The inhibitory influence of the lateral habenula on midbrain dopamine cells: Ultrastructural evidence for indirect mediation via the rostromedial mesopontine tegmental nucleus

Journal of Comparative Neurology

Volumn 519, Issue 6, 2011, Pages 1143-1164

  Balcita Pedicino, Judith Joyce ^a   Omelchenko, Natalia ^a   Bell, Roland ^a   Sesack, Susan R ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

GABA; Negative reinforcement; Ventral tegmental area

Indexed keywords

4 AMINOBUTYRIC ACID; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL ULTRASTRUCTURE; CONTROLLED STUDY; DENDRITE; DOPAMINERGIC NERVE CELL; ELECTRON MICROSCOPY; HABENULA; IMMUNOREACTIVITY; MALE; MESENCEPHALON; NONHUMAN; PRIORITY JOURNAL; RAT; ROSTROMEDIAL MESOPONTINE TEGMENTAL NUCLEUS; SYNAPTIC INHIBITION; SYNAPTIC TRANSMISSION; TISSUE SECTION; VENTRAL TEGMENTUM;

ANIMALS; DOPAMINE; HABENULA; IMMUNOHISTOCHEMISTRY; MALE; MESENCEPHALON; NEURAL PATHWAYS; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; TEGMENTUM MESENCEPHALI;

EID: 79951808106     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22561     Document Type: Article

References (117)

1. Aizawa H, Isomura Y, Kobayashi M, Harukuni R, Tanaka S, Fukai T, Okamoto H. 2008. Heterogeneity of the lateral habenular neurons revealed by gene expression Soc Neurosci Abstr: 490.492.
2. Amat J, Sparks PD, Matus-Amat P, Griggs J, Watkins LR, Maier SF. 2001. The role of the habenular complex in the elevation of dorsal raphe nucleus serotonin and the changes in the behavioral responses produced by uncontrollable stress. Brain Res 917: 118-126.
3. Araki M, McGeer PL, Kimura H. 1988. The efferent projections of the rat lateral habenular nucleus revealed by the PHA-L anterograde tracing method. Brain Res 441: 319-330.
4. Balcita-Pedicino JJ, Sesack SR. 2007. Orexin axons in the rat ventral tegmental area synapse infrequently onto dopamine and gamma-aminobutyric acid neurons. J Comp Neurol 503: 668-684.
5. Balcita-Pedicino JJ, Omelchenko N, Bell R, Sesack SR. 2009. The rostromedial mesopontine tegmentum as a relay between the lateral habenula and dopamine neurons in the ventral tegmental area: ultrastructural evidence in the rat. Soc Neurosci Abstr: 815.817.
6. Bayer VE, Pickel VM. 1990. Ultrastructural localization of tyrosine hydroxylase in the rat ventral tegmental area: relationship between immunolabeling density and neuronal associations. J Neurosci 10: 2996-3013.
7. Bayer VE, Pickel VM. 1991. GABA-labeled terminals form proportionally more synapses with dopaminergic neurons containing low densities of tyrosine hydroxylase-immunoreactivity in rat ventral tegmental area. Brain Res 559: 44-55.
8. Behzadi G, Kalen P, Parvopassu F, Wiklund L. 1990. Afferents to the median raphe nucleus of the rat: retrograde cholera toxin and wheat germ conjugated horseradish peroxidase tracing, and selective D-[3H]aspartate labelling of possible excitatory amino acid inputs. Neuroscience 37: 77-100.
9. Blurton-Jones M, Tuszynski MH. 2006. Estradiol-induced modulation of estrogen receptor-beta and GABA within the adult neocortex: a potential transsynaptic mechanism for estrogen modulation of BDNF. J Comp Neurol 499: 603-612.
10. Brazhnik E, Shah F, Tepper JM. 2008. GABAergic afferents activate both GABAA and GABAB receptors in mouse substantia nigra dopaminergic neurons in vivo. J Neurosci 28: 10386-10398.
11. Brinschwitz K, Lommel R, Penkalla A, Goertzen A, Geisler S, Veh RW. 2005. Glutamatergic fibers from the lateral habenula do not terminate on dopaminergic neurons in the ventral tegmental area. Soc Neurosci Abstr 31: 891.823.
