Dopamine neurons projecting to the posterior striatum form an anatomically distinct subclass

eLife

Volumn 4, Issue AUGUST2015, 2015, Pages

  Menegas, William ^a   Bergan, Joseph F ^a,c   Ogawa, Sachie K ^a,d   Isogai, Yoh ^a   Venkataraju, Kannan Umadevi ^b   Osten, Pavel ^b   Uchida, Naoshige ^a   Watabe Uchida, Mitsuko ^a  

^a HARVARD UNIVERSITY   (United States)

^b Simons Center for Quantitative Biology   (United States)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NITROGEN; OXYGEN; PARVOVIRUS VECTOR;

ADULT; AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CELL SUBPOPULATION; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; IMMUNOHISTOCHEMISTRY; MALE; MESENCEPHALON; MONOSYNAPTIC POTENTIAL; MOUSE; NERVE PROJECTION; NEUROANATOMICAL TRACT TRACING; NEUROIMAGING; NONHUMAN; NUCLEUS ACCUMBENS; PERFUSION; RABIES; SUBSTANTIA NIGRA PARS COMPACTA; VENTRAL STRIATUM; VENTRAL TEGMENTUM; ANATOMY AND HISTOLOGY; ANIMAL; BRAIN; NERVE TRACT; PHYSIOLOGY;

ANIMALS; BRAIN; CORPUS STRIATUM; DOPAMINERGIC NEURONS; MICE; NEURAL PATHWAYS;

EID: 84943646734     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.10032     Document Type: Article

References (110)

1. Alheid GF, Heimer L. 1988. New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience 27:1–39. doi: 10.1016/0306-4522(88)90217-5.
2. Backman CM, Malik N, Zhang Y, Shan L, Grinberg A, Hoffer BJ, Westphal H, Tomac AC. 2006. Characterization of a mouse strain expressing Cre recombinase from the 3′ untranslated region of the dopamine transporter locus. Genesis 44:383–390.
3. Bayer HM, Glimcher PW. 2005. Midbrain dopamine neurons encode a quantitative reward prediction error signal. Neuron 47:129–141. doi: 10.1016/j.neuron.2005.05.020.
4. Bayer VE, Pickel VM. 1990. Ultrastructural localization of tyrosine hydroxylase in the rat ventral tegmental area: relationship between immunolabeling density and neuronal associations. The Journal of Neuroscience 10:2996–3013.
5. Beier KT, Steinberg EE, DeLoach KE, Xie S, Miyamichi K, Schwarz L, Gao XJ, Kremer EJ, Malenka RC, Luo L. 2015. Circuit architecture of VTA dopamine neurons revealed by systematic input-output mapping. Cell 162:622–634. doi: 10.1016/j.cell.2015.07.015.
6. Belanger C, Zingler K, Young JA. 1995. Importance of cysteines in the LDLR-related domain of the subgroup A avian leukosis and sarcoma virus receptor for viral entry. Journal of Virology 69:1019–1024.
7. Benabid AL, Chabardes S, Mitrofanis J, Pollak P. 2009. Deep brain stimulation of the subthalamic nucleus for the treatment of Parkinson’s disease. The Lancet Neurology 8:67–81. doi: 10.1016/S1474-4422(08) 70291-6.
8. Berendse HW, Galis-de Graaf Y, Groenewegen HJ. 1992. Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. The Journal of Comparative Neurology 316:314–347. doi: 10.1002/cne.903160305.
9. Bjorklund A, Dunnett SB. 2007. Dopamine neuron systems in the brain: an update. Trends in Neurosciences 30:194–202.
10. Bromberg-Martin ES, Matsumoto M, Hikosaka O. 2010. Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 68:815–834. doi: 10.1016/j.neuron.2010.11.022.
11. Callaway EM, Luo L. 2015. Monosynaptic circuit tracing with glycoprotein-deleted rabies viruses. The Journal of Neuroscience 35:8979–8985. doi: 10.1523/JNEUROSCI.0409-15.2015.
