1. Neuroscience
Download icon

Thalamocortical synapses in the cat visual system in vivo are weak and unreliable

  1. Madineh Sedigh-Sarvestani  Is a corresponding author
  2. Larry A Palmer
  3. Diego Contreras  Is a corresponding author
  1. University of Pennsylvania School of Medicine, United States
Research Article
  • Cited 3
  • Views 1,112
  • Annotations
Cite this article as: eLife 2019;8:e41925 doi: 10.7554/eLife.41925

Abstract

The thalamocortical synapse of the visual system has been central to our understanding of sensory computations in the cortex. Although we have a fair understanding of the functional properties of the pre and post-synaptic populations, little is known about their synaptic properties, particularly in vivo. We used simultaneous recordings in LGN and V1 in cat in vivo to characterize the dynamic properties of thalamocortical synaptic transmission in monosynaptically connected LGN-V1 neurons. We found that thalamocortical synapses in vivo are unreliable, highly variable and exhibit short-term plasticity. Using biologically constrained models, we found that variable and unreliable synapses serve to increase cortical firing by means of increasing membrane fluctuations, similar to high conductance states. Thus, synaptic variability and unreliability, rather than acting as system noise, do serve a computational function. Our characterization of LGN-V1 synaptic properties constrains existing mathematical models, and mechanistic hypotheses, of a fundamental circuit in computational neuroscience.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files. Raw data and MATLAB code have been uploaded to Dryad (http://dx.doi.org/10.5061/dryad.57pv818).

The following data sets were generated

Article and author information

Author details

  1. Madineh Sedigh-Sarvestani

    Department of Neuroscience, University of Pennsylvania School of Medicine, Philadelphia, United States
    For correspondence
    msarvestani@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
  2. Larry A Palmer

    Department of Neuroscience, University of Pennsylvania School of Medicine, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Diego Contreras

    Department of Neuroscience, University of Pennsylvania School of Medicine, Philadelphia, United States
    For correspondence
    diegoc@upenn.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0197-9882

Funding

National Eye Institute (R01EY027205)

  • Larry A Palmer
  • Diego Contreras

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

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 institutional animal care and use committee (IACUC) of the University of Pennsylvania (Protocol # 803477). All surgery was performed under sodium pentobarbital or propofol anesthesia, and every effort was made to minimize suffering.

Reviewing Editor

  1. John Huguenard, Stanford University School of Medicine, United States

Publication history

  1. Received: September 11, 2018
  2. Accepted: April 27, 2019
  3. Accepted Manuscript published: April 29, 2019 (version 1)
  4. Version of Record published: May 8, 2019 (version 2)

Copyright

© 2019, Sedigh-Sarvestani 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

  • 1,112
    Page views
  • 234
    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.