):555-77
references.pmid: 8910735
references.citation: J Comp Neurol. 2005 Dec 5;493(1):111-4
references.pmid: 16254996
references.citation: Neuroscience. 2005;135(3):915-25
references.pmid: 16154276
references.citation: Front Hum Neurosci. 2013 Nov 13;7:778
references.pmid: 24294200
references.citation: Brain Res Bull. 1988 Mar;20(3):307-14
references.pmid: 2896530
references.citation: Neuropharmacology. 2009;56 Suppl 1:112-21
references.pmid: 18655797
references.citation: N Engl J Med. 1998 Oct 15;339(16):1130-43
references.pmid: 9770561
references.citation: Brain Res. 1987 May;434(2):117-65
references.pmid: 3107759
references.citation: Neuropharmacology. 2012 Nov;63(6):983-91
references.pmid: 22884466
references.citation: J Comp Neurol. 1998 Nov 2;400(4):487-503
references.pmid: 9786410
references.citation: J Neurosci. 2002 Feb 1;22(3):1137-45
references.pmid: 11826142
references.citation: Neuron. 2006 Sep 21;51(6):811-22
references.pmid: 16982425
references.citation: J Neural Transm Suppl. 2009;(73):49-58
references.pmid: 20411767
references.citation: Brain Res. 1993 Feb 5;602(2):275-89
references.pmid: 8095430
references.citation: Ann N Y Acad Sci. 1999 Jun 29;877:676-8
references.pmid: 10415681
references.citation: J Neurosci. 2013 May 1;33(18):7618-26
references.pmid: 23637156
references.citation: Neurosci Lett. 1989 Feb 27;97(3):252-8
references.pmid: 2717061
references.citation: J Comp Neurol. 2006 Sep 1;498(1):93-111
references.pmid: 16933208
references.citation: J Comp Neurol. 2013 Jan 1;521(1):50-68
references.pmid: 22628122
references.citation: J Comp Neurol. 1984 Mar 20;224(1):1-24
references.pmid: 6715573
references.citation: Neuroscience. 1991;41(1):89-125
references.pmid: 2057066
references.citation: Brain Res. 2000 Dec 15;886(1-2):113-164
references.pmid: 11119693
references.citation: J Neurosci. 2000 Mar 15;20(6):2369-82
references.pmid: 10704511
references.citation: Neurosci Lett. 1978 Feb;7(2-3):157-62
references.pmid: 19605105
references.citation: Cereb Cortex. 2009 Feb;19(2):424-34
references.pmid: 18550594
references.citation: Exp Brain Res. 1998 Nov;123(1-2):60-76
references.pmid: 9835393
references.citation: J Neurosci. 2011 Feb 16;31(7):2481-7
references.pmid: 21325515
references.citation: J Comp Neurol. 1977 May 1;173(1):147-64
references.pmid: 403205
references.citation: J Comp Neurol. 2014 Apr 1;522(5):1031-47
references.pmid: 23983069
references.citation: J Chem Neuroanat. 1998 Aug;15(2):111-27
references.pmid: 9719363
references.citation: Neuroscience. 1989;32(1):213-26
references.pmid: 2586750
references.citation: J Comp Neurol. 1991 Nov 22;313(4):643-68
references.pmid: 1783685
references.citation: Brain Res Rev. 2007 Nov;56(1):27-78
references.pmid: 17574681
references.citation: Proc Natl Acad Sci U S A. 2013 Oct 8;110(41):16287
references.pmid: 24106299
references.citation: J Pharmacol Exp Ther. 1996 Jul;278(1):384-92
references.pmid: 8764374
references.citation: J Neurosci. 1987 Dec;7(12):3915-34
references.pmid: 2891799
references.citation: J Neurosci. 2005 Apr 13;25(15):3881-8
references.pmid: 15829640
references.citation: Mov Disord. 2008;23 Suppl 3:S534-47
references.pmid: 18781680
references.citation: J Neurosci. 2009 Jan 14;29(2):444-53
references.pmid: 19144844
references.citation: Prog Neurobiol. 1996 Nov;50(4):381-425
references.pmid: 9004351
references.citation: Neuroscience. 1987 Jun;21(3):807-24
references.pmid: 3627435
references.citation: Eur J Neurosci. 2013 Sep;38(5):2774-85
references.pmid: 23773170
references.citation: Brain Res. 1977 Dec 16;138(2):271-83
references.pmid: 589476
references.citation: J Comp Neurol. 2005 Aug 29;489(3):349-71
references.pmid: 16025448
references.citation: Brain Res. 1984 May 21;300(1):157-60
references.pmid: 6733462