12. Canteras NS, Shammah-Lagnado SJ, Silva BA, Ricardo JA. 1990. Afferent connections of the subthalamic nucleus: a combined retrograde and anterograde horseradish peroxidase study in the rat. Brain Research 513:43–59. doi: 10.1016/0006-8993(90)91087-W.
13. Castro DC, Berridge KC. 2014. Advances in the neurobiological bases for food ‘liking’ versus ‘wanting’. Physiology & Behavior 136:22–30. doi: 10.1016/j.physbeh.2014.05.022.
14. Chaudhuri KR, Odin P. 2010. The challenge of non-motor symptoms in Parkinson’s disease. Progress in Brain Research 184:325–341. doi: 10.1016/S0079-6123(10)84017-8.
15. Chung K, Deisseroth K. 2013. CLARITY for mapping the nervous system. Nature Methods 10:508–513. doi: 10.1038/nmeth.2481.
16. Clark JJ, Hollon NG, Phillips PE. 2012. Pavlovian valuation systems in learning and decision making. Current Opinion in Neurobiology 22:1054–1061. doi: 10.1016/j.conb.2012.06.004.
17. Cohen JY, Haesler S, Vong L, Lowell BB, Uchida N. 2012. Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature 482:85–88. doi: 10.1038/nature10754.
18. Cyron D, Funk M, Deletter MA, Scheufler K. 2010. Preserved cognition after deep brain stimulation (DBS) in the subthalamic area for Parkinson’s disease: a case report. Acta Neurochirurgica 152:2097–2100. doi: 10.1007/s00701-010-0755-x.
19. Damier P, Hirsch EC, Agid Y, Graybiel AM. 1999. The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson’s disease. Brain 122:1437–1448.
20. Degos B, Deniau JM, Le Cam J, Mailly P, Maurice N. 2008. Evidence for a direct subthalamo-cortical loop circuit in the rat. The European Journal of Neuroscience 27:2599–2610. doi: 10.1111/j.1460-9568.2008.06229.x.
21. Deniau JM, Degos B, Bosch C, Maurice N. 2010. Deep brain stimulation mechanisms: beyond the concept of local functional inhibition. The European Journal of Neuroscience 32:1080–1091. doi: 10.1111/j.1460-9568.2010.07413.x.
22. Denk W, Briggman KL, Helmstaedter M. 2012. Structural neurobiology: missing link to a mechanistic understanding of neural computation. Nature Reviews Neuroscience 13:351–358. doi: 10.1038/nrn3169.
23. Doya K. 2008. Modulators of decision making. Nature Neuroscience 11:410–416. doi: 10.1038/nn2077.
24. Fallon JH, Loughlin SE. 1982. Monoamine innervation of the forebrain: collateralization. Brain Research Bulletin 9:295–307. doi: 10.1016/0361-9230(82)90143-5.
25. Fallon JH, Riley JN, Moore RY. 1978. Substantia nigra dopamine neurons: separate populations project to neostriatum and allocortex. Neuroscience Letters 7:157–162. doi: 10.1016/0304-3940(78)90160-X.
26. Fearnley JM, Lees AJ. 1991. Ageing and Parkinson’s disease: substantia nigra regional selectivity. Brain 114:2283–2301.
27. Febvret A, Berger B, Gaspar P, Verney C. 1991. Further indication that distinct dopaminergic subsets project to the rat cerebral cortex: lack of colocalization with neurotensin in the superficial dopaminergic fields of the anterior cingulate, motor, retrosplenial and visual cortices. Brain Research 547:37–52. doi: 10.1016/0006-8993(91)90572-D.
28. 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. doi: 10.1016/j.neuroscience.2008.02.003.
29. Fiorillo CD. 2013. Two dimensions of value: dopamine neurons represent reward but not aversiveness. Science 341:546–549. doi: 10.1126/science.1238699.
