Adaptation in cone photoreceptors contributes to an unexpected insensitivity of primate On parasol retinal ganglion cells to spatial structure in natural images

  1. Zhou Yu
  2. Maxwell H Turner
  3. Jacob Baudin
  4. Fred Rieke  Is a corresponding author
  1. University of Washington, United States

Abstract

Neural circuits are constructed from nonlinear building blocks, and not surprisingly overall circuit behavior is often strongly nonlinear. But neural circuits can also behave near linearly, and some circuits shift from linear to nonlinear behavior depending on stimulus conditions. Such control of nonlinear circuit behavior is fundamental to neural computation. Here, we study a surprising stimulus dependence of the responses of macaque On (but not Off) parasol retinal ganglion cells: these cells respond nonlinearly to spatial structure in some stimuli but near-linearly to spatial structure in others, including natural inputs. We show that these differences in the linearity of the integration of spatial inputs can be explained by a shift in the balance of excitatory and inhibitory synaptic inputs that originates at least partially from adaptation in the cone photoreceptors. More generally, this highlights how subtle asymmetries in signaling - here in the cone signals - can qualitatively alter circuit computation.

Data availability

Source data for Figures 2, 3, 5, and 7 is provided.

Article and author information

Author details

  1. Zhou Yu

    Department of Physiology and Biophysics, University of Washington, Seattle, United States
    Competing interests
    No competing interests declared.
  2. Maxwell H Turner

    Department of Physiology and Biophysics, University of Washington, Seattle, United States
    Competing interests
    No competing interests declared.
  3. Jacob Baudin

    Department of Physiology and Biophysics, University of Washington, Seattle, United States
    Competing interests
    No competing interests declared.
  4. Fred Rieke

    Department of Physiology and Biophysics, University of Washington, Seattle, United States
    For correspondence
    rieke@uw.edu
    Competing interests
    Fred Rieke, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1052-2609

Funding

National Institutes of Health (EY028542)

  • Fred Rieke

National Institutes of Health (F31-EY026288)

  • Maxwell H Turner

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

Reviewing Editor

  1. Marla B Feller, University of California, Berkeley, United States

Ethics

Animal experimentation: Experiments were performed on primate retina obtained through the Tissue Distribution Program of the University of Washington's Regional Primate Research Center. Recordings were made from retinas from Macaca fascicularis, Macaca nemestrina, and Macaca mulatta of both sexes, aged 2 through 20 years. All use of primate tissue was in accordance with the University of Washington Institutional Animal Care and Use Committee (protocol 4140-01).

Version history

  1. Received: May 22, 2021
  2. Preprint posted: June 30, 2021 (view preprint)
  3. Accepted: March 13, 2022
  4. Accepted Manuscript published: March 14, 2022 (version 1)
  5. Version of Record published: March 25, 2022 (version 2)

Copyright

© 2022, Yu 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

  • 940
    Page views
  • 118
    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)

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. Zhou Yu
  2. Maxwell H Turner
  3. Jacob Baudin
  4. Fred Rieke
(2022)
Adaptation in cone photoreceptors contributes to an unexpected insensitivity of primate On parasol retinal ganglion cells to spatial structure in natural images
eLife 11:e70611.
https://doi.org/10.7554/eLife.70611

Share this article

https://doi.org/10.7554/eLife.70611

Further reading

    1. Neuroscience
    Kiwamu Kudo, Kamalini G Ranasinghe ... Srikantan S Nagarajan
    Research Article

    Alzheimer’s disease (AD) is characterized by the accumulation of amyloid-β and misfolded tau proteins causing synaptic dysfunction, and progressive neurodegeneration and cognitive decline. Altered neural oscillations have been consistently demonstrated in AD. However, the trajectories of abnormal neural oscillations in AD progression and their relationship to neurodegeneration and cognitive decline are unknown. Here, we deployed robust event-based sequencing models (EBMs) to investigate the trajectories of long-range and local neural synchrony across AD stages, estimated from resting-state magnetoencephalography. The increases in neural synchrony in the delta-theta band and the decreases in the alpha and beta bands showed progressive changes throughout the stages of the EBM. Decreases in alpha and beta band synchrony preceded both neurodegeneration and cognitive decline, indicating that frequency-specific neuronal synchrony abnormalities are early manifestations of AD pathophysiology. The long-range synchrony effects were greater than the local synchrony, indicating a greater sensitivity of connectivity metrics involving multiple regions of the brain. These results demonstrate the evolution of functional neuronal deficits along the sequence of AD progression.

    1. Medicine
    2. Neuroscience
    Luisa Fassi, Shachar Hochman ... Roi Cohen Kadosh
    Research Article

    In recent years, there has been debate about the effectiveness of treatments from different fields, such as neurostimulation, neurofeedback, brain training, and pharmacotherapy. This debate has been fuelled by contradictory and nuanced experimental findings. Notably, the effectiveness of a given treatment is commonly evaluated by comparing the effect of the active treatment versus the placebo on human health and/or behaviour. However, this approach neglects the individual’s subjective experience of the type of treatment she or he received in establishing treatment efficacy. Here, we show that individual differences in subjective treatment - the thought of receiving the active or placebo condition during an experiment - can explain variability in outcomes better than the actual treatment. We analysed four independent datasets (N = 387 participants), including clinical patients and healthy adults from different age groups who were exposed to different neurostimulation treatments (transcranial magnetic stimulation: Studies 1 and 2; transcranial direct current stimulation: Studies 3 and 4). Our findings show that the inclusion of subjective treatment can provide a better model fit either alone or in interaction with objective treatment (defined as the condition to which participants are assigned in the experiment). These results demonstrate the significant contribution of subjective experience in explaining the variability of clinical, cognitive, and behavioural outcomes. We advocate for existing and future studies in clinical and non-clinical research to start accounting for participants’ subjective beliefs and their interplay with objective treatment when assessing the efficacy of treatments. This approach will be crucial in providing a more accurate estimation of the treatment effect and its source, allowing the development of effective and reproducible interventions.