The substantia nigra conveys target-dependent excitatory and inhibitory outputs from the basal ganglia to the thalamus

Journal of Neuroscience

Volumn 34, Issue 23, 2014, Pages 8032-8042

  Antal, Miklos ^a   Beneduce, Brandon M ^a   Regehr, Wade G ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Circuitry; Substantia nigra; vGluT2

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; TYROSINE 3 MONOOXYGENASE; VESICULAR GLUTAMATE TRANSPORTER 2;

ANIMAL TISSUE; ARTICLE; BASAL GANGLION; CONFOCAL MICROSCOPY; DOPAMINERGIC NERVE CELL; ELECTROPHYSIOLOGICAL PROCEDURES; EPIFLUORESCENCE MICROSCOPY; EXCITABILITY; EXCITATORY JUNCTION POTENTIAL; INHIBITORY POSTSYNAPTIC POTENTIAL; MOUSE; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; SUBSTANTIA NIGRA; SUBSTANTIA NIGRA PARS COMPACTA; SYNAPSE; SYNAPTIC TRANSMISSION; THALAMUS; THALAMUS POSTERIOR NUCLEUS; THALAMUS RETICULAR NUCLEUS; TRANSGENIC MOUSE; WHOLE CELL PATCH CLAMP;

CIRCUITRY; SUBSTANTIA NIGRA; VGLUT2;

ACTION POTENTIALS; ANIMALS; BASAL GANGLIA; DEPENDOVIRUS; GLUTAMATE DECARBOXYLASE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURAL INHIBITION; NEURAL PATHWAYS; NEUROTRANSMITTER AGENTS; PHOTIC STIMULATION; RHODOPSIN; SUBSTANTIA NIGRA; THALAMUS; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 84901757218     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0236-14.2014     Document Type: Article

References (111)

1. Adamantidis AR, Tsai HC, Boutrel B, Zhang F, Stuber GD, Budygin EA, Touriño C, Bonci A, Deisseroth K, de Lecea L (2011) Optogenetic interrogation of dopaminergic modulation of the multiple phases of rewardseeking behavior. J Neurosci 31:10829-10835. CrossRef Medline
2. Aggleton JP, Neave N, Nagle S, Sahgal A (1995) A comparison of the effects of medial prefrontal, cingulate cortex, and cingulum bundle lesions on tests of spatial memory: evidence of a double dissociation between frontal and cingulum bundle contributions. J Neurosci 15:7270-7281. Medline
3. Aggleton JP, Hunt PR, Nagle S, Neave N (1996) The effects of selective lesions within the anterior thalamic nuclei on spatial memory in the rat. Behav Brain Res 81:189-198. CrossRef Medline
4. Alexander GE, Crutcher MD (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13:266-271. CrossRef Medline
5. Alexander GE, Crutcher MD, De Long MR (1991) Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. In: The prefrontal cortex: its structure, function and pathology; Progress in Brain Research (Uylings HBM, ed), pp 119-146. New York: Elsevier.
6. Alexinsky T (2001) Differential effect of thalamic and cortical lesions on memory systems in the rat. Behav Brain Res 122:175-191. CrossRef Medline
7. Alsio J, Nordenankar K, Arvidsson E, Birgner C, Mahmoudi S, Halbout B, Smith C, Fortin GM, Olson L, Descarries L, Trudeau LE, Kullander K, Levesque D, Wallen-Mackenzie A (2011) Enhanced sucrose and cocaine self-administration and cue-induced drug seeking after loss of VGLUT2 in midbrain dopamine neurons in mice. J Neurosci 31:12593-12603. CrossRef Medline
8. Barbas H, Zikopoulos B (2007) The prefrontal cortex and flexible behavior. Neuroscientist 13:532-545. CrossRef Medline
9. Barbas H, García-Cabezas MÁ, Zikopoulos B (2013) Frontal-thalamic circuits associated with language. Brain Lang 126:49-61. CrossRef Medline
10. Bateup HS, Santini E, Shen W, Birnbaum S, Valjent E, Surmeier DJ, Fisone G, Nestler EJ, Greengard P (2010) Distinct subclasses of medium spiny neurons differentially regulate striatal motor behaviors. Proc Natl Acad Sci U S A 107:14845-14850. CrossRef Medline