references.citation: J Neurosci. 2011 Nov 30;31(48):17729-35
references.pmid: 22131433
references.citation: Neuroscience. 1984 May;12(1):165-78
references.pmid: 6087196
references.citation: J Comp Neurol. 2007 Aug 10;503(5):668-84
references.pmid: 17559101
references.citation: Brain Res. 1999 Oct 9;844(1-2):67-77
references.pmid: 10536262
references.citation: Neuroscience. 2006;138(1):221-34
references.pmid: 16361067
references.citation: J Neurosci. 2010 Jan 6;30(1):218-29
references.pmid: 20053904
references.citation: Brain Res. 1992 Aug 7;587(2):203-10
references.pmid: 1356063
references.citation: Eur J Neurosci. 2007 Mar;25(5):1557-67
references.pmid: 17425582
references.citation: Psychopharmacology (Berl). 2013 Jun;227(4):697-709
references.pmid: 23392354
references.citation: Brain Res. 1991 Apr 26;547(1):37-52
references.pmid: 1907216
references.citation: Science. 1975 Feb 14;187(4176):547-9
references.pmid: 1114313
references.citation: Neuroscience. 1987 Oct;23(1):223-42
references.pmid: 3683862
references.citation: Brain Res. 2013 Jul 19;1522:38-58
references.pmid: 23665053
references.citation: Neuroscience. 2011 Dec 15;198:95-111
references.pmid: 21872647
references.citation: Brain Res. 1981 Aug;228(1):1-34
references.pmid: 7023613
references.citation: Neurosci Lett. 1984 Jul 27;48(2):121-5
references.pmid: 6090994
references.citation: J Neurosci. 2001 Aug 15;21(16):RC160
references.pmid: 11473131
references.citation: Crit Rev Neurobiol. 1997;11(4):323-42
references.pmid: 9336716
references.citation: Neuroscience. 1989;30(1):33-50
references.pmid: 2473414
references.citation: Neuroscience. 1996 Aug;73(3):761-81
references.pmid: 8809796
references.citation: Trends Neurosci. 2012 Nov;35(11):681-90
references.pmid: 22824232
references.citation: Ciba Found Symp. 1984;107:3-29
references.pmid: 6437774
references.citation: Trends Neurosci. 1994 Feb;17(2):52-7
references.pmid: 7512768
references.citation: Brain Res Bull. 1982 Jul-Dec;9(1-6):295-307
references.pmid: 6129040
references.citation: Psychopharmacology (Berl). 1995 Aug;120(4):433-41
references.pmid: 8539324
references.citation: Hippocampus. 1994 Jun;4(3):354-73
references.pmid: 7842057
references.citation: Neuropharmacology. 2014 Jan;76 Pt B:329-41
references.pmid: 23664810
references.citation: Exp Brain Res. 1994;99(1):34-42
references.pmid: 7925794
references.citation: Synapse. 2000 Nov;38(2):114-23
references.pmid: 11018785
references.citation: J Comp Neurol. 1990 Apr 15;294(3):356-61
references.pmid: 2341615
references.citation: Nature. 2012 Oct 11;490(7419):262-6
references.pmid: 23034651
references.citation: Int Rev Neurobiol. 2007;78:41-68
references.pmid: 17349857
references.citation: J Neurosci. 1994 Jan;14(1):88-106
references.pmid: 7904306
references.citation: Neurosci Biobehav Rev. 1985 Winter;9(4):573-87
references.pmid: 2417173
references.citation: Neuroscience. 1985 Apr;14(4):1039-52
references.pmid: 2860616
references.citation: J Neurophysiol. 1997 Feb;77(2):853-62
references.pmid: 9065854
references.citation: Brain Res Bull. 1996;40(3):219-28
references.pmid: 8736584
references.citation: Neuropsychopharmacology. 2013 Apr;38(5):854-62
references.pmid: 23303063
references.citation: J Neurosci. 1995 Nov;15(11):7189-95
references.pmid: 7472473
references.citation: Nat Neurosci. 2005 Nov;8(11):1481-9
references.pmid: 16251991
references.citation: J Neurosci. 2010 Jun 16;30(24):8229-33
references.pmid: 20554874
references.citation: Nature. 2009 Jun 11;459(7248):837-41
references.pmid: 19448610
references.citation: Trends Neurosci. 2007 May;30(5):194-202
references.pmid: 17408759
references.citation: Prog Neurobiol. 1996 Aug;49(5):415-54
references.pmid: 8895995
references.citation: Brain Res. 2002 Dec 13;957(2):207-22