12. Brinschwitz K, Dittgen A, Madai VI, Lommel R, Geisler S, Veh RW. 2010. Glutamatergic axons from the lateral habenula mainly terminate on GABAergic neurons of the ventral midbrain. Neuroscience 168: 463-476.
13. Brischoux F, Chakraborty S, Brierley DI, Ungless MA. 2009. Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli. Proc Natl Acad Sci U S A 106: 4894-4899.
14. Caldecott-Hazard S, Mazziotta J, Phelps M. 1988. Cerebral correlates of depressed behavior in rats, visualized using 14C-2-deoxyglucose autoradiography. J Neurosci 8: 1951-1961.
15. Carlin RK, Grab DJ, Cohen RS, Siekevitz P. 1980. Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J Cell Biol 86: 831-845.
16. Carr DB, Sesack SR. 2000. Projections from the rat prefrontal cortex to the ventral tegmental area: target specificity in the synaptic associations with mesoaccumbens and mesocortical neurons. J Neurosci 20: 3864-3873.
17. Chan J, Aoki C, Pickel VM. 1990. Optimization of differential immunogold-silver and peroxidase labeling with maintenance of ultrastructure in brain sections before plastic embedding. J Neurosci Methods 33: 113-127.
18. Cheng D, Hoogenraad CC, Rush J, Ramm E, Schlager MA, Duong DM, Xu P, Wijayawardana SR, Hanfelt J, Nakagawa T, Sheng M, Peng J. 2006. Relative and absolute quantification of postsynaptic density proteome isolated from rat forebrain and cerebellum. Mol Cell Proteomics 5: 1158-1170.
19. Christoph GR, Leonzio RJ, Wilcox KS. 1986. Stimulation of the lateral habenula inhibits dopamine-containing neurons in the substantia nigra and ventral tegmental area of the rat. J Neurosci 6: 613-619.
20. Colonnier M. 1968. Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Res 9: 268-287.
21. Colussi-Mas J, Geisler S, Zimmer L, Zahm DS, Berod A. 2007. Activation of afferents to the ventral tegmental area in response to acute amphetamine: a double-labelling study. Eur J Neurosci 26: 1011-1025.
22. 2 receptor within GABAergic neurons of the rat striatum. Brain Res 746: 239-255.
23. Dommett E, Coizet V, Blaha CD, Martindale J, Lefebvre V, Walton N, Mayhew JE, Overton PG, Redgrave P. 2005. How visual stimuli activate dopaminergic neurons at short latency. Science 307: 1476-1479.
24. Dunlop BW, Nemeroff CB. 2007. The role of dopamine in the pathophysiology of depression. Arch Gen Psychiatry 64: 327-337.
25. Ferreira JG, Del-Fava F, Hasue RH, Shammah-Lagnado SJ. 2008. Organization of ventral tegmental area projections to the ventral tegmental area-nigral complex in the rat. Neuroscience 153: 196-213.
26. Fields HL, Hjelmstad GO, Margolis EB, Nicola SM. 2007. Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement. Annu Rev Neurosci 30: 289-316.
27. 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.
28. Geisler S, Trimble M. 2008. The lateral habenula: no longer neglected. CNS Spectr 13: 484-489.
29. Geisler S, Zahm DS. 2005. Afferents of the ventral tegmental area in the rat-anatomical substratum for integrative functions. J Comp Neurol 490: 270-294.
30. Geisler S, Derst C, Veh RW, Zahm DS. 2007. Glutamatergic afferents of the ventral tegmental area in the rat. J Neurosci 27: 5730-5743.
31. Geisler S, Marinelli M, Degarmo B, Becker ML, Freiman AJ, Beales M, Meredith GE, Zahm DS. 2008. Prominent activation of brainstem and pallidal afferents of the ventral tegmental area by cocaine. Neuropsychopharmacology 33: 2688-2700.
32. Grenhoff J, Tung CS, Svensson TH. 1988. The excitatory amino acid antagonist kynurenate induces pacemaker-like firing of dopamine neurons in rat ventral tegmental area in vivo. Acta Physiol Scand 134: 567-568.
33. Haber SN, Knutson B. 2010. The reward circuit: linking primate anatomy and human imaging. Neuropsychopharmacology 35: 4-26.