11. Bazhenov M, Timofeev I, Steriade M, Sejnowski TJ (1999) Self-sustained rhythmic activity in the thalamic reticular nucleus mediated by depolarizing GABAA receptor potentials. Nat Neurosci 2:168-174. CrossRef Medline
12. Beckstead RM (1983) Long collateral branches of substantia nigra pars reticulata axons to thalamus, superior colliculus and reticular formation in monkey and cat. Multiple retrograde neuronal labeling with fluorescent dyes. Neuroscience 10:767-779. CrossRef Medline
13. Berényi A, Gombköto P, Farkas A, Paróczy Z, Márkus Z, Averkin RG, Benedek G, Nagy A (2009) How moving visual stimuli modulate the activity of the substantia nigra pars reticulata. Neuroscience 163:1316-1326. CrossRef Medline
14. Birgner C, Nordenankar K, Lundblad M, Mendez JA, Smith C, le Greves M, Galter D, Olson L, Fredriksson A, Trudeau LE, Kullander K, Wallen-Mackenzie AVGLUT2in dopamine neurons is required for psychostimulantinduced behavioral activation. Proc Natl Acad Sci USA107:389-394. CrossRef Medline
15. Bolam JP, Hanley JJ, Booth PA, Bevan MD (2000) Synaptic organisation of the basal ganglia. J Anat 196:527-542. CrossRef Medline
16. Burton H, Jones EG (1976) The posterior thalamic region and its cortical projection in new world and old world monkeys. J Comp Neurol 168: 249-301. CrossRef Medline
17. Cappe C, Morel A, Barone P, Rouiller EM (2009) The thalamocortical projection systems in primate: an anatomical support for multisensory and sensorimotor interplay. Cereb Cortex 19:2025-2037. CrossRef Medline
18. Cebrián C, Prensa L (2010) Basal ganglia and thalamic input from neurons located within the ventral tier cell cluster region of the substantia nigra pars compacta in the rat. J Comp Neurol 518:1283-1300. CrossRef Medline
19. Cebrián C, Parent A, Prensa L (2005) Patterns of axonal branching of neurons of the substantia nigra pars reticulata and pars lateralis in the rat. J Comp Neurol 492:349-369. CrossRef Medline
20. Chevalier G, Deniau JM (1984) Spatio-temporal organization of a branched tecto-spinal/tecto-diencephalic neuronal system. Neuroscience 12:427-439. CrossRef Medline
21. Chevalier G, Deniau JM (1990) Disinhibition as a basic process in the expression of striatal functions. Trends Neurosci 13:277-280. CrossRef Medline
22. Chevalier G, Vacher S, Deniau JM, Desban M (1985) Disinhibition as a basic process in the expression of striatal functions. I. The striato-nigral influence on tecto-spinal/tecto-diencephalic neurons. Brain Res 334:215-226. CrossRef Medline
23. Daubaras M, Dal Bo G, Flores C (2014) Target-dependent expression of the netrin-1 receptor, UNC5C, in projection neurons of the ventral tegmental area. Neuroscience 260:36-46. CrossRef Medline
24. De Long MR, Wichmann T (2007) Circuits and circuit disorders of the basal ganglia. Arch Neurol 64:20-24. CrossRef Medline
25. Deniau JM, Mailly P, Maurice N, Charpier S (2007) The pars reticulata of the substantia nigra: a window to basal ganglia output. Prog Brain Res 160:151-172. CrossRef Medline
26. Destexhe A, Contreras D, Sejnowski TJ, Steriade M (1994) A model of spindle rhythmicity in the isolated thalamic reticular nucleus. J Neurophysiol 72:803-818. Medline
27. Deutch AY, Goldstein M, Roth RH (1986) The ascending projections of the dopaminergic neurons of the substantia nigra, zona reticulata: a combined retrograde tracer-immunohistochemical study. Neurosci Lett 71: 257-263. CrossRef Medline
28. Di Chiara G, Porceddu ML, Morelli M, Mulas ML, Gessa GL (1979) Evidence for a GABAergic projection from the substantia nigra to the ventromedial thalamus and to the superior colliculus of the rat. Brain Res 176:273-284. CrossRef Medline