30. Fiorillo CD, Song MR, Yun SR. 2013a. Multiphasic temporal dynamics in responses of midbrain dopamine neurons to appetitive and aversive stimuli. The Journal of Neuroscience 33:4710–4725. doi: 10.1523/JNEUROSCI.3883-12.2013.
31. Fiorillo CD, Yun SR, Song MR. 2013b. Diversity and homogeneity in responses of midbrain dopamine neurons. The Journal of Neuroscience 33:4693–4709. doi: 10.1523/JNEUROSCI.3886-12.2013.
32. Francois C, Grabli D, McCairn K, Jan C, Karachi C, Hirsch EC, Feger J, Tremblay L. 2004. Behavioural disorders induced by external globus pallidus dysfunction in primates II. Anatomical study. Brain 127:2055–2070.
33. Francois C, Yelnik J, Percheron G, Fenelon G. 1994. Topographic distribution of the axonal endings from the sensorimotor and associative striatum in the macaque pallidum and substantia nigra. Experimental Brain Research 102:305–318.
34. Franklin BJ, Paxinos G. 2008. The mouse brain in stereotaxic coordinates. California: Academic.
35. Frost JJ, Rosier AJ, Reich SG, Smith JS, Ehlers MD, Snyder SH, Ravert HT, Dannals RF. 1993. Positron emission tomographic imaging of the dopamine transporter with 11C-WIN 35,428 reveals marked declines in mild Parkinson’s disease. Annals of Neurology 34:423–431. doi: 10.1002/ana.410340331.
36. Geisler S, Derst C, Veh RW, Zahm DS. 2007. Glutamatergic afferents of the ventral tegmental area in the rat. The Journal of Neuroscience 27:5730–5743. doi: 10.1523/JNEUROSCI.0012-07.2007.
37. Geisler S, Zahm DS. 2005. Afferents of the ventral tegmental area in the rat-anatomical substratum for integrative functions. The Journal of Comparative Neurology 490:270–294. doi: 10.1002/cne.20668.
38. Goto M, Swanson LW. 2004. Axonal projections from the parasubthalamic nucleus. The Journal of Comparative Neurology 469:581–607. doi: 10.1002/cne.11036.
39. Haber SN. 2014. The place of dopamine in the cortico-basal ganglia circuit. Neuroscience 282C:248–257. doi: 10.1016/j.neuroscience.2014.10.008.
40. Haber SN, Fudge JL, McFarland NR. 2000. Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. The Journal of Neuroscience 20:2369–2382.
41. Hart AS, Rutledge RB, Glimcher PW, Phillips PE. 2014. Phasic dopamine release in the rat nucleus accumbens symmetrically encodes a reward prediction error term. The Journal of Neuroscience 34:698–704. doi: 10.1523/JNEUROSCI.2489-13.2014.
42. Houk JC, Adams JL. 1995. A model of how the basal ganglia generate and use neural signals that. Models of Information Processing in the Basal Ganglia 249.
43. Huang ZJ, Zeng H. 2013. Genetic approaches to neural circuits in the mouse. Annual Review of Neuroscience 36:183–215. doi: 10.1146/annurev-neuro-062012-170307.
44. Ikemoto S. 2007. Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Research Reviews 56:27–78. doi: 10.1016/j.brainresrev.2007.05.004.
45. Isogai Y, Richardson D, Dulac C, Bergan JF. Optimized protocol for imaging cleared neural issues using light microscopy. Methods in Molecular Biology. Springer. in press.
46. Jhou TC, Geisler S, Marinelli M, Degarmo BA, Zahm DS. 2009. 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. The Journal of Comparative Neurology 513:566–596. doi: 10.1002/cne.21891.
47. Joel D, Weiner I. 2000. The connections of the dopaminergic system with the striatum in rats and primates: an analysis with respect to the functional and compartmental organization of the striatum. Neuroscience 96:451–474. doi: 10.1016/S0306-4522(99)00575-8.
