1. Neuroscience

The cell adhesion molecule Sdk1 shapes assembly of a retinal circuit that detects localized edges

  1. Pierre-Luc Rochon
  2. Catherine Theriault
  3. Aline Giselle Rangel Olguin
  4. Arjun Krishnaswamy  Is a corresponding author
  1. McGill University, Canada
https://doi.org/10.7554/eLife.70870
Share this article
Cite this article
  1. Pierre-Luc Rochon
  2. Catherine Theriault
  3. Aline Giselle Rangel Olguin
  4. Arjun Krishnaswamy
(2021)
The cell adhesion molecule Sdk1 shapes assembly of a retinal circuit that detects localized edges
eLife 10:e70870.
https://doi.org/10.7554/eLife.70870
  2. Download BibTeX
  3. Download .RIS

Abstract

Nearly 50 different mouse retinal ganglion cell (RGC) types sample the visual scene for distinct features. RGC feature selectivity arises from their synapses with a specific subset of amacrine (AC) and bipolar cell (BC) types, but how RGC dendrites arborize and collect input from these specific subsets remains poorly understood. Here we examine the hypothesis that RGCs employ molecular recognition systems to meet this challenge. By combining calcium imaging and type-specific histological stains we define a family of circuits that express the recognition molecule Sidekick 1 (Sdk1) which include a novel RGC type (S1-RGC) that responds to local edges. Genetic and physiological studies revealed that Sdk1 loss selectively disrupts S1-RGC visual responses which result from a loss of excitatory and inhibitory inputs and selective dendritic deficits on this neuron. We conclude that Sdk1 shapes dendrite growth and wiring to help S1-RGCs become feature selective.

Data availability

Sample registration fields, registration code, and GCaMP6f datasets are available at Dryad (https://doi.org/10.5061/dryad.4xgxd2593).

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Pierre-Luc Rochon

    McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.

  2. Catherine Theriault

    McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.

  3. Aline Giselle Rangel Olguin

    McGill University, Montreal, Canada
    Competing interests
    The authors declare that no competing interests exist.

  4. Arjun Krishnaswamy

    McGill University, Montreal, Canada
    For correspondence
    arjun.krishnaswamy@mcgill.ca
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7706-4657

Funding

Canadian Institutes of Health Research (project grant)

  • Arjun Krishnaswamy

Natural Sciences and Engineering Research Council of Canada (discovery grant)

  • Arjun Krishnaswamy

Canadian Institutes of Health Research (Graduate Fellowship)

  • Pierre-Luc Rochon

Fonds de Recherche du Québec - Santé (Graduate Fellowship)

  • Aline Giselle Rangel Olguin

Consejo Nacional de Ciencia y Tecnología (Graduate Fellowship)

  • Aline Giselle Rangel Olguin

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: Animals were used in accordance with the rules and regulations established by the Canadian Council on Animal Care and protocol (2017-7889) was approved by the Animal Care Committee at McGill University

Version history

  1. Received: June 1, 2021
  2. Preprint posted: June 9, 2021 (view preprint)
  3. Accepted: September 11, 2021
  4. Accepted Manuscript published: September 21, 2021 (version 1)
  5. Version of Record published: October 13, 2021 (version 2)

Copyright

© 2021, Rochon 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

  • 1,229
    views
  • 135
    downloads
  • 4
    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. Pierre-Luc Rochon
  2. Catherine Theriault
  3. Aline Giselle Rangel Olguin
  4. Arjun Krishnaswamy
(2021)
The cell adhesion molecule Sdk1 shapes assembly of a retinal circuit that detects localized edges
eLife 10:e70870.
https://doi.org/10.7554/eLife.70870

Share this article

https://doi.org/10.7554/eLife.70870

Categories and tags

Research organism

Further reading

    1. Neuroscience

    Chronic intermittent hypoxia reveals role of the Postinspiratory Complex in the mediation of normal swallow production