29. Doupe AJ, Perkel DJ, Reiner A, Stern EA (2005) Birdbrains could teach basal ganglia research a new song. Trends Neurosci 28:353-363. CrossRef Medline
30. Engber TM, Papa SM, Boldry RC, Chase TN (1994) NMDAreceptor blockade reverses motor response alterations induced by levodopa. Neuroreport 5:2586-2588. CrossRef Medline
31. Eyre MD, Antal M, Nusser Z (2008) Distinct deep short-axon cell subtypes of the main olfactory bulb provide novel intrabulbar and extrabulbar GABAergic connections. J Neurosci 28:8217-8229. CrossRef Medline
32. Faull RL, Mehler WR (1978) The cells of origin of nigrotectal, nigrothalamic and nigrostriatal projections in the rat. Neuroscience 3:989-1002. CrossRef Medline
33. Ferrarelli F, Tononi G (2011) The thalamic reticular nucleus and schizophrenia. Schizophr Bull 37:306-315. CrossRef Medline
34. François C, Tande D, Yelnik J, Hirsch EC (2002) Distribution and morphology of nigral axons projecting to the thalamus in primates. J Comp Neurol 447:249-260. CrossRef Medline
35. Fremeau RT Jr, Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, Fortin D, Storm-Mathisen J, Edwards RH (2001) The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31:247-260. CrossRef Medline
36. Gittis AH, Nelson AB, Thwin MT, Palop JJ, Kreitzer AC (2010) Distinct roles of GABAergic interneurons in the regulation of striatal output pathways. J Neurosci 30:2223-2234. CrossRef Medline
37. Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, Schambra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME, Heintz N (2003) A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425:917-925. CrossRef Medline
38. Gong S, Doughty M, Harbaugh CR, Cummins A, Hatten ME, Heintz N, Gerfen CR (2007) Targeting Cre recombinase to specific neuron populations with bacterial artificial chromosome constructs. J Neurosci 27: 9817-9823. CrossRef Medline
39. Gossel M, Schmidt WJ, Löscher W, Zajaczkowski W, Danysz W (1995) Effect of coadministration of glutamate receptor antagonists and dopaminergic agonists on locomotion in monoamine-depleted rats. J Neural Transm Park Dis Dement Sect 10:27-39. CrossRef Medline
40. Gould E, Butcher LL (1986) Cholinergic neurons in the rat substantia nigra. Neurosci Lett 63:315-319. CrossRef Medline
41. Grueter BA, Rothwell PE, Malenka RC (2012) Integrating synaptic plasticity and striatal circuit function in addiction. Curr Opin Neurobiol 22:545-551. CrossRef Medline
42. Guillery RW, Harting JK (2003) Structure and connections of the thalamic reticular nucleus: advancing views over half a century. J Comp Neurol 463:360-371. CrossRef Medline
43. Haber SN, Calzavara R (2009) The cortico-basal ganglia integrative network: the role of the thalamus. Brain Res Bull 78:69-74. CrossRef Medline
44. Hauber W (1998) Involvement of basal ganglia transmitter systems in movement initiation. Prog Neurobiol 56:507-540. CrossRef Medline
45. Hicks RR, Huerta MF (1991) Differential thalamic connectivity of rostral and caudal parts of cortical area Fr2 in rats. Brain Res 568:325-329. CrossRef Medline
46. Jin X, Costa RM (2010) Start/stop signals emerge in nigrostriatal circuits during sequence learning. Nature 466:457-462. CrossRef Medline
47. Joel D, Weiner I (1994) The organization of the basal gangliathalamocortical circuits: open interconnected rather than closed segregated. Neuroscience 63:363-379. CrossRef Medline
