Medium spiny neurons activity reveals the discrete segregation of mouse dorsal striatum

  1. Javier Alegre-Cortés
  2. María Sáez
  3. Roberto Montanari
  4. Ramon Reig  Is a corresponding author
  1. Instituto de Neurociencias CSIC-UMH, Spain

Abstract

Behavioural studies differentiate the rodent dorsal striatum (DS) into lateral and medial regions; however, anatomical evidence suggests that it is a unified structure. To understand striatal dynamics and basal ganglia functions, it is essential to clarify the circuitry that supports this behavioural-based segregation. Here, we show that the mouse DS is made of two non-overlapping functional circuits divided by a boundary. Combining in vivo optopatch-clamp and extracellular recordings of spontaneous and evoked sensory activity, we demonstrate different coupling of lateral and medial striatum to the cortex together with an independent integration of the spontaneous activity, due to particular corticostriatal connectivity and local attributes of each region. Additionally, we show differences in slow and fast oscillations and in the electrophysiological properties between striatonigral and striatopallidal neurons. In summary, these results demonstrate that the rodent DS is segregated in two neuronal circuits, in homology with the caudate and putamen nuclei of primates.

Data availability

All data generated during and/or analysed during the current study, as well as the required code to reproduce the figures, is available on the CSIC public repository. This is the URL access http://dx.doi.org/10.20350/digitalCSIC/13750.

The following data sets were generated

Article and author information

Author details

  1. Javier Alegre-Cortés

    Cellular and Systems Neurobiology, Instituto de Neurociencias CSIC-UMH, San Juan de Alicante, Spain
    Competing interests
    The authors declare that no competing interests exist.
  2. María Sáez

    Cellular and Systems Neurobiology, Instituto de Neurociencias CSIC-UMH, San Juan de Alicante, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9137-6692
  3. Roberto Montanari

    Cellular and Systems Neurobiology, Instituto de Neurociencias CSIC-UMH, San Juan de Alicante, Spain
    Competing interests
    The authors declare that no competing interests exist.
  4. Ramon Reig

    Cellular and Systems Neurobiology, Instituto de Neurociencias CSIC-UMH, San Juan de Alicante, Spain
    For correspondence
    ramon.reig@umh.es
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6475-4181

Funding

Ministerio de Economía, Industria y Competitividad, Gobierno de España (BFU2014-60809-IN)

  • Ramon Reig

Ministerio de Economía, Industria y Competitividad, Gobierno de España (SEV-2013-0317 and SEV-2017-0723)

  • Ramon Reig

Ministerio de Economía, Industria y Competitividad, Gobierno de España (SEV2013-0317)

  • María Sáez

Fundacion la Caixa (2016/00006/001)

  • Roberto Montanari

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 the experimental procedures were conformed to the directive 2010/63/EU of the European Parliament and the RD 53/2013 Spanish regulation on the protection of animals use for scientific purposes, approved by the government of the Autonomous Community of Valencia, under the supervision of the Consejo Superior de Investigaciones Científicas and the Miguel Hernandez University Committee for Animal use in Laboratory.

Reviewing Editor

  1. Olivier J Manzoni, Aix-Marseille University, INSERM, INMED, France

Publication history

  1. Received: September 27, 2020
  2. Accepted: February 15, 2021
  3. Accepted Manuscript published: February 18, 2021 (version 1)
  4. Version of Record published: March 2, 2021 (version 2)

Copyright

© 2021, Alegre-Cortés 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.

Metrics

  • 3,125
    Page views
  • 411
    Downloads
  • 2
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Javier Alegre-Cortés
  2. María Sáez
  3. Roberto Montanari
  4. Ramon Reig
(2021)
Medium spiny neurons activity reveals the discrete segregation of mouse dorsal striatum
eLife 10:e60580.
https://doi.org/10.7554/eLife.60580
  1. Further reading

Further reading

    1. Cell Biology
    2. Neuroscience
    Alessandro Dema, Rabab A Charafeddine ... Torsten Wittmann
    Research Article

    A challenge in analyzing dynamic intracellular cell biological processes is the dearth of methodologies that are sufficiently fast and specific to perturb intracellular protein activities. We previously developed a light-sensitive variant of the microtubule plus end tracking protein EB1 by inserting a blue light-controlled protein dimerization module between functional domains. Here, we describe an advanced method to replace endogenous EB1 with this light-sensitive variant in a single genome editing step, thereby enabling this approach in human induced pluripotent stem cells (hiPSCs) and hiPSC-derived neurons. We demonstrate that acute and local optogenetic EB1 inactivation in developing cortical neurons induces microtubule depolymerization in the growth cone periphery and subsequent neurite retraction. In addition, advancing growth cones are repelled from areas of blue light exposure. These phenotypes were independent of the neuronal EB1 homolog EB3, revealing a direct dynamic role of EB1-mediated microtubule plus end interactions in neuron morphogenesis and neurite guidance.

    1. Neuroscience
    Yiya Chen, Yige Gao ... Jiawei Zhou
    Research Article

    The adult human visual system maintains the ability to be altered by sensory deprivation. What has not been considered is whether the internal neural states modulate visual sensitivity to short-term monocular deprivation. In this study we manipulated the internal neural state and reported changes in intrinsic neural oscillations with a patched eye open or closed. We investigated the influence of eye open/eye closure on the unpatched eye's contrast sensitivity and ocular dominance (OD) shifts induced by short-term monocular deprivation. The results demonstrate that internal neural states influence not only baseline contrast sensitivity but also the extent to which the adult visual system can undergo changes in ocular dominance.