Progress in understanding mood disorders: Optogenetic dissection of neural circuits

Genes, Brain and Behavior

Volumn 13, Issue 1, 2014, Pages 38-51

  Lammel, S ^a   Tye, K M ^b   Warden, M R ^c,d  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c Department of Obstetrics Gynecology   (United States)

^d Stanford University   (United States)

Author keywords

Animal models; Behavior; Depression; Dopamine; Mesolimbic; Mood disorders; Neural circuits; Optogenetics; Prefrontal cortex; Psychiatry

Indexed keywords

DOPAMINE;

ANXIETY DISORDER; ARTICLE; BRAIN NERVE CELL; DEPRESSION; MESENCEPHALON; MOOD DISORDER; NERVE CELL NETWORK; NONHUMAN; OPTOGENETICS; PREFRONTAL CORTEX; PRIORITY JOURNAL; VENTRAL TEGMENTUM;

ANIMAL MODELS; BEHAVIOR; DEPRESSION; DOPAMINE; MESOLIMBIC; MOOD DISORDERS; NEURAL CIRCUITS; OPTOGENETICS; PREFRONTAL CORTEX; PSYCHIATRY;

ANIMALS; BRAIN; CONNECTOME; DOPAMINE; HUMANS; MOOD DISORDERS; NERVE NET; OPTOGENETICS;

EID: 84891605859     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/gbb.12049     Document Type: Article

References (175)

1. Abercrombie, E.D., Keefe, K.A., DiFrischia, D.S. & Zigmond, M.J. (1989) Differential effect of stress on in vivo dopamine release in striatum, nucleus accumbens, and medial frontal cortex. J Neurochem 52, 1655-1658.
2. Adamantidis, A.R., Tsai, H.C., Boutrel, B., Zhang, F., Stuber, G.D., Budygin, E.A., Tourino, C., Bonci, A., Deisseroth, K. & de Lecea, L. (2011) Optogenetic interrogation of dopaminergic modulation of the multiple phases of reward-seeking behavior. J Neurosci 31, 10829-10835.
3. Amat, J., Baratta, M.V., Paul, E., Bland, S.T., Watkins, L.R. & Maier, S.F. (2005) Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat Neurosci 8, 365-371.
4. Anikeeva, P., Andalman, A.S., Witten, I., Warden, M., Goshen, I., Grosenick, L., Gunaydin, L., Frank, L.M. & Deisseroth, K. (2012) Optetrode: a multichannel readout for optogenetic control in freely moving mice. Nat Neurosci 15, 163-170.
5. Anstrom, K.K. & Woodward, D.J. (2005) Restraint increases dopaminergic burst firing in awake rats. Neuropsychopharmacology 30, 1832-1840.
6. Anstrom, K.K., Miczek, K.A. & Budygin, E.A. (2009) Increased phasic dopamine signaling in the mesolimbic pathway during social defeat in rats. Neuroscience 161, 3-12.
7. Balcita-Pedicino, J.J., Omelchenko, N., Bell, R. & Sesack, S.R. (2011) The inhibitory influence of the lateral habenula on midbrain dopamine cells: ultrastructural evidence for indirect mediation via the rostromedial mesopontine tegmental nucleus. J Comp Neurol 519, 1143-1164.
8. Baratta, M.V., Zarza, C.M., Gomez, D.M., Campeau, S., Watkins, L.R. & Maier, S.F. (2009) Selective activation of dorsal raphe nucleus-projecting neurons in the ventral medial prefrontal cortex by controllable stress. Eur J Neurosci 30, 1111-1116.
9. Barris, R.W. & Schuman, H.R. (1953) Bilateral anterior cingulate gyrus lesions: syndrome of the anterior cingulate gyri. Neurology 3, 44-52.
10. Beck, A.T. & Alford, B.A. (2009) Depression: Causes and Treatments, 2nd edn. University of Pennsylvania Press.
11. Benton, A. (1968) Differential behavioral effects in frontal lobe disease. Neuropsychologia 6, 53-60.
12. Bernard, R. & Veh, R.W. (2012) Individual neurons in the rat lateral habenular complex project mostly to the dopaminergic ventral tegmental area or to the serotonergic raphe nuclei. J Comp Neurol 520, 2545-2558.
13. Berton, O., McClung, C.A., Dileone, R.J., Krishnan, V., Renthal, W., Russo, S.J., Graham, D., Tsankova, N.M., Bolanos, C.A., Rios M., Monteggia L.M., Self, D.W. & Nestler, E.J. (2006) Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311, 864-868.
14. Berton, O., Hahn, C.-G. & Thase, M.E. (2012) Are we getting closer to valid translational models for major depression? Science 338, 75-79.
15. Bewernick, B.H., Hurlemann, R., Matusch, A., Kayser, S., Grubert, C., Hadrysiewicz, B., Axmacher, N., Lemke, M., Cooper-Mahkorn, D., Cohen, M.X., Brockmann, H., Lenartz, D., Sturm, V. & Schlaepfer, T.E. (2010) Nucleus accumbens deep brain stimulation decreases ratings of depression and anxiety in treatment-resistant depression. Biol Psychiatry 67, 110-116.
