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

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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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William Menegas

Center for Brain Science, Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States

Competing interests
No competing interests declared.
Joseph F Bergan

Department of Psychological and Brain Sciences, University of Massachusetts Amherst, Amherst, United States

Competing interests
Joseph F Bergan, Yoh Isogai and Joseph Bergan have filed a patent application on OptiView.
Sachie K Ogawa

RIKEN-MIT Center for Neural Circuit Genetics at the Picower Institute for Learning and Memory, Department of Biology, Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United States

Competing interests
No competing interests declared.
Yoh Isogai

Center for Brain Science, Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States

Competing interests
Yoh Isogai, Yoh Isogai and Joseph Bergan have filed a patent application on OptiView.
Kannan Umadevi Venkataraju

Cold Spring Harbor Laboratory, Cold Spring Harbor, United States

Competing interests
No competing interests declared.
Pavel Osten

Cold Spring Harbor Laboratory, Cold Spring Harbor, United States

Competing interests
No competing interests declared.
Naoshige Uchida

Center for Brain Science, Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States

Competing interests
Naoshige Uchida, Reviewing editor, eLife.
Mitsuko Watabe-Uchida

Center for Brain Science, Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States

For correspondence
mitsuko@mcb.harvard.edu

Competing interests
No competing interests declared.

Ethics

Animal experimentation: This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. All of the animals were handled according to approved Harvard animal care and use committee (IACUC) protocols (#26-03) of Harvard University. All surgery was performed under isofluorane anesthesia, and every effort was made to minimize suffering.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.