34. Herkenham M, Nauta WJ. 1977. Afferent connections of the habenular nuclei in the rat. A horseradish peroxidase study, with a note on the fiber-of-passage problem. J Comp Neurol 173: 123-146.
35. Herkenham M, Nauta WJ. 1979. Efferent connections of the habenular nuclei in the rat. J Comp Neurol 187: 19-47.
36. Herzog E, Gilchrist J, Gras C, Muzerelle A, Ravassard P, Giros B, Gaspar P, El Mestikawy S. 2004. Localization of VGLUT3, the vesicular glutamate transporter type 3, in the rat brain. Neuroscience 123: 983-1002.
37. Hikosaka O, Sesack SR, Lecourtier L, Shepard PD. 2008. Habenula: crossroad between the basal ganglia and the limbic system. J Neurosci 28: 11825-11829.
38. Hong S, Hikosaka O. 2008. The globus pallidus sends reward-related signals to the lateral habenula. Neuron 60: 720-729.
39. Hong S, Hikosaka O. 2009. Negative reward signals from lateral habenula to dopamine neurons are mediated by a group of medial mesopontine neurons. Soc Neurosci Abstr: 482.486.
40. Horvitz JC, Stewart T, Jacobs BL. 1997. Burst activity of ventral tegmental dopamine neurons is elicited by sensory stimuli in the awake cat. Brain Res 759: 251-258.
41. Hyland BI, Reynolds JN, Hay J, Perk CG, Miller R. 2002. Firing modes of midbrain dopamine cells in the freely moving rat. Neuroscience 114: 475-492.
42. IsHak WW, Davis M, Jeffrey J, Balayan K, Pechnick RN, Bagot K, Rapaport MH. 2009. The role of dopaminergic agents in improving quality of life in major depressive disorder. Curr Psychiatry Rep 11: 503-508.
43. Jhou TC, Gallagher M. 2007. Paramedian raphe neurons that project to midbrain dopamine neurons are activated by aversive stimuli. Soc Neurosci Abstr 33: 425.425.
44. Jhou TC, Fields HL, Baxter MG, Saper CB, Holland PC. 2009a. The rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses. Neuron 61: 786-800.
45. Jhou TC, Geisler S, Marinelli M, Degarmo BA, Zahm DS. 2009b. The mesopontine rostromedial tegmental nucleus: a structure targeted by the lateral habenula that projects to the ventral tegmental area of Tsai and substantia nigra compacta. J Comp Neurol 513: 566-596.
46. Ji H, Shepard PD. 2007. Lateral habenula stimulation inhibits rat midbrain dopamine neurons through a GABA(A) receptor-mediated mechanism. J Neurosci 27: 6923-6930.
47. Jia HG, Yamuy J, Sampogna S, Morales FR, Chase MH. 2003. Colocalization of gamma-aminobutyric acid and acetylcholine in neurons in the laterodorsal and pedunculopontine tegmental nuclei in the cat: a light and electron microscopic study. Brain Res 992: 205-219.
48. Johnson SW, North RA. 1992. Two types of neurone in the rat ventral tegmental area and their synaptic inputs. J Physiol 450: 455-468.
49. Jones DG, Harris RJ. 1995. An analysis of contemporary morphological concepts of synaptic remodelling in the CNS: perforated synapses revisited. Rev Neurosci 6: 177-219.
50. Kalén P, Karlson M, Wiklund L. 1985. Possible excitatory amino acid afferents to nucleus raphe dorsalis of the rat investigated with retrograde wheat germ agglutinin and D-[3H]aspartate tracing. Brain Res 360: 285-297.
51. Kapur S, Mann JJ. 1992. Role of the dopaminergic system in depression. Biol Psychiat 32: 1-17.
52. Kaufling J, Veinante P, Pawlowski SA, Freund-Mercier M-J, Barrot M. 2009. Afferents to the GABAergic tail of the ventral tegmental area in the rat. J Comp Neurol 513: 597-621.
53. Kaufling J, Veinante P, Pawlowski SA, Freund-Mercier MJ, Barrot M. 2010. Gamma-aminobutyric acid cells with cocaine-induced DeltaFosB in the ventral tegmental area innervate mesolimbic neurons. Biol Psychiat 67: 88-92.
54. Kim U. 2009. Topographic commissural and descending projections of the habenula in the rat. J Comp Neurol 513: 173-187.