48. Keller PJ, Schmidt AD, Santella A, Khairy K, Bao Z, Wittbrodt J, Stelzer EH. 2010. Fast, high-contrast imaging of animal development with scanned light sheet-based structured-illumination microscopy. Nature Methods 7:637–642. doi: 10.1038/nmeth.1476.
49. KhamassiM, Humphries MD. 2012. Integrating cortico-limbic-basal ganglia architectures for learning model-based and model-free navigation strategies. Frontiers in Behavioral Neuroscience 6:79. doi: 10.3389/fnbeh.2012.00079.
50. Kim HF, Ghazizadeh A, Hikosaka O. 2014. Separate groups of dopamine neurons innervate caudate head and tail encoding flexible and stable value memories. Frontiers in Neuroanatomy 8:120. doi: 10.3389/fnana.2014.00120.
51. Kim HF, Hikosaka O. 2013. Distinct basal ganglia circuits controlling behaviors guided by flexible and stable values. Neuron 79:1001–1010. doi: 10.1016/j.neuron.2013.06.044.
52. Kish SJ, Shannak K, Hornykiewicz O. 1988. Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson’s disease. Pathophysiologic and clinical implications. The New England Journal of Medicine 318:876–880. doi: 10.1056/NEJM198804073181402.
53. Kita H, Kitai ST. 1987. Efferent projections of the subthalamic nucleus in the rat: light and electron microscopic analysis with the PHA-L method. The Journal of Comparative Neurology 260:435–452. doi: 10.1002/cne. 902600309.
54. Kita T, Osten P, Kita H. 2014. Rat subthalamic nucleus and zona incerta share extensively overlapped representations of cortical functional territories. The Journal of Comparative Neurology 522:4043–4056. doi: 10. 1002/cne.23655.
55. Klein S, Staring M, Murphy K, Viergever MA, Pluim JP. 2010. elastix: a toolbox for intensity-based medical image registration. IEEE Transactions on Medical Imaging 29:196–205. doi: 10.1109/TMI.2009.2035616.
56. Kobayashi Y, Okada K. 2007. Reward prediction error computation in the pedunculopontine tegmental nucleus neurons. Annals of the New York Academy of Sciences 1104:310–323. doi: 10.1196/annals.1390.003.
57. 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. doi: 10.1016/j.neuron.2008.01.022.
58. Lammel S, Ion DI, Roeper J, Malenka RC. 2011. Projection-specific modulation of dopamine neuron synapses by aversive and rewarding stimuli. Neuron 70:855–862. doi: 10.1016/j.neuron.2011.03.025.
59. Lammel S, Lim BK, Malenka RC. 2014. Reward and aversion in a heterogeneous midbrain dopamine system. Neuropharmacology 76:351–359. doi: 10.1016/j.neuropharm.2013.03.019.
60. Lammel S, Lim BK, Ran C, Huang KW, Betley MJ, Tye KM, Deisseroth K, Malenka RC. 2012. Input-specific control of reward and aversion in the ventral tegmental area. Nature 491:212–217. doi: 10.1038/nature11527.
61. Lehericy S, Benali H, Van de Moortele PF, Pelegrini-Issac M, Waechter T, Ugurbil K, Doyon J. 2005. Distinct basal ganglia territories are engaged in early and advanced motor sequence learning. Proceedings of the National Academy of Sciences of USA 102:12566–12571. doi: 10.1073/pnas.0502762102.
62. Lerner TN, Shilyansky C, Davidson TJ, Evans KE, Beier KT, Zalocusky KA, Crow AK, Malenka RC, Luo L, Tomer R, Deisseroth K. 2015. Intact-brain analyses reveal distinct information carried by SNc dopamine subcircuits. Cell 162:635–647. doi: 10.1016/j.cell.2015.07.014.
63. Loughlin SE, Fallon JH. 1984. Substantia nigra and ventral tegmental area projections to cortex: topography and collateralization. Neuroscience 11:425–435. doi: 10.1016/0306-4522(84)90034-4.
