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Two-photon imaging in mice shows striosomes and matrix have overlapping but differential reinforcement-related responses

  1. Bernard Bloem
  2. Rafiq Huda
  3. Mriganka Sur
  4. Ann M Graybiel  Is a corresponding author
  1. Massachusetts Institute of Technology, United States
Research Article
  • Cited 35
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Cite this article as: eLife 2017;6:e32353 doi: 10.7554/eLife.32353

Abstract

Despite the discovery of striosomes several decades ago, technical hurdles have hampered the study of the functions of these striatal compartments. Here we used 2-photon calcium imaging in neuronal birthdate-labeled Mash1-CreER;Ai14 mice to image simultaneously the activity of striosomal and matrix neurons as mice performed an auditory conditioning task. With this method, we were able to identify circumscribed zones of tdTomato-labeled neuropil that correspond to striosomes as verified immunohistochemically. Neurons in both striosomes and matrix responded to reward-predicting cues and were active during or after consummatory licking. However, we found quantitative differences in response strength: striosomal neurons fired more to reward-predicting cues and encoded more information about expected outcome as mice learned the task, whereas matrix neurons were more strongly modulated by recent reward history. These findings open the possibility of harnessing in vivo imaging to determine the contributions of striosomes and matrix to striatal circuit function.

Article and author information

Author details

  1. Bernard Bloem

    McGovern Institute for Brain Reseach, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Rafiq Huda

    Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Mriganka Sur

    Department of Brain and Cognitive Sciences, Massachusetts Institute of Technology, Cambridge, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Ann M Graybiel

    McGovern Institute for Brain Reseach, Massachusetts Institute of Technology, Cambridge, United States
    For correspondence
    graybiel@MIT.EDU
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9197-7711

Funding

Simons Foundation (306140)

  • Ann M Graybiel

National Science Foundation (EF1451125)

  • Mriganka Sur

Simons Foundation Autism Research Initiative

  • Mriganka Sur

National Eye Institute (F32 EY024857)

  • Rafiq Huda

National Institute of Mental Health (K99 MH112855)

  • Rafiq Huda

Nancy Lurie Marks Family Foundation

  • Ann M Graybiel

William N. & Bernice E. Bumpus foundation (RRDA pilot 2013.1)

  • Ann M Graybiel

William N. & Bernice E. Bumpus foundation

  • Bernard Bloem

National Institute of Mental Health (R01 MH060379)

  • Ann M Graybiel

Saks Kavanaugh Foundation

  • Ann M Graybiel

Bachmann-Strauss Dystonia and Parkinson Foundation

  • Ann M Graybiel

Netherlands Organization for Scientific Research - Rubicon

  • Bernard Bloem

National Institute of Neurological Disorders and Stroke (U01 NS090473)

  • Mriganka Sur

National Eye Institute (R01 EY007023)

  • Mriganka Sur

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 experiments were conducted in accordance with the National Institute of Health guidelines and with the approval of the Committee on Animal Care at the Massachusetts Institute of Technology (protocol #: 1114-122-17).

Reviewing Editor

  1. Geoffrey Schoenbaum, NIDA, United States

Publication history

  1. Received: September 28, 2017
  2. Accepted: December 16, 2017
  3. Accepted Manuscript published: December 18, 2017 (version 1)
  4. Version of Record published: January 11, 2018 (version 2)

Copyright

© 2017, Bloem 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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