55. Kiss J, Csaki A, Bokor H, Kocsis K, Kocsis B. 2002. Possible glutamatergic/aspartatergic projections to the supramammillary nucleus and their origins in the rat studied by selective [(3)H]D-aspartate labelling and immunocytochemistry. Neuroscience 111: 671-691.
56. Klemm WR. 2004. Habenular and interpeduncularis nuclei: shared components in multiple-function networks. Med Sci Monit 10: RA261-273.
57. Lecourtier L, Kelly PH. 2007. A conductor hidden in the orchestra? Role of the habenular complex in monoamine transmission and cognition. Neurosci Biobehav Rev 31: 658-672.
58. Lecourtier L, Defrancesco A, Moghaddam B. 2008. Differential tonic influence of lateral habenula on prefrontal cortex and nucleus accumbens dopamine release. Eur J Neurosci 27: 1755-1762.
59. Lehmann H, Ebert U, Loscher W. 1998. Amygdala-kindling induces a lasting reduction of GABA-immunoreactive neurons in a discrete area of the ipsilateral piriform cortex. Synapse 29: 299-309.
60. Ligorio MA, Akmentin W, Gallery F, Cabot JB. 2000. Ultrastructural localization of the binding fragment of tetanus toxin in putative gamma-aminobutyric acidergic terminals in the intermediolateral cell column: a potential basis for sympathetic dysfunction in generalized tetanus. J Comp Neurol 419: 471-484.
61. Lindvall O, Björklund A, Divac I. 1978. Organization of catecholamine neurons projecting to the frontal cortex in the rat. Brain Res 142: 1-24.
62. Lisoprawski A, Herve D, Blanc G, Glowinski J, Tassin JP. 1980. Selective activation of the mesocortico-frontal dopaminergic neurons induced by lesion of the habenula in the rat. Brain Res 183: 229-234.
63. Liu ZH, Shin R, Ikemoto S. 2008. Dual role of medial A10 dopamine neurons in affective encoding. Neuropsychopharmacology 33: 3010-3020.
64. Ljungberg T, Apicella P, Schultz W. 1992. Responses of monkey dopamine neurons during learning of behavioral reactions. J Neurophysiol 67: 145-163.
65. Matsuda Y, Fujimura K. 1992. Action of habenular efferents on ventral tegmental area neurons studied in vitro. Brain Res Bull 28: 743-749.
66. Matsumoto M, Hikosaka O. 2007. Lateral habenula as a source of negative reward signals in dopamine neurons. Nature 447: 1111-1115.
67. Matsumoto M, Hikosaka O. 2008. Negative motivational control of saccadic eye movement by the lateral habenula. Prog Brain Res 171: 399-402.
68. Matsumoto M, Hikosaka O. 2009. Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 459: 837-841.
69. McCormack AL, Atienza JG, Langston JW, Di Monte DA. 2006. Decreased susceptibility to oxidative stress underlies the resistance of specific dopaminergic cell populations to paraquat-induced degeneration. Neuroscience 141: 929-937.
70. Miner LH, Jedema HP, Moore FW, Blakely RD, Grace AA, Sesack SR. 2006. Chronic stress increases the plasmalemmal distribution of the norepinephrine transporter and the coexpression of tyrosine hydroxylase in norepinephrine axons in the prefrontal cortex. J Neurosci 26: 1571-1578.
71. Montgomery SA. 2008. The under-recognized role of dopamine in the treatment of major depressive disorder. Int Clin Psychopharmacol 23: 63-69.
72. Morris JS, Smith KA, Cowen PJ, Friston KJ, Dolan RJ. 1999. Covariation of activity in habenula and dorsal raphe nuclei following tryptophan depletion. NeuroImage 10: 163-172.
73. Nair-Roberts RG, Chatelain-Badie SD, Benson E, White-Cooper H, Bolam JP, Ungless MA. 2008. Stereological estimates of dopaminergic, GABAergic and glutamatergic neurons in the ventral tegmental area, substantia nigra and retrorubral field in the rat. Neuroscience 152: 1024-1031.
74. Nishikawa T, Fage D, Scatton B. 1986. Evidence for, and nature of, the tonic inhibitory influence of habenulointerpeduncular pathways upon cerebral dopaminergic transmission in the rat. Brain Res 373: 324-336.