references.pmid: 12445963
references.citation: J Comp Neurol. 2010 Mar 1;518(5):668-86
references.pmid: 20034056
references.citation: Nat Neurosci. 1998 Aug;1(4):304-9
references.pmid: 10195164
references.citation: J Comp Neurol. 2004 Feb 2;469(2):170-84
references.pmid: 14694532
references.citation: Neuroscience. 2011 Oct 13;193:229-40
references.pmid: 21784133
references.citation: Neurochem Int. 1998 Nov;33(5):383-97
references.pmid: 9874089
references.citation: J Comp Neurol. 1988 Jan 15;267(3):433-53
references.pmid: 2449477
references.citation: J Neurosci. 2002 Jun 15;22(12):5173-87
references.pmid: 12077212
references.citation: Neuroscience. 2002;111(2):379-87
references.pmid: 11983323
references.citation: Ann N Y Acad Sci. 1988;537:1-9
references.pmid: 3059916
references.citation: Braz J Med Biol Res. 2003 May;36(5):557-66
references.pmid: 12715074
references.citation: Eur J Neurosci. 2000 Dec;12(12):4578-82
references.pmid: 11122372
references.citation: Eur J Neurosci. 2005 May;21(10):2817-24
references.pmid: 15926929
references.citation: Brain Res. 1986 Aug 20;380(2):331-5
references.pmid: 3756484
references.citation: Neuron. 2013 Jul 24;79(2):347-60
references.pmid: 23810541
references.citation: J Comp Neurol. 2008 Apr 1;507(4):1465-78
references.pmid: 18203181
references.citation: Neuron. 2010 Mar 11;65(5):643-56
references.pmid: 20223200
references.citation: Parkinsonism Relat Disord. 1999 Dec;5(4):193-201
references.pmid: 18591140
references.citation: Exp Physiol. 2002 Mar;87(2):251-8
references.pmid: 11856971
references.citation: J Comp Neurol. 1993 Mar 1;329(1):111-28
references.pmid: 8454722
references.citation: Life Sci (1962). 1964 Jun;3:523-30
references.pmid: 14187491
references.citation: Neurosci Lett. 2007 Nov 12;427(3):165-70
references.pmid: 17949902
references.citation: Trends Neurosci. 2013 Jun;36(6):336-42
references.pmid: 23582338
references.citation: J Comp Neurol. 1986 Jul 22;249(4):511-20, 484-5
references.pmid: 2427554
references.citation: Annu Rev Neurosci. 1978;1:129-69
references.pmid: 756202
references.citation: Front Mol Neurosci. 2013 Jul 17;6:18
references.pmid: 23882179
references.citation: Brain Res. 1990 Jul 23;523(2):288-90
references.pmid: 2144781
references.citation: Nat Neurosci. 2012 Dec;15(12):1624-6
references.pmid: 23143514
references.citation: J Comp Neurol. 2010 May 1;518(9):1460-99
references.pmid: 20187136
references.citation: Neuroscience. 1978;3(4-5):385-401
references.pmid: 683502
references.citation: Neuroscience. 2008 Apr 22;153(1):196-213
references.pmid: 18358616
references.citation: Nature. 2013 Apr 11;496(7444):219-23
references.pmid: 23515158
references.citation: Brain Res. 1979 Oct 19;175(2):191-217
references.pmid: 314832
references.citation: Neuroscience. 1999;94(4):1097-123
references.pmid: 10625051
references.citation: World J Biol Psychiatry. 2011 Sep;12 Suppl 1:19-22
references.pmid: 21905990
references.citation: J Neurosci. 2004 Jan 28;24(4):972-81
references.pmid: 14749442
references.citation: Neuron. 2001 Aug 2;31(2):247-60
references.pmid: 11502256
references.citation: Eur J Neurosci. 2013 Dec;38(11):3602-10
references.pmid: 24102658
references.citation: Trends Neurosci. 2004 Feb;27(2):98-103
references.pmid: 15102489
references.citation: J Comp Neurol. 2005 Mar 7;483(2):217-35
references.pmid: 15678476
references.citation: Neuroscience. 1988 Feb;24(2):379-431
references.pmid: 2452377
references.citation: J Comp Neurol. 1983 Aug 1;218(2):220-38
references.pmid: 6886073
references.citation: Biol Psychiatry. 1999 Jul 1;46(1):40-55
references.pmid: 10394473
references.citation: J Neurosci. 1997 May 15;17(10):3913-9
references.pmid: 9133409
references.citation: Brain Res. 1990 Sep 17;527(2):266-79
references.pmid: 1701338