16. Bjorklund, A. & Dunnett, S.B. (2007) Dopamine neuron systems in the brain: an update. Trends Neurosci 30, 194-202.
17. Bourdy, R. & Barrot, M. (2012) A new control center for dopaminergic systems: pulling the VTA by the tail. Trends Neurosci 35, 681-690.
18. Boyden, E.S., Zhang, F., Bamberg, E., Nagel, G. & Deisseroth, K. (2005) Millisecond-timescale, genetically targeted optical control of neural activity. Nat Neurosci 8, 1263-1268.
19. Brinschwitz, K., Dittgen, A., Madai, V.I., Lommel, R., Geisler, S. & Veh, R.W. (2010) Glutamatergic axons from the lateral habenula mainly terminate on GABAergic neurons of the ventral midbrain. Neuroscience 168, 463-476.
20. Brischoux, F., Chakraborty, S., Brierley, D.I. & Ungless, M.A. (2009) Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli. Proc Natl Acad Sci USA 106, 4894-4899.
21. Britt, J.P., Benaliouad, F., McDevitt, R.A., Stuber, G.D., Wise, R.A. & Bonci, A. (2012) Synaptic and behavioral profile of multiple glutamatergic inputs to the nucleus accumbens. Neuron 76, 790-803.
22. Bromberg-Martin, E.S. & Hikosaka, O. (2011) Lateral habenula neurons signal errors in the prediction of reward information. Nat Neurosci 14, 1209-1216.
23. Bromberg-Martin, E.S., Matsumoto, M. & Hikosaka, O. (2010) Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 68, 815-834.
24. Brown, V.J. & Bowman, E.M. (2002) Rodent models of prefrontal cortical function. Trends Neurosci 25, 340-343.
25. Brown, M.T.C., Tan, K.R., O'Connor, E.C., Nikonenko, I., Muller, D. & Lüscher, C. (2012) Ventral tegmental area GABA projections pause accumbal cholinergic interneurons to enhance associative learning. Nature 492, 452-456.
26. Butts, K.A., Weinberg, J., Young, A.H. & Phillips, A.G. (2011) Glucocorticoid receptors in the prefrontal cortex regulate stress-evoked dopamine efflux and aspects of executive function. Proc Natl Acad Sci USA 108, 18459-18464.
27. Cabib, S., Ventura, R. & Puglisi-Allegra, S. (2002) Opposite imbalances between mesocortical and mesoaccumbens dopamine responses to stress by the same genotype depending on living conditions. Behav Brain Res 129, 179-185.
28. Cao, J.L., Covington, H.E., Friedman, A.K., Wilkinson, M.B., Walsh, J.J., Cooper, D.C., Nestler, E.J. & Han, M.H. (2010) Mesolimbic dopamine neurons in the brain reward circuit mediate susceptibility to social defeat and antidepressant action. J Neurosci 30, 16453-16458.
29. Carr, D.B. & Sesack, S.R. (2000a) GABA-containing neurons in the rat ventral tegmental area project to the prefrontal cortex. Synapse 38, 114-123.
30. Carr, D.B. & Sesack, S.R. (2000b) 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.
31. Chaki, S. & Okubo, T. (2007) Melanocortin-4 receptor antagonists for the treatment of depression and anxiety disorders. Curr Top Med Chem 7, 1145-1151.
32. Chang, C. & Grace, A.A. (2013) Amygdala β-noradrenergic receptors modulate delayed downregulation of dopamine activity following restraint. J Neurosci 33, 1441-1450.
33. Chaudhury, D., Walsh, J.J., Friedman, A.K., Juarez, B., Ku, S.M., Koo, J.W., Ferguson, D., Tsai, H.-C., Pomeranz, L., Christoffel, D.J., Nectow, A.R., Ekstrand, M., Domingos, A., Mazei-Robison, M.S., Mouzon, E., Lobo, M.K., Neve, R.L., Friedman, J.M., Russo, S.J., Deisseroth, K., Nestler, E.J. & Han, M.H. (2013) Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons. Nature 493, 532-536.
34. Christoph, G.R., Leonzio, R.J. & Wilcox, K.S. (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.
35. Cohen, J.Y., Haesler, S., Vong, L., Lowell, B.B. & Uchida, N. (2012) Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature 482, 85-88.
36. Covington, H.E. III, Lobo, M.K., Maze, I., Vialou, V., Hyman, J.M., Zaman, S., LaPlant, Q., Mouzon, E., Ghose, S., Tamminga, C.A., Neve, R.L., Deisseroth, K. & Nestler, E.J. (2010) Antidepressant effect of optogenetic stimulation of the medial prefrontal cortex. J Neurosci 30, 16082-16090.
37. Cryan, J.F., Markou, A. & Lucki, I. (2002a) Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci 23, 238-245.
38. Cryan, J.F., Markou, A. & Lucki, I. (2002b) Assessing antidepressant activity in rodents: recent developments and future needs. Trends Pharmacol Sci 23, 238-245.
39. Cummings, J.L. (1995) Anatomic and behavioral aspects of frontal-subcortical circuits. Ann N Y Acad Sci 769, 1-13.
40. D'Ardenne, K., McClure, S.M., Nystrom, L.E. & Cohen, J.D. (2008) BOLD responses reflecting dopaminergic signals in the human ventral tegmental area. Science 319, 1264-1267.