64. Lynd-Balta E, Haber SN. 1994. Primate striatonigral projections: a comparison of the sensorimotor-related striatum and the ventral striatum. The Journal of Comparative Neurology 345:562–578. doi: 10.1002/cne.903450407.
65. Maco B, Cantoni M, Holtmaat A, Kreshuk A, Hamprecht FA, Knott GW. 2014. Semiautomated correlative 3D electron microscopy of in vivo-imaged axons and dendrites. Nature Protocols 9:1354–1366. doi: 10.1038/nprot.2014.101.
66. Matsuda W, Furuta T, Nakamura KC, Hioki H, Fujiyama F, Arai R, Kaneko T. 2009. Single nigrostriatal dopaminergic neurons form widely spread and highly dense axonal arborizations in the neostriatum. The Journal of Neuroscience 29:444–453. doi: 10.1523/JNEUROSCI.4029-08.2009.
67. Matsumoto M, Hikosaka O. 2009. Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 459:837–841.
68. Metz CT, Klein S, Schaap M, van Walsum T, Niessen WJ. 2011. Nonrigid registration of dynamic medical imaging data using nD + t B-splines and a groupwise optimization approach. Medical Image Analysis 15:238–249. doi: 10.1016/j.media.2010.10.003.
69. Miyachi S, Hikosaka O, Miyashita K, Karadi Z, Rand MK. 1997. Differential roles of monkey striatum in learning of sequential hand movement. Experimental Brain Research 115:1–5. doi: 10.1007/PL00005669.
70. Moore RY, Bloom FE. 1978. Central catecholamine neuron systems: anatomy and physiology of the dopamine systems. Annual Review of Neuroscience 1:129–169. doi: 10.1146/annurev.ne.01.030178.001021.
71. Morrish PK, Sawle GV, Brooks DJ. 1995. Clinical and [18F] dopa PET findings in early Parkinson’s disease. Journal of Neurology, Neurosurgery, and Psychiatry 59:597–600.
72. Ogawa SK, Cohen JY, Hwang D, Uchida N, Watabe-Uchida M. 2014. Organization of monosynaptic inputs to the serotonin and dopamine neuromodulatory systems. Cell Reports 8:1105–1118. doi: 10.1016/j.celrep.2014.06.042.
73. Oh SW, Harris JA, Ng L, Winslow B, Cain N, Mihalas S, Wang Q, Lau C, Kuan L, Henry AM, Mortrud MT, Ouellette B, Nguyen TN, Sorensen SA, Slaughterbeck CR, Wakeman W, Li Y, Feng D, Ho A, Nicholas E, Hirokawa KE, Bohn P, Joines KM, Peng H, Hawrylycz MJ, Phillips JW, Hohmann JG, Wohnoutka P, Gerfen CR, Koch C, Bernard A, Dang C, Jones AR, Zeng H. 2014. A mesoscale connectome of the mouse brain. Nature 508:207–214. doi: 10.1038/nature13186.
74. Olanow CW, Tatton WG. 1999. Etiology and pathogenesis of Parkinson’s disease. Annual Review of Neuroscience 22:123–144. doi: 10.1146/annurev.neuro.22.1.123.
75. Osten P, Margrie TW. 2013. Mapping brain circuitry with a light microscope. Nature Methods 10:515–523. doi: 10.1038/nmeth.2477.
76. Pavese N, Brooks DJ. 2009. Imaging neurodegeneration in Parkinson’s disease. Biochimica et Biophysica Acta 1792:722–729. doi: 10.1016/j.bbadis.2008.10.003.
77. Pennartz CM, Groenewegen HJ, Lopes da Silva FH. 1994. The nucleus accumbens as a complex of functionally distinct neuronal ensembles: an integration of behavioural, electrophysiological and anatomical data. Progress in Neurobiology 42:719–761. doi: 10.1016/0301-0082(94)90025-6.