    Alyssa D Huff, Marlusa Karlen-Amarante ... Jan-Marino Ramirez
    Research Advance

    Obstructive sleep apnea (OSA) is a prevalent sleep-related breathing disorder that results in multiple bouts of intermittent hypoxia. OSA has many neurological and systemic comorbidities, including dysphagia, or disordered swallow, and discoordination with breathing. However, the mechanism in which chronic intermittent hypoxia (CIH) causes dysphagia is unknown. Recently, we showed the postinspiratory complex (PiCo) acts as an interface between the swallow pattern generator (SPG) and the inspiratory rhythm generator, the preBötzinger complex, to regulate proper swallow-breathing coordination (Huff et al., 2023). PiCo is characterized by interneurons co-expressing transporters for glutamate (Vglut2) and acetylcholine (ChAT). Here we show that optogenetic stimulation of ChATcre:Ai32, Vglut2cre:Ai32, and ChATcre:Vglut2FlpO:ChR2 mice exposed to CIH does not alter swallow-breathing coordination, but unexpectedly disrupts swallow behavior via triggering variable swallow motor patterns. This suggests that glutamatergic–cholinergic neurons in PiCo are not only critical for the regulation of swallow-breathing coordination, but also play an important role in the modulation of swallow motor patterning. Our study also suggests that swallow disruption, as seen in OSA, involves central nervous mechanisms interfering with swallow motor patterning and laryngeal activation. These findings are crucial for understanding the mechanisms underlying dysphagia, both in OSA and other breathing and neurological disorders.

    1. Neuroscience

    Unifying network model links recency and central tendency biases in working memory

    Vezha Boboeva, Alberto Pezzotta ... Athena Akrami
    Research Article

    The central tendency bias, or contraction bias, is a phenomenon where the judgment of the magnitude of items held in working memory appears to be biased toward the average of past observations. It is assumed to be an optimal strategy by the brain and commonly thought of as an expression of the brain’s ability to learn the statistical structure of sensory input. On the other hand, recency biases such as serial dependence are also commonly observed and are thought to reflect the content of working memory. Recent results from an auditory delayed comparison task in rats suggest that both biases may be more related than previously thought: when the posterior parietal cortex (PPC) was silenced, both short-term and contraction biases were reduced. By proposing a model of the circuit that may be involved in generating the behavior, we show that a volatile working memory content susceptible to shifting to the past sensory experience – producing short-term sensory history biases – naturally leads to contraction bias. The errors, occurring at the level of individual trials, are sampled from the full distribution of the stimuli and are not due to a gradual shift of the memory toward the sensory distribution’s mean. Our results are consistent with a broad set of behavioral findings and provide predictions of performance across different stimulus distributions and timings, delay intervals, as well as neuronal dynamics in putative working memory areas. Finally, we validate our model by performing a set of human psychophysics experiments of an auditory parametric working memory task.

    1. Neuroscience

    Octopamine integrates the status of internal energy supply into the formation of food-related memories

    Michael Berger, Michèle Fraatz ... Henrike Scholz
    Research Article

    The brain regulates food intake in response to internal energy demands and food availability. However, can internal energy storage influence the type of memory that is formed? We show that the duration of starvation determines whether Drosophila melanogaster forms appetitive short-term or longer-lasting intermediate memories. The internal glycogen storage in the muscles and adipose tissue influences how intensely sucrose-associated information is stored. Insulin-like signaling in octopaminergic reward neurons integrates internal energy storage into memory formation. Octopamine, in turn, suppresses the formation of long-term memory. Octopamine is not required for short-term memory because octopamine-deficient mutants can form appetitive short-term memory for sucrose and to other nutrients depending on the internal energy status. The reduced positive reinforcing effect of sucrose at high internal glycogen levels, combined with the increased stability of food-related memories due to prolonged periods of starvation, could lead to increased food intake.