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

  1. William Menegas
  2. Joseph F Bergan
  3. Sachie K Ogawa
  4. Yoh Isogai
  5. Kannan Umadevi Venkataraju
  6. Pavel Osten
  7. Naoshige Uchida
  8. Mitsuko Watabe-Uchida  Is a corresponding author
  1. Harvard University, United States
  2. University of Massachusetts Amherst, United States
  3. Massachusetts Institute of Technology, United States
  4. Cold Spring Harbor Laboratory, United States

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.

Article and author information

Author details

  1. William Menegas

    Center for Brain Science, Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States
    Competing interests
    No competing interests declared.
  2. 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.
  3. 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.
  4. 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.
  5. Kannan Umadevi Venkataraju

    Cold Spring Harbor Laboratory, Cold Spring Harbor, United States
    Competing interests
    No competing interests declared.
  6. Pavel Osten

    Cold Spring Harbor Laboratory, Cold Spring Harbor, United States
    Competing interests
    No competing interests declared.
  7. Naoshige Uchida

    Center for Brain Science, Department of Molecular and Cellular Biology, Harvard University, Cambridge, United States
    Competing interests
    Naoshige Uchida, Reviewing editor, eLife.
  8. 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.

Reviewing Editor

  1. Sacha B Nelson, Brandeis University, United States

Publication history

  1. Received: July 11, 2015
  2. Accepted: August 28, 2015
  3. Accepted Manuscript published: August 31, 2015 (version 1)
  4. Version of Record published: October 9, 2015 (version 2)

Copyright

© 2015, Menegas et al.

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.

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  1. William Menegas
  2. Joseph F Bergan
  3. Sachie K Ogawa
  4. Yoh Isogai
  5. Kannan Umadevi Venkataraju
  6. Pavel Osten
  7. Naoshige Uchida
  8. Mitsuko Watabe-Uchida
(2015)
Dopamine neurons projecting to the posterior striatum form an anatomically distinct subclass
eLife 4:e10032.
https://doi.org/10.7554/eLife.10032
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