78. Pollak Dorocic I, Furth D, Xuan Y, Johansson Y, Pozzi L, Silberberg G, Carlen M, Meletis K. 2014. A whole-brain atlas of inputs to serotonergic neurons of the dorsal and median raphe nuclei. Neuron 83:663–678. doi: 10.1016/j.neuron.2014.07.002.
79. Ponce FA, Lozano AM. 2010. Deep brain stimulation state of the art and novel stimulation targets. Progress in Brain Research 184:311–324. doi: 10.1016/S0079-6123(10)84016-6.
80. Preuss TM. 1995. Do rats have prefrontal cortex? the rose-woolsey-akert program reconsidered. Journal of Cognitive Neuroscience 7:1–24. doi: 10.1162/jocn.1995.7.1.1.
81. Ragan T, Kadiri LR, Venkataraju KU, Bahlmann K, Sutin J, Taranda J, Arganda-Carreras I, Kim Y, Seung HS, Osten P. 2012. Serial two-photon tomography for automated ex vivo mouse brain imaging. Nature Methods 9:255–258. doi: 10.1038/nmeth.1854.
82. Rao RP. 2010. Decision making under uncertainty: a neural model based on partially observable markov decision processes. Frontiers in Computational Neuroscience 4:146. doi: 10.3389/fncom.2010.00146.
83. Redgrave P, Gurney K. 2006. The short-latency dopamine signal: a role in discovering novel actions? Nature Reviews Neuroscience 7:967–975. doi: 10.1038/nrn2022.
84. Redgrave P, Rodriguez M, Smith Y, Rodriguez-Oroz MC, Lehericy S, Bergman H, Agid Y, DeLong MR, Obeso JA. 2010. Goal-directed and habitual control in the basal ganglia: implications for Parkinson’s disease. Nature Reviews Neuroscience 11:760–772. doi: 10.1038/nrn2915.
85. Renier N, Wu Z, Simon DJ, Yang J, Ariel P, Tessier-Lavigne M. 2014. iDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging. Cell 159:896–910.
86. Rodriguez MC, Obeso JA, Olanow CW. 1998. Subthalamic nucleus-mediated excitotoxicity in Parkinson’s disease: a target for neuroprotection. Annals of Neurology 44:S175–S188. doi: 10.1002/ana.410440726.
87. Roitman MF, Wheeler RA, Wightman RM, Carelli RM. 2008. Real-time chemical responses in the nucleus accumbens differentiate rewarding and aversive stimuli. Nature Neuroscience 11:1376–1377. doi: 10.1038/nn.2219.
88. Schultz W. 2007. Multiple dopamine functions at different time courses. Annual Review of Neuroscience 30:259–288. doi: 10.1146/annurev.neuro.28.061604.135722.
89. Schultz W. 2015. Neuronal reward and decision signals: from theories to data. Physiological Reviews 95:853–951. doi: 10.1152/physrev.00023.2014.
90. Schultz W, Dayan P, Montague PR. 1997. A neural substrate of prediction and reward. Science 275:1593–1599. doi: 10.1126/science.275.5306.1593.
91. Sobel E, Corbett D. 1984. Axonal branching of ventral tegmental and raphe projections to the frontal cortex in the rat. Neuroscience Letters 48:121–125. doi: 10.1016/0304-3940(84)90006-5.
92. Sommer C, Straehle C, Koethe U, Hamprecht F. 2011. ilastik: Interactive learning and segmentation toolkit. Paper presented at: Biomedical Imaging: From Nano to Macro, 2011 IEEE International Symposium on (IEEE).
93. Subach OM, Gundorov IS, Yoshimura M, Subach FV, Zhang J, Gruenwald D, Souslova EA, Chudakov DM, Verkhusha VV. 2008. Conversion of red fluorescent protein into a bright blue probe. Chemistry & Biology 15:1116–1124. doi: 10.1016/j.chembiol.2008.08.006.