75. Okabe S. 2007. Molecular anatomy of the postsynaptic density. Mol Cell Neurosci 34: 503-518.
76. Olson VG, Nestler EJ. 2007. Topographical organization of GABAergic neurons within the ventral tegmental area of the rat. Synapse 61: 87-95.
77. Omelchenko N, Sesack SR. 2005. Laterodorsal tegmental projections to identified cell populations in the rat ventral tegmental area. J Comp Neurol 483: 217-235.
78. Omelchenko N, Sesack SR. 2006. Cholinergic axons in the rat ventral tegmental area synapse preferentially onto mesoaccumbens dopamine neurons. J Comp Neurol 494: 863-875.
79. Omelchenko N, Sesack SR. 2007. Glutamate synaptic inputs to ventral tegmental area neurons in the rat derive primarily from subcortical sources. Neuroscience 146: 1259-1274.
80. Omelchenko N, Sesack SR. 2009. Ultrastructural analysis of local collaterals of rat ventral tegmental area neurons: GABA phenotype and synapses onto dopamine and GABA cells. Synapse 63: 895-906.
81. Omelchenko N, Bell R, Sesack SR. 2009. Lateral habenula projections to dopamine and GABA neurons in the rat ventral tegmental area. Eur J Neurosci 30: 1239-1250.
82. Omelchenko N, Sesack SR. 2010. Periaqueductal gray afferents synapse onto dopamine and GABA neurons in the rat ventral tegmental area. J Neurosci Res 88: 981-991.
83. Overton PG, Clark D. 1997. Burst firing in midbrain dopaminergic neurons. Brain Res Rev 25: 312-334.
84. Pan WX, Hyland BI. 2005. Pedunculopontine tegmental nucleus controls conditioned responses of midbrain dopamine neurons in behaving rats. J Neurosci 25: 4725-4732.
85. Paxinos G, Watson C. 1997. The rat brain in stereotaxic coordinates, 3rd ed. San Diego: Academic Press.
86. Perrotti LI, Bolanos CA, Choi KH, Russo SJ, Edwards S, Ulery PG, Wallace DL, Self DW, Nestler EJ, Barrot M. 2005. DeltaFosB accumulates in a GABAergic cell population in the posterior tail of the ventral tegmental area after psychostimulant treatment. Eur J Neurosci 21: 2817-2824.
87. Pickel VM, Towle A, Joh TH, Chan J. 1988. Gamma-aminobutyric acid in the medial rat nucleus accumbens: ultrastructural localization in neurons receiving monosynaptic input from catecholaminergic afferents. J Comp Neurol 272: 1-14.
88. Pickel VM, Nirenberg MJ, Milner TA. 1996. Ultrastructural view of central catecholaminergic transmission: immunocytochemical localization of synthesizing enzymes, transporters and receptors. J Neurocytol 25: 843-856.
89. Ranft K, Dobrowolny H, Krell D, Bielau H, Bogerts B, Bernstein HG. 2010. Evidence for structural abnormalities of the human habenular complex in affective disorders but not in schizophrenia. Psychol Med 40: 557-567.
90. Redgrave P, Gurney K. 2006. The short-latency dopamine signal: a role in discovering novel actions? Nat Rev Neurosci 7: 967-975.
91. Sandyk R. 1992. Pineal and habenula calcification in schizophrenia. Int J Neurosci 67: 19-30.
92. Sartorius A, Kiening KL, Kirsch P, von Gall CC, Haberkorn U, Unterberg AW, Henn FA, Meyer-Lindenberg A. 2010. Remission of major depression under deep brain stimulation of the lateral habenula in a therapy-refractory patient. Biol Psychiat 67: e9-e11.
93. Scammell TE, Estabrooke IV, McCarthy MT, Chemelli RM, Yanagisawa M, Miller MS, Saper CB. 2000. Hypothalamic arousal regions are activated during modafinil-induced wakefulness. J Neurosci 20: 8620-8628.
94. Schultz W. 1998. Predictive reward signal of dopamine neurons. J Neurophysiol 80: 1-27.
95. Sesack SR, Pickel VM. 1992. Dual ultrastructural localization of enkephalin and tyrosine hydroxylase immunoreactivity in the rat ventral tegmental area: multiple substrates for opiate-dopamine interactions. J Neurosci 12: 1335-1350.