41. Damasio, A.R., Tranel, D. & Damasio, H. (1990) Individuals with sociopathic behavior caused by frontal damage fail to respond autonomically to social stimuli. Behav Brain Res 41, 81-94.
42. Deisseroth, K. (2011) Optogenetics. Nat Methods 8, 26-29.
43. Der-Avakian, A. & Markou, A. (2012) The neurobiology of anhedonia and other reward-related deficits. Trends Neurosci 35, 68-77.
44. Di Chiara, G., Loddo, P. & Tanda, G. (1999) Reciprocal changes in prefrontal and limbic dopamine responsiveness to aversive and rewarding stimuli after chronic mild stress: implications for the psychobiology of depression. Biol Psychiatry 46, 1624-1633.
45. Disner, S.G., Beevers, C.G., Haigh, E.A.P. & Beck, A.T. (2011) Neural mechanisms of the cognitive model of depression. Nat Rev Neurosci 12, 467-477.
46. Dostrovsky, J.O. & Lozano, A.M. (2002) Mechanisms of deep brain stimulation. Mov Disord 17 (Suppl 3), S63-S68.
47. Drevets, W.C. (1999) Prefrontal cortical-amygdalar metabolism in major depression. Ann N Y Acad Sci 877, 614-637.
48. Drevets, W.C., Price, J.L. & Furey, M.L. (2008) Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Struct Funct 213, 93-118.
49. Duffy, J.D. & Campbell, J.J. (1994) The regional prefrontal syndromes: a theoretical and clinical overview. J Neuropsychiatry Clin Neurosci 6, 379-387.
50. Dulawa, S.C., Holick, K.A., Gundersen, B. & Hen, R. (2004) Effects of chronic fluoxetine in animal models of anxiety and depression. Neuropsychopharmacology 29, 1321-1330.
51. Fesenmeier, J.T., Kuzniecky, R. & Garcia, J.H. (1990) Akinetic mutism caused by bilateral anterior cerebral tuberculous obliterative arteritis. Neurology 40, 1005-1006.
52. Fields, H.L., Hjelmstad, G.O., Margolis, E.B. & Nicola, S.M. (2007) Ventral tegmental area neurons in learned appetitive behavior and positive reinforcement. Annu Rev Neurosci 30, 289-316.
53. Fone, K.C.F. & Porkess, M.V. (2008) Behavioural and neurochemical effects of post-weaning social isolation in rodents-relevance to developmental neuropsychiatric disorders. Neurosci Biobehav Rev 32, 1087-1102.
54. Ford, C.P., Mark, G.P. & Williams, J.T. (2006) Properties and opioid inhibition of mesolimbic dopamine neurons vary according to target location. J Neurosci 26, 2788-2797.
55. Geisler, S., Derst, C., Veh, R.W. & Zahm, D.S. (2007) Glutamatergic afferents of the ventral tegmental area in the rat. J Neurosci 27, 5730-5743.
56. George, M.S., Ketter, T.A. & Post, R.M. (1994) Prefrontal cortex dysfunction in clinical depression. Depression 2, 59-72.
57. Goncalves, L., Sego, C. & Metzger, M. (2012) Differential projections from the lateral habenula to the rostromedial tegmental nucleus and ventral tegmental area in the rat. J Comp Neurol 520, 1278-1300.
58. Hamani, C., Mayberg, H., Snyder, B., Giacobbe, P., Kennedy, S. & Lozano, A.M. (2009) Deep brain stimulation of the subcallosal cingulate gyrus for depression: anatomical location of active contacts in clinical responders and a suggested guideline for targeting. J Neurosurg 111, 1209-1215.
59. Hamani, C., Diwan, M., Macedo, C.E., Brandão, M.L., Shumake, J., Gonzalez-Lima, F., Raymond, R., Lozano, A.M., Fletcher, P.J. & Nobrega, J.N. (2010a) Antidepressant-like effects of medial prefrontal cortex deep brain stimulation in rats. Biol Psychiatry 67, 117-124.
60. Hamani, C., Diwan, M., Isabella, S., Lozano, A.M. & Nobrega, J.N. (2010b) Effects of different stimulation parameters on the antidepressant-like response of medial prefrontal cortex deep brain stimulation in rats. J Psychiatr Res 44, 683-687.
61. Hamani, C., Machado, D.C., Hipólide, D.C., Dubiela, F.P., Suchecki, D., Macedo, C.E., Tescarollo, F., Martins, U., Covolan, L. & Nobrega, J.N. (2011) Deep brain stimulation reverses anhedonic-like behavior in a chronic model of depression: role of serotonin and brain derived neurotrophic factor. Biol Psychiatry 71, 30-35.
62. Henn, F.A. & Vollmayr, B. (2005) Stress models of depression: forming genetically vulnerable strains. Neurosci Biobehav Rev 29, 799-804.
63. Herkenham, M. & Nauta, W.J. (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.
64. Hikosaka, O., Sesack, S.R., Lecourtier, L. & Shepard, P.D. (2008) Habenula: crossroad between the Basal Ganglia and the Limbic System. J Neurosci 28, 11825-11829.
65. Hong, S., Jhou, T.C., Smith, M., Saleem, K.S. & Hikosaka, O. (2011) Negative reward signals from the lateral habenula to dopamine neurons are mediated by rostromedial tegmental nucleus in primates. J Neurosci 31, 11457-11471.
