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

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.

Reviewing Editor

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

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.

Version 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

  • 1,369
    views
  • 263
    downloads
  • 6
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

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. Madineh Sedigh-Sarvestani
  2. Larry A Palmer
  3. Diego Contreras
(2019)
Thalamocortical synapses in the cat visual system in vivo are weak and unreliable
eLife 8:e41925.
https://doi.org/10.7554/eLife.41925

Share this article

https://doi.org/10.7554/eLife.41925

Further reading

    1. Neuroscience
    Ivan Tomić, Paul M Bays
    Research Article

    Probing memory of a complex visual image within a few hundred milliseconds after its disappearance reveals significantly greater fidelity of recall than if the probe is delayed by as little as a second. Classically interpreted, the former taps into a detailed but rapidly decaying visual sensory or ‘iconic’ memory (IM), while the latter relies on capacity-limited but comparatively stable visual working memory (VWM). While iconic decay and VWM capacity have been extensively studied independently, currently no single framework quantitatively accounts for the dynamics of memory fidelity over these time scales. Here, we extend a stationary neural population model of VWM with a temporal dimension, incorporating rapid sensory-driven accumulation of activity encoding each visual feature in memory, and a slower accumulation of internal error that causes memorized features to randomly drift over time. Instead of facilitating read-out from an independent sensory store, an early cue benefits recall by lifting the effective limit on VWM signal strength imposed when multiple items compete for representation, allowing memory for the cued item to be supplemented with information from the decaying sensory trace. Empirical measurements of human recall dynamics validate these predictions while excluding alternative model architectures. A key conclusion is that differences in capacity classically thought to distinguish IM and VWM are in fact contingent upon a single resource-limited WM store.

    1. Neuroscience
    Emilio Salinas, Bashirul I Sheikh
    Insight

    Our ability to recall details from a remembered image depends on a single mechanism that is engaged from the very moment the image disappears from view.