96. Sesack SR, Grace AA. 2010. Cortico-basal ganglia reward network: microcircuitry. Neuropsychopharmacology 35: 27-47.
97. Sesack SR, Snyder CL, Lewis DA. 1995. Axon terminals immunolabeled for dopamine or tyrosine hydroxylase synapse on GABA-immunoreactive dendrites in rat and monkey cortex. J Comp Neurol 363: 264-280.
98. Sesack SR, Hawrylak VA, Guido MA, Levey AI. 1998. Dopamine axon varicosities in the rat prefrontal cortex exhibit sparse immunoreactivity for the dopamine transporter. J Neurosci 18: 2697-2708.
99. Sesack SR, Miner LAH, Omelchenko N. 2006. Pre-embedding immunoelectron microscopy: applications for studies of the nervous system. In: Zaborszky L, Wouterlood FG, Lanciego JL, editors. Neuroanatomical tract-tracing 3: molecules, neurons, systems. New York: Springer. p 6-71.
100. Sheng M, Hoogenraad CC. 2007. The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu Rev Biochem 76: 823-847.
101. Shepard PD, Holcomb HH, Gold JM. 2006. Schizophrenia in translation: the presence of absence: habenular regulation of dopamine neurons and the encoding of negative outcomes. Schiz Bull 32: 417-421.
102. Shink E, Smith Y. 1995. Differential synaptic innervation of neurons in the internal and external segments of the globus pallidus by the GABA- and glutamate-containing terminals in the squirrel monkey. J Comp Neurol 358: 119-141.
103. Shumake J, Gonzalez-Lima F. 2003. Brain systems underlying susceptibility to helplessness and depression. Behav Cogn Neurosci Rev 2: 198-221.
104. Steffensen SC, Svingos AL, Pickel VM, Henriksen SJ. 1998. Electrophysiological characterization of GABAergic neurons in the ventral tegmental area. J Neurosci 18: 8003-8015.
105. Sutherland RJ. 1982. The dorsal diencephalic conduction system: a review of the anatomy and functions of the habenular complex. Neurosci Biobehav Rev 6: 1-13.
106. Swanson LW. 1982. The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 9: 321-353.
107. Tepper JM, Lee CR. 2007. GABAergic control of substantia nigra dopaminergic neurons. Prog Brain Res 160: 189-208.
108. Ullsperger M, von Cramon DY. 2003. Error monitoring using external feedback: specific roles of the habenular complex, the reward system, and the cingulate motor area revealed by functional magnetic resonance imaging. J Neurosci 23: 4308-4314.
109. Ungless MA, Magill PJ, Bolam JP. 2004. Uniform inhibition of dopamine neurons in the ventral tegmental area by aversive stimuli. Science 303: 2040-2042.
110. Van Bockstaele EJ, Pickel VM. 1995. GABA-containing neurons in the ventral tegmental area project to the nucleus accumbens in rat brain. Brain Res 682: 215-221.
111. Van Bockstaele EJ, Chan J, Pickel VM. 1996. Pre- and postsynaptic sites for serotonin modulation of GABA-containing neurons in the shell region of the rat nucleus accumbens. J Comp Neurol 371: 116-128.
112. Veznedaroglu E, Milner TE. 1992. Elimination of artifactual labeling of hippocampal mossy fibers seen following pre-embedding immunogold-silver technique by pretreatment with zinc chelator. Microscopy Res Tech 23: 100-101.
113. Wang DG, Gong N, Luo B, Xu TL. 2006. Absence of GABA type A signaling in adult medial habenular neurons. Neuroscience 141: 133-141.
114. Wise RA. 2004. Dopamine, learning and motivation. Nat Rev Neurosci 5: 483-494.
115. Wolf ME, Kapatos G. 1989. Flow cytometric analysis of rat striatal nerve terminals. J Neurosci 9: 94-105.
116. Yamauchi T. 2002. Molecular constituents and phosphorylation-dependent regulation of the post-synaptic density. Mass Spectrom Rev 21: 266-286.
117. Yang LM, Hu B, Xia YH, Zhang BL, Zhao H. 2008. Lateral habenula lesions improve the behavioral response in depressed rats via increasing the serotonin level in dorsal raphe nucleus. Behav Brain Res 188: 84-90.