A comprehensive excitatory input map of the striatum reveals novel functional organization

Abstract

The striatum integrates excitatory inputs from the cortex and the thalamus to control diverse functions. Although the striatum is thought to consist of sensorimotor, associative and limbic domains, their precise demarcations and whether additional functional subdivisions exist remain unclear. How striatal inputs are differentially segregated into each domain is also poorly understood. This study presents a comprehensive map of the excitatory inputs to the mouse striatum. The input patterns reveal boundaries between the known striatal domains. The most posterior striatum likely represents a novel functional subdivision, and the dorsomedial striatum integrates highly heterogeneous, multimodal inputs. The complete thalamo-cortico-striatal circuit loop is also presented, which reveals that the thalamic subregions innervated by the basal ganglia preferentially interconnect with motor-related cortical areas. Optogenetic experiments show the subregion-specific heterogeneity in the synaptic properties of striatal inputs from both the cortex and the thalamus. This projectome will guide functional studies investigating diverse striatal functions.

Data availability

The following previously published data sets were used
    1. Barbara Hunnicutt
    2. Brian Long
    3. Deniz Kusefoglu
    4. Katrina Gertz
    5. Haining Zhong
    6. Tianyi Mao
    (2014) Thalamus-whole brain projection dataset
    Downsized images are freely available for download. Full size images are available from T. Mao lab upon request.

Article and author information

Author details

  1. Barbara J Hunnicutt

    Vollum Institute, Oregon Health and Science University, Portland, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Bart C Jongbloets

    Vollum Institute, Oregon Health and Science University, Portland, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. William T Birdsong

    Vollum Institute, Oregon Health and Science University, Portland, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Katrina J Gertz

    Vollum Institute, Oregon Health and Science University, Portland, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Haining Zhong

    Vollum Institute, Oregon Health and Science University, Portland, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7109-4724
  6. Tianyi Mao

    Vollum Institute, Oregon Health and Science University, Portland, United States
    For correspondence
    mao@ohsu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3532-8319

Funding

National Institute of Neurological Disorders and Stroke (R01NS081071)

  • Tianyi Mao

National Institute of Mental Health (DP2OD008425)

  • Haining Zhong

National Science Foundation

  • Barbara J Hunnicutt

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All animal experiments were conducted according to National Institutes of Health guidelines for animal research and were approved by the Institutional Animal Care and Use Committee (IACUC protocol number: IS00003542).

Copyright

© 2016, Hunnicutt 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. Barbara J Hunnicutt
  2. Bart C Jongbloets
  3. William T Birdsong
  4. Katrina J Gertz
  5. Haining Zhong
  6. Tianyi Mao
(2016)
A comprehensive excitatory input map of the striatum reveals novel functional organization
eLife 5:e19103.
https://doi.org/10.7554/eLife.19103

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https://doi.org/10.7554/eLife.19103