48. Kagan R, Kainz V, Burstein R, Noseda R (2013) Hypothalamic and basal ganglia projections to the posterior thalamus: possible role in modulation of migraine headache and photophobia. Neuroscience 248C:359-368. CrossRef Medline
49. Kamishina H, Yurcisin GH, Corwin JV, Reep RL (2008) Striatal projections from the rat lateral posterior thalamic nucleus. Brain Res 1204:24-39. CrossRef Medline
50. Kamishina H, Conte WL, Patel SS, Tai RJ, Corwin JV, Reep RL (2009) Cortical connections of the rat lateral posterior thalamic nucleus. Brain Res 1264:39-56. CrossRef Medline
51. Katz LC, Burkhalter A, Dreyer WJ (1984) Fluorescent latex microspheres as a retrograde neuronal marker for in vivo and in vitro studies of visual cortex. Nature 310:498-500. CrossRef Medline
52. Kawano M, Kawasaki A, Sakata-Haga H, Fukui Y, Kawano H, Nogami H, Hisano S (2006) Particular subpopulations of midbrain and hypothalamic dopamine neurons express vesicular glutamate transporter 2 in the rat brain. J Comp Neurol 498:581-592. CrossRef Medline
53. Kha HT, Finkelstein DI, Tomas D, Drago J, Pow DV, Horne MK (2001) Projections from the substantia nigra pars reticulata to the motor thalamus of the rat: single axon reconstructions and immunohistochemical study. J Comp Neurol 440:20-30. CrossRef Medline
54. Kilpatrick IC, Starr MS, Fletcher A, James TA, MacLeod NK (1980) Evidence for a GABAergic nigrothalamic pathway in the rat. Exp Brain Res 40:45. Medline
55. Klockgether T, Turski L (1990) NMDA antagonists potentiate antiparkinsonian actions of L-dopa in monoamine-depleted rats. Ann Neurol 28: 539-546. CrossRef Medline
56. Klockgether T, Turski L, Honoré T, Zhang ZM, Gash DM, Kurlan R, Greenamyre JT (1991) The AMPA receptor antagonist NBQX has antiparkinsonian effects in monoamine-depleted rats and MPTP-treated monkeys. Ann Neurol 30:717-723. CrossRef Medline
57. Kravitz AV, Freeze BS, Parker PR, Kay K, Thwin MT, Deisseroth K, Kreitzer AC (2010) Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466:622-626. CrossRef Medline
58. Lammel S, Hetzel A, Häckel O, Jones I, Liss B, Roeper J (2008) Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron 57:760-773. CrossRef Medline
59. Landisman CE, Long MA, Beierlein M, Deans MR, Paul DL, Connors BW (2002) Electrical synapses in the thalamic reticular nucleus. J Neurosci 22:1002-1009. Medline
60. Lavin A, Grace AA (1998) Dopamine modulates the responsivity of mediodorsal thalamic cells recorded in vitro. J Neurosci 18:10566-10578. Medline
61. Leblois A, Bodor AL, Person AL, Perkel DJ (2009) Millisecond timescale disinhibition mediates fast information transmission through an avian basal ganglia loop. J Neurosci 29:15420-15433. CrossRef Medline
62. Levandis G, Bazzini E, Armentero MT, Nappi G, Blandini F (2008) Systemic administration of an m Glu R5 antagonist, but not unilateral subthalamic lesion, counteracts l-DOPA-induced dyskinesias in a rodent model of Parkinson's disease. Neurobiol Dis 29:161-168. CrossRef Medline
63. Löschmann PA, Lange KW, Kunow M, Rettig KJ, Jähnig P, Honoré T, Turski L, Wachtel H, Jenner P, Marsden CD (1991) Synergism of the AMPAantagonist NBQXand the NMDA-antagonist CPP with L-dopa in models of Parkinson's disease. J Neural Transm Park Dis Dement Sect 3:203-213. CrossRef Medline
64. MacLeod NK, James TA, Kilpatrick IC, Starr MS (1980) Evidence for a GABAergic nigrothalamic pathway in the rat. II. Electrophysiological studies. Exp Brain Res 40:55-61. Medline
65. Maj J, Rogoz Z, Skuza G, Kolodziejczyk K (1995) Some central effects of GYKI 52466, a non-competitive AMPA receptor antagonist. Polish J Pharmacol 47:501-507.