66. Hoover, W.B. & Vertes, R.P. (2007) Anatomical analysis of afferent projections to the medial prefrontal cortex in the rat. Brain Struct Funct 212, 149-179.
67. Hsu, R., Taylor, J.R., Newton, S.S., Alvaro, J.D., Haile, C., Han, G., Hruby, V.J., Nestler, E.J. & Duman, R.S. (2005) Blockade of melanocortin transmission inhibits cocaine reward. Eur J Neurosci 21, 2233-2242.
68. Ikemoto, S. (2007) Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res Rev 56, 27-78.
69. Ikemoto, S. & Wise, R.A. (2004) Mapping of chemical trigger zones for reward. Neuropharmacology 47 (Suppl. 1), 190-201.
70. Imperato, A., Cabib, S. & Puglisi-Allegra, S. (1993) Repeated stressful experiences differently affect the time-dependent responses of the mesolimbic dopamine system to the stressor. Brain Res 601, 333-336.
71. Itoyama, Y., Sekizawa, T., Openshaw, H., Kogure, K. & Goto, I. (1991) Early loss of astrocytes in herpes simplex virus-induced central nervous system demyelination. Ann Neurol 29, 285-292.
72. Jackson, M.E. & Moghaddam, B. (2004) Stimulus-specific plasticity of prefrontal cortex dopamine neurotransmission. J Neurochem 88, 1327-1334.
73. Jackson, M.E., Frost, A.S. & Moghaddam, B. (2001) Stimulation of prefrontal cortex at physiologically relevant frequencies inhibits dopamine release in the nucleus accumbens. J Neurochem 78, 920-923.
74. Jhou, T.C., Geisler, S., Marinelli, M., Degarmo, B.A. & Zahm, D.S. (2009a) 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.
75. Jhou, T.C., Fields, H.L., Baxter, M.G., Saper, C.B. & Holland, P.C. (2009b) The rostromedial tegmental nucleus (RMTg), a GABAergic afferent to midbrain dopamine neurons, encodes aversive stimuli and inhibits motor responses. Neuron 61, 786-800.
76. Ji, H. & Shepard, P.D. (2007) Lateral habenula stimulation inhibits rat midbrain dopamine neurons through a GABA(A) receptor-mediated mechanism. J Neurosci 27, 6923-6930.
77. Kaneyuki, H., Yokoo, H., Tsuda, A., Yoshida, M., Mizuki, Y., Yamada, M. & Tanaka, M. (1991) Psychological stress increases dopamine turnover selectively in mesoprefrontal dopamine neurons of rats: reversal by diazepam. Brain Res 557, 154-161.
78. Kaufling, J., Veinante, P., Pawlowski, S.A., 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.
79. Kessler, R.C. (1997) The effects of stressful life events on depression. Annu Rev Psychol 48, 191-214.
80. Kim, S.-Y., Adhikari, A., Lee, S.Y., Marshel, J.H., Kim, C.K., Mallory, C.S., Lo, M., Pak, S., Mattis, J., Lim, B.K., Malenka, R.C., Warden, M.R., Neve, R., Tye, K.M. & Deisseroth, K. (2013a) Diverging neural pathways assemble a behavioural state from separable features in anxiety. Nature 496, 219-223.
81. Kim, T.I., McCall, J.G., Jung, Y.H., Huang, X., Siuda, E.R., Li, Y., Song, J., Song, Y.M., Pao, H.A., Kim, R.-H. Chaofeng Lu, C., Lee, S.D, Song, I.S., Shin, G., Al-Hasani, R., Kim, S., Tan M.P., Huang, Y., Omenetto F.G., Rogers J.A. & Bruchas M.R. (2013b) Injectable, cellular-scale optoelectronics with applications for wireless optogenetics. Science 340, 211-216.
82. Kishi, T., Aschkenasi, C.J., Lee, C.E., Mountjoy, K.G., Saper, C.B. & Elmquist, J.K. (2003) Expression of melanocortin 4 receptor mRNA in the central nervous system of the rat. J Comp Neurol 457, 213-235.
83. Klimke, A., Larisch, R., Janz, A., Vosberg, H., Müller-Gärtner, H.W. & Gaebel, W. (1999a) Dopamine D2 receptor binding before and after treatment of major depression measured by [123I]IBZM SPECT. Psychiatry Res 90, 91-101.
84. Klimke, A., Larisch, R., Janz, A., Vosberg, H., Müller-Gärtner, H.-W. & Gaebel, W. (1999b) Dopamine D2 receptor binding before and after treatment of major depression measured by [123I]IBZM SPECT. Psychiat Res: Neuroim 90, 91-101.
85. Krishnan, V., Han, M.-H., Graham, D.L., Berton, O., Renthal, W., Russo, S.J., Laplant, Q., Graham, A., Lutter, M., Lagace, D.C., Ghose, S., Reister, R., Tannous, P., Green, T.A., Neve, R.L., Chakravarty, S., Kumar, A., Eisch, A.J., Self, D.W., Lee, F.S., Tamminga, C.A., Cooper, D.C., Gershenfeld, H.K. & Nestler, E.J. (2007) Molecular adaptations underlying susceptibility and resistance to social defeat in brain reward regions. Cell 131, 391-404.
