Dopamine Neurons Projecting to the Posterior Striatum Form an Anatomically Distinct Subclass

Overview

Journal Elife

Specialty Biology

Date 2015 Sep 1

PMID 26322384

Citations 168

Authors

William Menegas

Joseph F Bergan

Sachie K Ogawa

Yoh Isogai

Kannan Umadevi Venkataraju

Pavel Osten

Naoshige Uchida

Mitsuko Watabe-Uchida

Affiliations

Soon will be listed here.

Abstract

Combining rabies-virus tracing, optical clearing (CLARITY), and whole-brain light-sheet imaging, we mapped the monosynaptic inputs to midbrain dopamine neurons projecting to different targets (different parts of the striatum, cortex, amygdala, etc) in mice. We found that most populations of dopamine neurons receive a similar set of inputs rather than forming strong reciprocal connections with their target areas. A common feature among most populations of dopamine neurons was the existence of dense 'clusters' of inputs within the ventral striatum. However, we found that dopamine neurons projecting to the posterior striatum were outliers, receiving relatively few inputs from the ventral striatum and instead receiving more inputs from the globus pallidus, subthalamic nucleus, and zona incerta. These results lay a foundation for understanding the input/output structure of the midbrain dopamine circuit and demonstrate that dopamine neurons projecting to the posterior striatum constitute a unique class of dopamine neurons regulated by different inputs.

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References

Olanow C, Tatton W . Etiology and pathogenesis of Parkinson's disease. Annu Rev Neurosci. 1999; 22:123-44. DOI: 10.1146/annurev.neuro.22.1.123. View

Damier P, Hirsch E, Agid Y, Graybiel A . The substantia nigra of the human brain. II. Patterns of loss of dopamine-containing neurons in Parkinson's disease. Brain. 1999; 122 ( Pt 8):1437-48. DOI: 10.1093/brain/122.8.1437. View

Haber S, Fudge J, McFarland N . Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci. 2000; 20(6):2369-82. PMC: 6772499. View

Joel D, Weiner I . 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. 2000; 96(3):451-74. DOI: 10.1016/s0306-4522(99)00575-8. View

Zaborszky L, Vadasz C . The midbrain dopaminergic system: anatomy and genetic variation in dopamine neuron number of inbred mouse strains. Behav Genet. 2001; 31(1):47-59. DOI: 10.1023/a:1010257808945. View

Zahm D, Brog J . On the significance of subterritories in the "accumbens" part of the rat ventral striatum. Neuroscience. 1992; 50(4):751-67. DOI: 10.1016/0306-4522(92)90202-d. View

Vertes R . Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse. 2003; 51(1):32-58. DOI: 10.1002/syn.10279. View

Uylings H, Groenewegen H, Kolb B . Do rats have a prefrontal cortex?. Behav Brain Res. 2003; 146(1-2):3-17. DOI: 10.1016/j.bbr.2003.09.028. View

Goto M, Swanson L . Axonal projections from the parasubthalamic nucleus. J Comp Neurol. 2004; 469(4):581-607. DOI: 10.1002/cne.11036. View

10.

Wise R . Dopamine, learning and motivation. Nat Rev Neurosci. 2004; 5(6):483-94. DOI: 10.1038/nrn1406. View

11.

Voorn P, Vanderschuren L, Groenewegen H, Robbins T, Pennartz C . Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci. 2004; 27(8):468-74. DOI: 10.1016/j.tins.2004.06.006. View

12.

Francois C, Grabli D, McCairn K, Jan C, Karachi C, Hirsch E . Behavioural disorders induced by external globus pallidus dysfunction in primates II. Anatomical study. Brain. 2004; 127(Pt 9):2055-70. DOI: 10.1093/brain/awh239. View

13.

Berendse H, Galis-de Graaf Y, Groenewegen H . Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. J Comp Neurol. 1992; 316(3):314-47. DOI: 10.1002/cne.903160305. View

14.

Bayer H, Glimcher P . Midbrain dopamine neurons encode a quantitative reward prediction error signal. Neuron. 2005; 47(1):129-41. PMC: 1564381. DOI: 10.1016/j.neuron.2005.05.020. View

15.

Geisler S, Zahm D . Afferents of the ventral tegmental area in the rat-anatomical substratum for integrative functions. J Comp Neurol. 2005; 490(3):270-94. DOI: 10.1002/cne.20668. View

16.

Lehericy S, Benali H, Van de Moortele P, Pelegrini-Issac M, Waechter T, Ugurbil K . Distinct basal ganglia territories are engaged in early and advanced motor sequence learning. Proc Natl Acad Sci U S A. 2005; 102(35):12566-71. PMC: 1194910. DOI: 10.1073/pnas.0502762102. View

17.

Zahm D . The evolving theory of basal forebrain functional-anatomical 'macrosystems'. Neurosci Biobehav Rev. 2005; 30(2):148-72. DOI: 10.1016/j.neubiorev.2005.06.003. View

18.

Backman C, Malik N, Zhang Y, Shan L, Grinberg A, Hoffer B . Characterization of a mouse strain expressing Cre recombinase from the 3' untranslated region of the dopamine transporter locus. Genesis. 2006; 44(8):383-90. DOI: 10.1002/dvg.20228. View

19.

Redgrave P, Gurney K . The short-latency dopamine signal: a role in discovering novel actions?. Nat Rev Neurosci. 2006; 7(12):967-75. DOI: 10.1038/nrn2022. View

20.

Wickersham I, Lyon D, Barnard R, Mori T, Finke S, Conzelmann K . Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons. Neuron. 2007; 53(5):639-47. PMC: 2629495. DOI: 10.1016/j.neuron.2007.01.033. View