references.citation: J Comp Neurol. 2005 Sep 26;490(3):270-94
references.pmid: 16082674
references.citation: Neuroscience. 1983 Oct;10(2):333-48
references.pmid: 6633865
references.citation: Eur J Neurosci. 2003 Jan;17(1):28-40
references.pmid: 12534966
references.citation: Nat Neurosci. 2012 Sep;15(9):1281-9
references.pmid: 22902719
references.citation: Science. 1997 Mar 14;275(5306):1593-9
references.pmid: 9054347
references.citation: J Comp Neurol. 2011 Nov 1;519(16):3159-88
references.pmid: 21618227
references.citation: Ann N Y Acad Sci. 1999 Jun 29;877:1-32
references.pmid: 10415640
references.citation: J Comp Neurol. 1993 Jan 8;327(2):220-32
references.pmid: 8425943
references.citation: Rev Neurosci. 2013;24(4):389-400
references.pmid: 23843581
references.citation: Brain Res Bull. 1994;33(4):445-52
references.pmid: 8124582
references.citation: Nature. 1996 Feb 1;379(6564):449-51
references.pmid: 8559249
references.citation: Exp Brain Res. 1987;66(1):191-210
references.pmid: 2884126
references.citation: J Neurosci. 2012 Nov 28;32(48):17477-91
references.pmid: 23197738
references.citation: J Comp Neurol. 1984 Mar 1;223(3):347-67
references.pmid: 6323552
references.citation: Nature. 2012 Nov 8;491(7423):212-7
references.pmid: 23064228
references.citation: J Neurosci. 1987 Sep;7(9):2927-35
references.pmid: 3114439
references.citation: Neuroscience. 2000;99(3):445-56
references.pmid: 11029537
references.citation: Neuron. 2008 Mar 13;57(5):760-73
references.pmid: 18341995
references.citation: J Neurol Neurosurg Psychiatry. 1990 Jun;53(6):492-5
references.pmid: 2380730
references.citation: Adv Pharmacol. 1998;42:703-6
references.pmid: 9327996
references.citation: PLoS One. 2012;7(7):e42365
references.pmid: 22860119
references.citation: Brain Res. 1984 Jul 30;307(1-2):99-108
references.pmid: 6087992
references.citation: Neuroscience. 1992 Dec;51(3):691-703
references.pmid: 1283209
references.citation: Eur J Pharmacol. 1979 Nov 16;59(3-4):211-8
references.pmid: 527646
references.citation: Brain Res Bull. 1992 Mar;28(3):447-54
references.pmid: 1591601
references.citation: J Neurosci. 2010 May 19;30(20):7105-10
references.pmid: 20484653
references.citation: Neuroscience. 1993 Nov;57(1):113-42
references.pmid: 8278047
references.citation: Nat Neurosci. 2003 Sep;6(9):968-73
references.pmid: 12897785
references.citation: Trends Pharmacol Sci. 1991 Jun;12(6):232-6
references.pmid: 2048219
references.citation: J Comp Neurol. 1990 Jun 1;296(1):47-64
references.pmid: 1694189
references.citation: J Physiol. 1987 Nov;392:397-416
references.pmid: 2451725
references.citation: Brain Res. 1995 Aug 14;689(1):151-6
references.pmid: 8528700
references.citation: J Neurosci. 1998 Jun 15;18(12):4588-602
references.pmid: 9614234
references.citation: Physiol Behav. 2002 Dec;77(4-5):513-7
references.pmid: 12526992
references.citation: Behav Neurosci. 1991 Dec;105(6):817-25
references.pmid: 1777104
references.citation: Annu Rev Neurosci. 2007;30:289-316
references.pmid: 17376009
references.citation: J Neurosci. 2011 Jun 8;31(23):8476-90
references.pmid: 21653852
references.citation: Neuron. 2006 Sep 21;51(6):801-10
references.pmid: 16982424
references.citation: Eur J Neurosci. 1999 Apr;11(4):1119-26
references.pmid: 10103108
references.citation: Behav Neurosci. 1992 Oct;106(5):798-807
references.pmid: 1359898
references.citation: J Comp Neurol. 1991 Jul 15;309(3):341-62
references.pmid: 1717517
references.citation: J Hirnforsch. 1984;25(1):1-10
references.pmid: 6725937
references.citation: Neuron. 2012 Nov 8;76(3):470-85
references.pmid: 23141060
references.citation: Neuroscience. 1994 Apr;59(3):625-40
references.pmid: 7516506
references.citation: J Pharmacol Exp Ther. 2004 Oct;311(1):282-9
references.pmid: 15169831