86. Kumar, S., Black, S.J., Hultman, R., Szabo, S.T., DeMaio, K.D., Du, J., Katz, B.M., Feng, G., Covington, H.E. & Dzirasa, K. (2013) Cortical control of affective networks. J Neurosci 33, 1116-1129.
87. Laasonen-Balk, T., Kuikka, J., Viinamäki, H., Husso-Saastamoinen, M., Lehtonen, J. & Tiihonen, J. (1999) Striatal dopamine transporter density in major depression. Psychopharmacology (Berl) 144, 282-285.
88. Lammel, S., Hetzel, A., Hackel, O., Jones, I., Liss, B. & Roeper, J. (2008) Unique properties of mesoprefrontal neurons within a dual mesocorticolimbic dopamine system. Neuron 57, 760-773.
89. Lammel, S., Ion, D.I., Roeper, J. & Malenka, R.C. (2011) Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli. Neuron 70, 855-862.
90. Lammel, S., Lim, B.K., Ran, C., Huang, K.W., Betley, M.J., Tye, K.M., Deisseroth, K. & Malenka, R.C. (2012) Input-specific control of reward and aversion in the ventral tegmental area. Nature 491, 212-217.
91. Lammel, S., Lim, B.K. & Malenka, R.C. (2013) Reward and aversion in a heterogeneous midbrain dopamine system. Neuropharmacology, DOI:10.1016/j.neuropharm.2013.03.019.
92. Larisch, R., Klimke, A., Vosberg, H., Löffler, S., Gaebel, W. & Müller-Gärtner, H.W. (1997) In vivo evidence for the involvement of dopamine-D2 receptors in striatum and anterior cingulate gyrus in major depression. Neuroimage 5, 251-260.
93. Lecourtier, L. & Kelly, P.H. (2005) Bilateral lesions of the habenula induce attentional disturbances in rats. Neuropsychopharmacology 30, 484-496.
94. Lecourtier, L. & Kelly, P.H. (2007) A conductor hidden in the orchestra? Role of the habenular complex in monoamine transmission and cognition. Neurosci Biobehav Rev 31, 658-672.
95. 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.
96. Lee, J.H., Durand, R., Gradinaru, V., Zhang, F., Goshen, I., Kim, D.-S., Fenno, L.E., Ramakrishnan, C. & Deisseroth, K. (2010) Global and local fMRI signals driven by neurons defined optogenetically by type and wiring. Nature 465, 788-792.
97. Lemos, J.C., Wanat, M.J., Smith, J.S., Reyes, B.A.S., Hollon, N.G., Bockstaele, E.J.V., Chavkin, C. & Phillips, P.E.M. (2012) Severe stress switches CRF action in the nucleus accumbens from appetitive to aversive. Nature 490, 402-406.
98. Li, B., Piriz, J., Mirrione, M., Chung, C., Proulx, C.D., Schulz, D., Henn, F. & Malinow, R. (2011) Synaptic potentiation onto habenula neurons in the learned helplessness model of depression. Nature 470, 535-539.
99. Lim, B.K., Huang, K.W., Grueter, B.A., Rothwell, P.E. & Malenka, R.C. (2012) Anhedonia requires MC4R-mediated synaptic adaptations in nucleus accumbens. Nature 487, 183-189.
100. Malone, D.A. Jr, Dougherty, D.D., Rezai, A.R., Carpenter, L.L., Friehs, G.M., Eskandar, E.N., Rauch, S.L., Rasmussen, S.A., Machado, A.G., Kubu, C.S., Tyrka, A.R., Price, L.H., Stypulkowski, P.H., Giftakis, J.E., Rise, M.T., Malloy, P.F., Salloway, S.P. & Greenberg, B.D. (2009) Deep brain stimulation of the ventral capsule/ventral striatum for treatment-resistant depression. Biol Psychiatry 65, 267-275.
101. Manes, F., Sahakian, B., Clark, L., Rogers, R., Antoun, N., Aitken, M. & Robbins, T. (2002) Decision-making processes following damage to the prefrontal cortex. Brain 125, 624-639.
102. Mantz, J., Thierry, A.M. & Glowinski, J. (1989) Effect of noxious tail pinch on the discharge rate of mesocortical and mesolimbic dopamine neurons: selective activation of the mesocortical system. Brain Res 476, 377-381.
103. Margolis, E.B., Toy, B., Himmels, P., Morales, M. & Fields, H.L. (2012) Identification of rat ventral tegmental area GABAergic neurons. PLoS One 7, e42365.
104. Matsui, A. & Williams, J.T. (2011) Opioid-sensitive GABA Inputs from rostromedial tegmental nucleus synapse onto midbrain dopamine neurons. J Neurosci 31, 17729-17735.
105. Matsumoto, M. & Hikosaka, O. (2007) Lateral habenula as a source of negative reward signals in dopamine neurons. Nature 447, 1111-1115.
106. Matsumoto, M. & Hikosaka, O. (2009a) Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 459, 837-841.
107. Matsumoto, M. & Hikosaka, O. (2009b) Representation of negative motivational value in the primate lateral habenula. Nat Neurosci 12, 77-84.
108. Mayberg, H.S., Liotti, M., Brannan, S.K., McGinnis, S., Mahurin, R.K., Jerabek, P.A., Silva, J.A., Tekell, J.L., Martin, C.C., Lancaster, J.L. & Fox, P.T. (1999) Reciprocal limbic-cortical function and negative mood: converging PET findings in depression and normal sadness. Am J Psychiatry 156, 675-682.