66. Marks GA, Roffwarg HP (1993) Spontaneous activity in the thalamic reticular nucleus during the sleep/wake cycle of the freely-moving rat. Brain Res 623:241-248. CrossRef Medline
67. Marti M, Paganini F, Stocchi S, Mela F, Beani L, Bianchi C, Morari M (2003) Plasticity of glutamatergic control of striatal acetylcholine release in experimental parkinsonism: opposite changes at group-II metabotropic and NMDA receptors. J Neurochem 84:792-802. CrossRef Medline
68. McAlonan K, Cavanaugh J, Wurtz RH (2006) Attentional modulation of thalamic reticular neurons. J Neurosci 26:4444-4450. CrossRef Medline
69. Miyamoto Y, Jinnai K (1994) The inhibitory input from the substantia nigra to the mediodorsal nucleus neurons projecting to the prefrontal cortex in the cat. Brain Res 649:313-318. CrossRef Medline
70. Oertel WH, Mugnaini E (1984) Immunocytochemical studies of GABAergic neurons in rat basal ganglia and their relations to other neuronal systems. Neurosci Lett 47:233-238. CrossRef Medline
71. Packard MG, Knowlton BJ (2002) Learning and memory functions of the basal ganglia. Annu Rev Neurosci 25:563-593. CrossRef Medline
72. Paré D, Hazrati LN, Parent A, Steriade M (1990) Substantia nigra pars reticulata projects to the reticular thalamic nucleus of the cat: a morphological and electrophysiological study. Brain Res 535:139-146. CrossRef Medline
73. Pascoli V, Turiault M, Lüscher C (2012) Reversal of cocaine-evoked synaptic potentiation resets drug-induced adaptive behaviour. Nature 481:71-75. CrossRef Medline
74. Person AL, Perkel DJ (2005) Unitary IPSPs drive precise thalamic spiking in a circuit required for learning. Neuron 46:129-140. CrossRef Medline
75. Pinault D (2004) The thalamic reticular nucleus: structure, function and concept. Brain Res Brain Res Rev 46:1-31. CrossRef Medline
76. Przedborski S (2005) Pathogenesis of nigral cell death in Parkinson's disease. Parkinsonism Relat Disord 11 [Suppl 1]:S3-S7. CrossRef Medline
77. Quattrochi JJ, Mamelak AN, Madison RD, Macklis JD, Hobson JA (1989) Mapping neuronal inputs to REM sleep induction sites with carbacholfluorescent microspheres. Science 245:984-986. CrossRef Medline
78. Rajakumar N, Elisevich K, Flumerfelt BA (1994) Parvalbumin-containing GABAergic neurons in the basal ganglia output system of the rat. J Comp Neurol 350:324-336. CrossRef Medline
79. Ray JP, Price JL (1992) The organization of the thalamocortical connections of the mediodorsal thalamic nucleus in the rat, related to the ventral forebrain-prefrontal cortex topography. J Comp Neurol 323:167-197. CrossRef Medline
80. Reep RL, Corwin JV, Hashimoto A, Watson RT (1987) Efferent connections of the rostral portion of medial agranular cortex in rats. Brain Res Bull 19:203-221. CrossRef Medline
81. Reep RL, Chandler HC, King V, Corwin JV (1994) Rat posterior parietal cortex: topography of corticocortical and thalamic connections. Exp Brain Res 100:67-84. CrossRef Medline
82. Riddle DR, Lo DC, Katz LC (1995) NT-4-mediated rescue of lateral geniculate neurons from effects of monocular deprivation. Nature 378:189-191. CrossRef Medline
83. Robelet S, Melon C, Guillet B, Salin P, Kerkerian-Le Goff L (2004) Chronic L-DOPA treatment increases extracellular glutamate levels and GLT1 expression in the basal ganglia in a rat model of Parkinson's disease. Eur J Neurosci 20:1255-1266. CrossRef Medline
84. Russchen FT, Amaral DG, Price JL (1987) The afferent input to the magnocellular division of the mediodorsal thalamic nucleus in the monkey, Macaca fascicularis. J Comp Neurol 256:175-210. CrossRef Medline
85. Sakai ST, Grofova I, Bruce K (1998) Nigrothalamic projections and nigrothalamocortical pathway to the medial agranular cortex in the rat: single-and double-labeling light and electron microscopic studies. J Comp Neurol 391:506-525. CrossRef Medline
86. Samadi P, Grégoire L, Morissette M, Calon F, Hadj Tahar A, Dridi M, Belanger N, Meltzer LT, Bédard PJ, Di Paolo T (2008) m Glu R5 metabotropic glutamate receptors and dyskinesias in MPTP monkeys. Neurobiol Aging 29:1040-1051. CrossRef Medline
87. Sánchez-González MA, García-Cabezas MA, Rico B, Cavada C (2005) The primate thalamus is a key target for brain dopamine. J Neurosci 25:6076-6083. CrossRef Medline
88. Schmidt R, Leventhal DK, Mallet N, Chen F, Berke JD (2013) Canceling actions involves a race between basal ganglia pathways. Nat Neurosci 16:1118-1124. CrossRef Medline
