1. Neuroscience
Download icon

Learning speed and detection sensitivity controlled by distinct cortico-fugal neurons in visual cortex

  1. Sarah Ruediger  Is a corresponding author
  2. Massimo Scanziani  Is a corresponding author
  1. UCSF and HHMI, United States
Research Article
  • Cited 3
  • Views 2,270
  • Annotations
Cite this article as: eLife 2020;9:e59247 doi: 10.7554/eLife.59247

Abstract

Vertebrates can change their behavior upon detection of visual stimuli according to the outcome their actions produce. Such goal-directed behavior involves evolutionary conserved brain structures like the striatum and optic tectum, which receive ascending visual input from the periphery. In mammals, however, these structures also receive descending visual input from visual cortex (VC), via neurons that give rise to cortico-fugal projections. The function of cortico-fugal neurons in visually-guided, goal-directed behavior remains unclear. Here we address the impact of two populations of cortico-fugal neurons in mouse VC in the learning and performance of a visual detection task. We show that the ablation of striatal projecting neurons reduces learning speed while the ablation of superior colliculus projecting neurons does not impact learning but reduces detection sensitivity. This functional dissociation between distinct cortico-fugal neurons in controlling learning speed and detection sensitivity suggests an adaptive contribution of cortico-fugal pathways even in simple goal-directed behavior.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files. Numerical data for graphs represented in figures 1-6, figure 1-figure supplement 2,3,4,5, figure 2-figure supplement 1, figure 4-figure supplement 1 are provided as source data files. The software used to generate visual stimuli and record neuronal activity is available at: https://github.com/mscaudill/neuroGit and https://github.com/aresulaj/ResRueOlsSca18.

Article and author information

Author details

  1. Sarah Ruediger

    Physiology, UCSF and HHMI, San Francisco, United States
    For correspondence
    sarruedi@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
  2. Massimo Scanziani

    Physiology, UCSF and HHMI, San Francisco, United States
    For correspondence
    massimo@ucsf.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5331-9686

Funding

National Eye Institute (NIH R01EY025668)

  • Massimo Scanziani

Howard Hughes Medical Institute

  • Massimo Scanziani

European Molecular Biology Organization (ALTF741-2012)

  • Sarah Ruediger

Swiss National Science Foundation (151168)

  • Sarah Ruediger

Swiss National Science Foundation (138719)

  • Sarah Ruediger

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 experimental procedures were performed with the approval of the Committee on Animal Care at UCSD and UCSF. Authorization # AN179056

Reviewing Editor

  1. Inna Slutsky, Tel Aviv University, Israel

Publication history

  1. Received: May 23, 2020
  2. Accepted: December 6, 2020
  3. Accepted Manuscript published: December 7, 2020 (version 1)
  4. Version of Record published: December 18, 2020 (version 2)

Copyright

© 2020, Ruediger & Scanziani

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

  • 2,270
    Page views
  • 352
    Downloads
  • 3
    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)

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

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

Further reading

    1. Cell Biology
    2. Neuroscience
    Rene Solano Fonseca et al.
    Research Article Updated

    Concussion is associated with a myriad of deleterious immediate and long-term consequences. Yet the molecular mechanisms and genetic targets promoting the selective vulnerability of different neural subtypes to dysfunction and degeneration remain unclear. Translating experimental models of blunt force trauma in C. elegans to concussion in mice, we identify a conserved neuroprotective mechanism in which reduction of mitochondrial electron flux through complex IV suppresses trauma-induced degeneration of the highly vulnerable dopaminergic neurons. Reducing cytochrome C oxidase function elevates mitochondrial-derived reactive oxygen species, which signal through the cytosolic hypoxia inducing transcription factor, Hif1a, to promote hyperphosphorylation and inactivation of the pyruvate dehydrogenase, PDHE1α. This critical enzyme initiates the Warburg shunt, which drives energetic reallocation from mitochondrial respiration to astrocyte-mediated glycolysis in a neuroprotective manner. These studies demonstrate a conserved process in which glycolytic preconditioning suppresses Parkinson-like hypersensitivity of dopaminergic neurons to trauma-induced degeneration via redox signaling and the Warburg effect.

    1. Biochemistry and Chemical Biology
    2. Neuroscience
    Lloyd Davis et al.
    Tools and Resources Updated

    Synthetic strategies for optically controlling gene expression may enable the precise spatiotemporal control of genes in any combination of cells that cannot be targeted with specific promoters. We develop an improved genetic code expansion system in Caenorhabditis elegans and use it to create a photoactivatable Cre recombinase. We laser-activate Cre in single neurons within a bilaterally symmetric pair to selectively switch on expression of a loxP-controlled optogenetic channel in the targeted neuron. We use the system to dissect, in freely moving animals, the individual contributions of the mechanosensory neurons PLML/PLMR to the C. elegans touch response circuit, revealing distinct and synergistic roles for these neurons. We thus demonstrate how genetic code expansion and optical targeting can be combined to break the symmetry of neuron pairs and dissect behavioural outputs of individual neurons that cannot be genetically targeted.