109. Mayberg, H.S., Lozano, A.M., Voon, V., McNeely, H.E., Seminowicz, D., Hamani, C., Schwalb, J.M. & Kennedy, S.H. (2005) Deep brain stimulation for treatment-resistant depression. Neuron 45, 651-660.
110. Mega, M.S. & Cummings, J.L. (1994) Frontal-subcortical circuits and neuropsychiatric disorders. J Neuropsychiatry Clin Neurosci 6, 358-370.
111. Meyer, J.H., Krüger, S., Wilson, A.A., Christensen, B.K., Goulding, V.S., Schaffer, A., Minifie, C., Houle, S., Hussey, D. & Kennedy, S.H. (2001) Lower dopamine transporter binding potential in striatum during depression. Neuroreport 12, 4121-4125.
112. Mizoguchi, K., Yuzurihara, M., Ishige, A., Sasaki, H., Chui, D.H. & Tabira, T. (2000) Chronic stress induces impairment of spatial working memory because of prefrontal dopaminergic dysfunction. J Neurosci 20, 1568-1574.
113. Mizoguchi, K., Shoji, H., Ikeda, R., Tanaka, Y. & Tabira, T. (2008) Persistent depressive state after chronic stress in rats is accompanied by HPA axis dysregulation and reduced prefrontal dopaminergic neurotransmission. Pharmacol Biochem Behav 91, 170-175.
114. Moore, H., Rose, H.J. & Grace, A.A. (2001) Chronic cold stress reduces the spontaneous activity of ventral tegmental dopamine neurons. Neuropsychopharmacology 24, 410-419.
115. Morrow, B.A., Roth, R.H. & Elsworth, J.D. (2000) TMT, a predator odor, elevates mesoprefrontal dopamine metabolic activity and disrupts short-term working memory in the rat. Brain Res Bull 52, 519-523.
116. Nair-Roberts, R.G., Chatelain-Badie, S.D., Benson, E., White-Cooper, H., Bolam, J.P. & Ungless, M.A. (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.
117. Nestler, E.J. & Carlezon, W.A. (2006) The mesolimbic dopamine reward circuit in depression. Biol Psychiatry 59, 1151-1159.
118. Neve, R.L., Neve, K.A., Nestler, E.J. & Carlezon, W.A. (2005) Use of herpes virus amplicon vectors to study brain disorders. Biotechniques 39, 381-391.
119. Nieh, E.H., Kim, S.Y., Namburi, P. & Tye, K.M. (2012) Optogenetic dissection of neural circuits underlying emotional valence and motivated behaviors. Brain Res 1511, 73-92.
120. Niwa, M., Jaaro-Peled, H., Tankou, S., Seshadri, S., Hikida, T., Matsumoto, Y., Cascella, N.G., Kano, S., Ozaki, N., Nabeshima, T. & Sawa, A. (2013) Adolescent stress-induced epigenetic control of dopaminergic neurons via glucocorticoids. Science 339, 335-339.
121. O'Donnell, P. & Grace, A.A. (1995) Synaptic interactions among excitatory afferents to nucleus accumbens neurons: hippocampal gating of prefrontal cortical input. J Neurosci 15, 3622-3639.
122. Omelchenko, N., Bell, R. & Sesack, S.R. (2009) Lateral habenula projections to dopamine and GABA neurons in the rat ventral tegmental area. Eur J Neurosci 30, 1239-1250.
123. Ongür, D. & Price, J.L. (2000) The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb Cortex 10, 206-219.
124. Osakada, F., Mori, T., Cetin, A.H., Marshel, J.H., Virgen, B. & Callaway, E.M. (2011) New rabies virus variants for monitoring and manipulating activity and gene expression in defined neural circuits. Neuron 71, 617-631.
125. Pan, W.-X., Brown, J. & Dudman, J.T. (2012) Neural signals of extinction in the inhibitory microcircuit of the ventral midbrain. Nat Neurosci 16, 71-78.
126. Papp, M., Klimek, V. & Willner, P. (1994) Parallel changes in dopamine D2 receptor binding in limbic forebrain associated with chronic mild stress-induced anhedonia and its reversal by imipramine. Psychopharmacology (Berl) 115, 441-446.
127. Porsolt, R., Le Pichon, M. & Jalfre, M. (1977) Depression: a new animal model sensitive to antidepressant treatments. Nature 266, 730-732.
128. Preuss, T.M. (1995) Do rats have prefrontal cortex? The Rose-Woolsey-Akert program reconsidered. J Cogn Neurosci 7, 1-24.
129. Razzoli, M., Andreoli, M., Michielin, F., Quarta, D. & Sokal, D.M. (2011) Increased phasic activity of VTA dopamine neurons in mice 3weeks after repeated social defeat. Behav Brain Res 218, 253-257.
130. Roeper, J. (2013) Dissecting the diversity of midbrain dopamine neurons. Trends Neurosci. 36, 336-342.
131. Roseberry, A.G. (2013) Altered feeding and body weight following melanocortin administration to the ventral tegmental area in adult rats. Psychopharmacology (Berl) 226, 25-34.
132. Salamone, J.D. & Correa, M. (2012) The mysterious motivational functions of mesolimbic dopamine. Neuron 76, 470-485.