94. Susaki EA, Tainaka K, Perrin D, Kishino F, Tawara T, Watanabe TM, Yokoyama C, Onoe H, Eguchi M, Yamaguchi S, Abe T, Kiyonari H, Shimizu Y, Miyawaki A, Yokota H, Ueda HR. 2014. Whole-brain imaging with single-cell resolution using chemical cocktails and computational analysis. Cell 157:726–739. doi: 10.1016/j.cell.2014.03.042.
95. 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 Research Bulletin 9:321–353. doi: 10.1016/0361-9230(82)90145-9.
96. Takada M, Hattori T. 1986. Collateral projections from the substantia nigra to the cingulate cortex and striatum in the rat. Brain Research 380:331–335. doi: 10.1016/0006-8993(86)90230-1.
97. Tomer R, Ye L, Hsueh B, Deisseroth K. 2014. Advanced CLARITY for rapid and high-resolution imaging of intact tissues. Nature Protocols 9:1682–1697. doi: 10.1038/nprot.2014.123.
98. Uylings HB, Groenewegen HJ, Kolb B. 2003. Do rats have a prefrontal cortex? Behavioural Brain Research 146:3–17. doi: 10.1016/j.bbr.2003.09.028.
99. Vertes RP. 2004. Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51:32–58. doi: 10.1002/syn.10279.
100. 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. doi: 10.1016/j.neuron.2011.05.028.
101. Voorn P, Vanderschuren LJ, Groenewegen HJ, Robbins TW, Pennartz CM. 2004. Putting a spin on the dorsalventral divide of the striatum. Trends in Neurosciences 27:468–474. doi: 10.1016/j.tins.2004.06.006.
102. Watabe-Uchida M, Zhu L, Ogawa SK, Vamanrao A, Uchida N. 2012. Whole-brain mapping of direct inputs to midbrain dopamine neurons. Neuron 74:858–873. doi: 10.1016/j.neuron.2012.03.017.
103. Weissbourd B, Ren J, DeLoach KE, Guenthner CJ, Miyamichi K, Luo L. 2014. Presynaptic partners of dorsal raphe serotonergic and GABAergic neurons. Neuron 83:645–662. doi: 10.1016/j.neuron.2014.06.024.
104. Wickersham IR, Lyon DC, Barnard RJ, Mori T, Finke S, Conzelmann KK, Young JA, Callaway EM. 2007. Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons. Neuron 53:639–647. doi: 10.1016/j.neuron.2007.01.033.
105. Wise RA. 2004. Dopamine, learning and motivation. Nature Reviews Neuroscience 5:483–494. doi: 10.1038/nrn1406.
106. Yang B, Treweek JB, Kulkarni RP, Deverman BE, Chen CK, Lubeck E, Shah S, Cai L, Gradinaru V. 2014. Single-cell phenotyping within transparent intact tissue through whole-body clearing. Cell 158:945–958. doi: 10.1016/j.cell.2014.07.017.
107. Yetnikoff L, Lavezzi HN, Reichard RA, Zahm DS. 2014. An update on the connections of the ventral mesencephalic dopaminergic complex. Neuroscience 282C:23–48. doi: 10.1016/j.neuroscience.2014.04.010.
108. Zaborszky L, Vadasz C. 2001. The midbrain dopaminergic system: anatomy and genetic variation in dopamine neuron number of inbred mouse strains. Behavior Genetics 31:47–59. doi: 10.1023/A:1010257808945.
109. Zahm DS. 2006. The evolving theory of basal forebrain functional-anatomical ‘macrosystems’. Neuroscience and Biobehavioral Reviews 30:148–172. doi: 10.1016/j.neubiorev.2005.06.003.
110. Zahm DS, Brog JS. 1992. On the significance of subterritories in the ‘accumbens’ part of the rat ventral striatum. Neuroscience 50:751–767. doi: 10.1016/0306-4522(92)90202-D.