89. Silkis I (2001) The cortico-basal ganglia-thalamocortical circuit with synaptic plasticity. II. Mechanism of synergistic modulation of thalamic activity via the direct and indirect pathways through the basal ganglia. Biosystems 59:7-14. CrossRef Medline
90. Smith AD, Bolam JP (1990) The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurones. Trends Neurosci 13:259-265. CrossRef Medline
91. Sridharan D, Prashanth PS, Chakravarthy VS (2006) The role of the basal ganglia in exploration in a neural model based on reinforcement learning. Int J Neural Syst 16:111-124. CrossRef Medline
92. Stuber GD, Hnasko TS, Britt JP, Edwards RH, Bonci A (2010) Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate. J Neurosci 30:8229-8233. CrossRef Medline
93. Sukekawa K (1988) Reciprocal connections between medial prefrontal cortex and lateral posterior nucleus in rats. Brain Behav Evol 32:246-251. CrossRef Medline
94. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, Kaneko T (2003) Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467:60-79. CrossRef Medline
95. Tecuapetla F, Patel JC, Xenias H, English D, Tadros I, Shah F, Berlin J, Deisseroth K, Rice ME, Tepper JM, Koos T (2010) Glutamatergic signaling by mesolimbic dopamine neurons in the nucleus accumbens. J Neurosci 30:7105-7110. CrossRef Medline
96. Timmerman W, Westerink BH (1997) Electrical stimulation of the substantia nigra reticulata: detection of neuronal extracellular GABA in the ventromedial thalamus and its regulatory mechanism using microdialysis in awake rats. Synapse (New York) 26:62-71. CrossRef Medline
97. Tritsch NX, Sabatini BL (2012) Dopaminergic modulation of synaptic transmission in cortex and striatum. Neuron 76:33-50. CrossRef Medline
98. Tsumori T, Yokota S, Ono K, Yasui Y (2002) Synaptic organization of GABAergic projections from the substantia nigra pars reticulata and the reticular thalamic nucleus to the parafascicular thalamic nucleus in the rat. Brain Res 957:231-241. CrossRef Medline
99. Ueki A, Uno M, Anderson M, Yoshida M (1977) Monosynaptic inhibition of thalamic neurons produced by stimulation of the substantia nigra. Experientia 33:1480-1482. CrossRef Medline
100. Vargo JM, Corwin JV, King V, Reep RL (1988) Hemispheric asymmetry in neglect produced by unilateral lesions of dorsomedial prefrontal cortex in rats. Exp Neurol 102:199-209. CrossRef Medline
101. Vong L, Ye C, Yang Z, Choi B, Chua S Jr, Lowell BB (2011) Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons. Neuron 71:142-154. CrossRef Medline
102. Wichmann T, De Long MR (2007) Anatomy and physiology of the basal ganglia: relevance to Parkinson's disease and related disorders. In: Handbook of clinical neurology (Aminoff MJ, Boller F, Swaab DF, Koller WC, Melamed E, eds.), pp. 1, 3-18. New York: Elsevier.
103. Witten IB, Lin SC, Brodsky M, Prakash R, Diester I, Anikeeva P, Gradinaru V, Ramakrishnan C, Deisseroth K (2010) Cholinergic interneurons control local circuit activity and cocaine conditioning. Science 330:1677-1681. CrossRef Medline
104. Xiao D, Zikopoulos B, Barbas H (2009) Laminar and modular organization of prefrontal projections to multiple thalamic nuclei. Neuroscience 161: 1067-1081. CrossRef Medline
105. Yagüe JG, Cavaccini A, Errington AC, Crunelli V, Di Giovanni G (2013) Dopaminergic modulation of tonic but not phasic GABAA-receptormediated current in the ventrobasal thalamus of Wistar and GAERS rats. Exp Neurol 247:1-7. CrossRef Medline
106. Yamaguchi T, Wang HL, Morales M (2013) Glutamate neurons in the substantia nigra compacta and retrorubral field. Eur J Neurosci 38:3602-3610. CrossRef Medline
107. Yung KK, Kwok KH, Gao ZG, Choi SY, Kwok FS (1998) Expression of GABA transaminase immunoreactivity in interneurons of the rat neostriatum. Neurochem Int 33:567-572. CrossRef Medline
108. Zikopoulos B, Barbas H (2006) Prefrontal projections to the thalamic reticular nucleus form a unique circuit for attentional mechanisms. J Neurosci 26:7348-7361. CrossRef Medline
109. Zikopoulos B, Barbas H (2007a) Circuits formultisensory integration and attentional modulation through the prefrontal cortex and the thalamic reticular nucleus in primates. Rev Neurosci 18:417-438. Medline
110. Zikopoulos B, Barbas H (2007b) Parallel driving and modulatory pathways link the prefrontal cortex and thalamus. PLo S One 2:e848. CrossRef Medline
111. Zikopoulos B, Barbas H (2012) Pathways for emotions and attention converge on the thalamic reticular nucleus in primates. J Neurosci 32:5338-5350. CrossRef Medline