133. Sartorius, A., Mahlstedt, M.M., Vollmayr, B., Henn, F.A. & Ende, G. (2007) Elevated spectroscopic glutamate/gamma-amino butyric acid in rats bred for learned helplessness. Neuroreport 18, 1469-1473.
134. Sartorius, A., Kiening, K.L., Kirsch, P., von Gall, C.C., Haberkorn, U., Unterberg, A.W., Henn, F.A. & Meyer-Lindenberg, A. (2010) Remission of major depression under deep brain stimulation of the lateral habenula in a therapy-refractory patient. Biol Psychiatry 67, e9-e11.
135. Sasaki, T., Beppu, K., Tanaka, K.F., Fukazawa, Y., Shigemoto, R. & Matsui, K. (2012) Application of an optogenetic byway for perturbing neuronal activity via glial photostimulation. Proc Natl Acad Sci USA 109, 20720-20725.
136. Schmidt, K., Nolte-Zenker, B., Patzer, J., Bauer, M., Schmidt, L.G. & Heinz, A. (2001) Psychopathological correlates of reduced dopamine receptor sensitivity in depression, schizophrenia, and opiate and alcohol dependence. Pharmacopsychiatry 34, 66-72.
137. Schultz, W. (1997) Dopamine neurons and their role in reward mechanisms. Curr Opin Neurobiol 7, 191-197.
138. Schultz, W. (2007) Behavioral dopamine signals. Trends Neurosci 30, 203-210.
139. Schwarcz, R., Hökfelt, T., Fuxe, K., Jonsson, G., Goldstein, M. & Terenius, L. (1979) Ibotenic acid-induced neuronal degeneration: a morphological and neurochemical study. Exp Brain Res 37, 199-216.
140. Shabel, S.J., Proulx, C.D., Trias, A., Murphy, R.T. & Malinow, R. (2012) Input to the lateral habenula from the basal ganglia is excitatory, aversive, and suppressed by serotonin. Neuron 74, 475-481.
141. Shumake, J. & Gonzalez-Lima, F. (2003) Brain systems underlying susceptibility to helplessness and depression. Behav Cogn Neurosci Rev 2, 198-221.
142. Sierra-Mercado, D., Padilla-Coreano, N. & Quirk, G.J. (2011) Dissociable roles of prelimbic and infralimbic cortices, ventral hippocampus, and basolateral amygdala in the expression and extinction of conditioned fear. Neuropsychopharmacology 36, 529-538.
143. Slattery, D.A., Neumann, I.D. & Cryan, J.F. (2011) Transient inactivation of the infralimbic cortex induces antidepressant-like effects in the rat. J Psychopharmacol 25, 1295-1303.
144. Stamatakis, A.M. & Stuber, G.D. (2012) Activation of lateral habenula inputs to the ventral midbrain promotes behavioral avoidance. Nat Neurosci 15, 1105-1107.
145. Stuber, G.D., Sparta, D.R., Stamatakis, A.M., van Leeuwen, W.A., Hardjoprajitno, J.E., Cho, S., Tye, K.M., Kempadoo, K.A., Zhang, F., Deisseroth, K. & Bonci, A. (2011) Excitatory transmission from the amygdala to nucleus accumbens facilitates reward seeking. Nature 475, 377-380.
146. Tan, K.R., Yvon, C., Turiault, M., Mirzabekov, J.J., Doehner, J., Labouèbe, G., Deisseroth, K., Tye, K.M. & Lüscher, C. (2012) GABA neurons of the VTA drive conditioned place aversion. Neuron 73, 1173-1183.
147. Tanaka, K., Furuyashiki, T., Kitaoka, S., Senzai, Y., Imoto, Y., Segi-Nishida, E., Deguchi, Y., Breyer, R.M., Breyer, M.D. & Narumiya, S. (2012) Prostaglandin E2-mediated attenuation of mesocortical dopaminergic pathway is critical for susceptibility to repeated social defeat stress in mice. J Neurosci 32, 4319-4329.
148. Thierry, A.M., Tassin, J.P., Blanc, G. & Glowinski, J. (1976) Selective activation of mesocortical DA system by stress. Nature 263, 242-244.
149. Tidey, J.W. & Miczek, K.A. (1996) Social defeat stress selectively alters mesocorticolimbic dopamine release: an in vivo microdialysis study. Brain Res 721, 140-149.
150. Tsai, H.C., Zhang, F., Adamantidis, A., Stuber, G.D., Bonci, A., de Lecea, L. & Deisseroth, K. (2009) Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324, 1080-1084.
151. Tye, K.M. & Deisseroth, K. (2012) Optogenetic investigation of neural circuits underlying brain disease in animal models. Nat Rev Neurosci 13, 251-266.
152. Tye, K.M., Prakash, R., Kim, S.-Y., Fenno, L.E., Grosenick, L., Zarabi, H., Thompson, K.R., Gradinaru, V., Ramakrishnan, C. & Deisseroth, K. (2011) Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 471, 358-362.
153. Tye, K.M., Mirzabekov, J.J., Warden, M.R., Ferenczi, E.A., Tsai, H.-C., Finkelstein, J., Kim, S.-Y., Adhikari, A., Thompson, K.R., Andalman, A.S., Gunaydin, L.A., Witten, I.B. & Deisseroth, K. (2013) Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature 493, 537-541.
