1. Neuroscience
Download icon

Reconstruction of natural images from responses of primate retinal ganglion cells

  1. Nora Brackbill  Is a corresponding author
  2. Colleen Rhoades
  3. Alexandra Kling
  4. Nishal Pradeepbhai Shah
  5. Alexander Sher
  6. Alan M Litke
  7. E J Chichilnisky
  1. Stanford University, United States
  2. University of California, Santa Cruz, United States
  3. Stanford School of Medicine, United States
Research Article
  • Cited 2
  • Views 1,517
  • Annotations
Cite this article as: eLife 2020;9:e58516 doi: 10.7554/eLife.58516

Abstract

The visual message conveyed by a retinal ganglion cell (RGC) is often summarized by its spatial receptive field, but in principle also depends on the responses of other RGCs and natural image statistics. This possibility was explored by linear reconstruction of natural images from responses of the four numerically-dominant macaque RGC types. Reconstructions were highly consistent across retinas. The optimal reconstruction filter for each RGC – its visual message – reflected natural image statistics, and resembled the receptive field only when nearby, same-type cells were included. ON and OFF cells conveyed largely independent, complementary representations, and parasol and midget cells conveyed distinct features. Correlated activity and nonlinearities had statistically significant but minor effects on reconstruction. Simulated reconstructions, using linear-nonlinear cascade models of RGC light responses that incorporated measured spatial properties and nonlinearities, produced similar results. Spatiotemporal reconstructions exhibited similar spatial properties, suggesting that the results are relevant for natural vision.

Data availability

Code and data to generate all of the summary plots are included in the supporting files. We are not able to release the raw voltage recordings, which total >5 TBs and require a complex processing pipeline. This paper is only the first analysis using these large data sets, which were collected over many years, and are still in use by students in our lab for other projects and papers funded by grants that were used to acquire them in a lab-wide collaboration. We will be happy to work directly with specific researchers to release additional data to them for the purposes of replication only, but not for further use, until we have had an opportunity to complete our analysis of the data and the PhD students doing this work have been able to publish their findings.

Article and author information

Author details

  1. Nora Brackbill

    Physics, Stanford University, Stanford, United States
    For correspondence
    nbrackbill@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0308-1382
  2. Colleen Rhoades

    Bioengineering, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Alexandra Kling

    Neurosurgery; Ophthalmology; Hansen Experimental Physics Laboratory, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Nishal Pradeepbhai Shah

    Electrical Engineering, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1275-0381
  5. Alexander Sher

    Santa Cruz Institute for Particle Physics, University of California, Santa Cruz, Santa Cruz, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Alan M Litke

    Institute for Particle Physics, University of California, Santa Cruz, Santa Cruz, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3973-3642
  7. E J Chichilnisky

    Department of Neurosurgery, Stanford School of Medicine, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5613-0248

Funding

National Science Foundation (NSF IGERT 0801700)

  • Nora Brackbill

National Science Foundation (CRCNS Grant IIS-1430348)

  • E J Chichilnisky

National Science Foundation (GRFP DGE-114747)

  • Nora Brackbill
  • Colleen Rhoades

National Eye Institute (F31EY027166)

  • Colleen Rhoades

Pew Charitable Trusts (Fellowship in Biomedical Sciences)

  • Alexander Sher

John Chen (donation)

  • Alan M Litke

National Institutes of Health (R01EY017992)

  • E J Chichilnisky

National Institutes of Health (R01-EY029247)

  • E J Chichilnisky

National Eye Institute (R01-EY029247)

  • E J Chichilnisky

National Institutes of Health (CRCNS Grant IIS-1430348)

  • E J Chichilnisky

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

Ethics

Animal experimentation: Animal experimentation: Eyes were removed from terminally anesthetized macaque monkeys (Macaca mulatta, Macaca fascicularis) used by other laboratories in the course of their experiments, in accordance with the Institutional Animal Care and Use Committee guidelines. All of the animals were handled according to approved institutional animal care and use committee (IACUC) protocols (#28860) of the Stanford University. The protocol was approved by the Administrative Panel on Laboratory Animal Care of the Stanford University (Assurance Number: A3213-01).

Reviewing Editor

  1. Markus Meister, California Institute of Technology, United States

Publication history

  1. Received: May 2, 2020
  2. Accepted: November 2, 2020
  3. Accepted Manuscript published: November 4, 2020 (version 1)
  4. Version of Record published: December 21, 2020 (version 2)

Copyright

© 2020, Brackbill 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

  • 1,517
    Page views
  • 239
    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)

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. Neuroscience
    Zhengchao Xu et al.
    Tools and Resources Updated

    The dorsal raphe nucleus (DR) and median raphe nucleus (MR) contain populations of glutamatergic and GABAergic neurons that regulate diverse behavioral functions. However, their whole-brain input-output circuits remain incompletely elucidated. We used viral tracing combined with fluorescence micro-optical sectioning tomography to generate a comprehensive whole-brain atlas of inputs and outputs of glutamatergic and GABAergic neurons in the DR and MR. We found that these neurons received inputs from similar upstream brain regions. The glutamatergic and GABAergic neurons in the same raphe nucleus had divergent projection patterns with differences in critical brain regions. Specifically, MR glutamatergic neurons projected to the lateral habenula through multiple pathways. Correlation and cluster analysis revealed that glutamatergic and GABAergic neurons in the same raphe nucleus received heterogeneous inputs and sent different collateral projections. This connectivity atlas further elucidates the anatomical architecture of the raphe nuclei, which could facilitate better understanding of their behavioral functions.

    1. Neuroscience
    Shankar Ramachandran et al.
    Research Article Updated

    Neuromodulators promote adaptive behaviors that are often complex and involve concerted activity changes across circuits that are often not physically connected. It is not well understood how neuromodulatory systems accomplish these tasks. Here, we show that the Caenorhabditis elegans NLP-12 neuropeptide system shapes responses to food availability by modulating the activity of head and body wall motor neurons through alternate G-protein coupled receptor (GPCR) targets, CKR-1 and CKR-2. We show ckr-2 deletion reduces body bend depth during movement under basal conditions. We demonstrate CKR-1 is a functional NLP-12 receptor and define its expression in the nervous system. In contrast to basal locomotion, biased CKR-1 GPCR stimulation of head motor neurons promotes turning during local searching. Deletion of ckr-1 reduces head neuron activity and diminishes turning while specific ckr-1 overexpression or head neuron activation promote turning. Thus, our studies suggest locomotor responses to changing food availability are regulated through conditional NLP-12 stimulation of head or body wall motor circuits.