154. Valenti, O., Lodge, D.J. & Grace, A.A. (2011) Aversive stimuli alter ventral tegmental area dopamine neuron activity via a common action in the ventral hippocampus. J Neurosci 31, 4280-4289.
155. Valenti, O., Gill, K.M. & Grace, A.A. (2012) Different stressors produce excitation or inhibition of mesolimbic dopamine neuron activity: response alteration by stress pre-exposure. Eur J Neurosci 35, 1312-1321.
156. Venzala, E., García-García, A.L., Elizalde, N. & Tordera, R.M. (2012a) Social vs. environmental stress models of depression from a behavioural and neurochemical approach. Eur Neuropsychopharmacol, DOI:10.1016/j.euroneuro.2012.05.010.
157. Venzala, E., García-García, A.L., Elizalde, N., Delagrange, P. & Tordera, R.M. (2012b) Chronic social defeat stress model: behavioral features, antidepressant action, and interaction with biological risk factors. Psychopharmacology (Berl) 224, 313-325.
158. Vidal-Gonzalez, I., Vidal-Gonzalez, B., Rauch, S.L. & Quirk, G.J. (2006) Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear. Learn Mem 13, 728-733.
159. Vitek, J.L. (2002) Mechanisms of deep brain stimulation: excitation or inhibition. Mov Disord 17 (Suppl 3), S69-S72.
160. Voorn, P., Vanderschuren, L.J.M., Groenewegen, H.J., Robbins, T.W. & Pennartz, C.M. (2004) Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci 27, 468-474.
161. Wallace, D.L., Han, M.-H., Graham, D.L., Green, T.A., Vialou, V., Iñiguez, S.D., Cao, J.-L., Kirk, A., Chakravarty, S., Kumar, A., Krishnan, V., Neve, R.L., Cooper, D.C., Bolaños C.A., Barrot M., McClung, C.A. & Nestler, E.J. (2009) CREB regulation of nucleus accumbens excitability mediates social isolation-induced behavioral deficits. Nat Neurosci 12, 200-209.
162. Wallis, J.D. (2011) Cross-species studies of orbitofrontal cortex and value-based decision-making. Nat Neurosci 15, 1-7.
163. Warden, M.R., Selimbeyoglu, A., Mirzabekov, J.J., Lo, M., Thompson, K.R., Kim, S.-Y., Adhikari, A., Tye, K.M., Frank, L.M. & Deisseroth, K. (2012) A prefrontal cortex-brainstem neuronal projection that controls response to behavioural challenge. Nature 492, 428-432.
164. Wilkinson, L.S., Humby, T., Killcross, A.S., Torres, E.M., Everitt, B.J. & Robbins, T.W. (1998) Dissociations in dopamine release in medial prefrontal cortex and ventral striatum during the acquisition and extinction of classical aversive conditioning in the rat. Eur J Neurosci 10, 1019-1026.
165. Willner, P. (2005) Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 52, 90-110.
166. Willner, P., Towell, A., Sampson, D., Sophokleous, S. & Muscat, R. (1987) Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology (Berl) 93, 358-364.
167. Willner, P., Hale, A.S. & Argyropoulos, S. (2005) Dopaminergic mechanism of antidepressant action in depressed patients. J Affect Disord 86, 37-45.
168. Willner, P., Scheel-Krüger, J. & Belzung, C. (2012) The neurobiology of depression and antidepressant action. Neurosci Biobehav Rev, http://dx.doi.org/10.1016/j.neubiorev.2012.12.007.
169. Winter, C., Vollmayr, B., Djodari-Irani, A., Klein, J. & Sartorius, A. (2011) Pharmacological inhibition of the lateral habenula improves depressive-like behavior in an animal model of treatment resistant depression. Behav Brain Res 216, 463-465.
170. Wise, R.A. (2004) Dopamine, learning and motivation. Nat Rev Neurosci 5, 483-494.
171. Wise, S.P. (2008) Forward frontal fields: phylogeny and fundamental function. Trends Neurosci 31, 599-608.
172. Witten, I.B., Steinberg, E.E., Lee, S.Y., Davidson, T.J., Zalocusky, K.A., Brodsky, M., Yizhar, O., Cho, S.L., Gong, S., Ramakrishnan, C., Stuber, G.D., Tye, K.M., Janak, P.H. & Deisseroth, K. (2011) Recombinase-driver rat lines: tools, techniques, and optogenetic application to dopamine-mediated reinforcement. Neuron 72, 721-733.
173. Yizhar, O., Fenno, L.E., Prigge, M., Schneider, F., Davidson, T.J., O'Shea, D.J., Sohal, V.S., Goshen, I., Finkelstein, J., Paz, J.T., Stehfest, K., Fudim, R., Ramakrishnan, C., Huguenard, J.R., Hegemann, P. & Deisseroth, K. (2011) Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 477, 171-178.
174. Zamboni, G., Huey, E.D., Krueger, F., Nichelli, P.F. & Grafman, J. (2008) Apathy and disinhibition in frontotemporal dementia: Insights into their neural correlates. Neurology 71, 736-742.
175. van Zessen, R., Phillips, J.L., Budygin, E.A. & Stuber, G.D. (2012) Activation of VTA GABA neurons disrupts reward consumption. Neuron 73, 1184-1194.