A visual sense of number emerges from divisive normalization in a simple center-surround convolutional network

  1. Joonkoo Park  Is a corresponding author
  2. David E Huber
  1. University of Massachusetts Amherst, United States

Abstract

Many species of animals exhibit an intuitive sense of number, suggesting a fundamental neural mechanism for representing numerosity in a visual scene. Recent empirical studies demonstrate that early feedforward visual responses are sensitive to numerosity of a dot array but substantially less so to continuous dimensions orthogonal to numerosity, such as size and spacing of the dots. However, the mechanisms that extract numerosity are unknown. Here we identified the core neurocomputational principles underlying these effects: (1) center-surround contrast filters; (2) at different spatial scales; with (3) divisive normalization across network units. In an untrained computational model, these principles eliminated sensitivity to size and spacing, making numerosity the main determinant of the neuronal response magnitude. Moreover, a model implementation of these principles explained both well-known and relatively novel illusions of numerosity perception across space and time. This supports the conclusion that the neural structures and feedforward processes that encode numerosity naturally produce visual illusions of numerosity. Together, these results identify a set of neurocomputational properties that gives rise to the ubiquity of the number sense in the animal kingdom.

Data availability

The current manuscript is a computational study, so no data have been generated for this manuscript. Modelling code is uploaded in the following public repository: https://osf.io/4rwjs/.

Article and author information

Author details

  1. Joonkoo Park

    Department of Psychological and Brain Sciences, University of Massachusetts Amherst, Amherst, United States
    For correspondence
    joonkoo@umass.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6703-3961
  2. David E Huber

    Department of Psychological and Brain Sciences, University of Massachusetts Amherst, Amherst, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Science Foundation (BCS 1654089)

  • Joonkoo Park

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 T Serences, University of California, San Diego, United States

Version history

  1. Preprint posted: June 1, 2022 (view preprint)
  2. Received: June 11, 2022
  3. Accepted: October 2, 2022
  4. Accepted Manuscript published: October 3, 2022 (version 1)
  5. Version of Record published: October 19, 2022 (version 2)

Copyright

© 2022, Park & Huber

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

  • 961
    views
  • 254
    downloads
  • 3
    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. Joonkoo Park
  2. David E Huber
(2022)
A visual sense of number emerges from divisive normalization in a simple center-surround convolutional network
eLife 11:e80990.
https://doi.org/10.7554/eLife.80990

Share this article

https://doi.org/10.7554/eLife.80990

Further reading

    1. Genetics and Genomics
    2. Neuroscience
    Kenneth Chiou, Noah Snyder-Mackler
    Insight

    Single-cell RNA sequencing reveals the extent to which marmosets carry genetically distinct cells from their siblings.

    1. Cell Biology
    2. Neuroscience
    Mariana I Tsap, Andriy S Yatsenko ... Halyna R Shcherbata
    Research Article

    Mutations in Drosophila Swiss Cheese (SWS) gene or its vertebrate orthologue Neuropathy Target Esterase (NTE) lead to progressive neuronal degeneration in flies and humans. Despite its enzymatic function as a phospholipase is well-established, the molecular mechanism responsible for maintaining nervous system integrity remains unclear. In this study, we found that NTE/SWS is present in surface glia that forms the blood-brain-barrier (BBB) and that NTE/SWS is important to maintain its structure and permeability. Importantly, BBB glia-specific expression of Drosophila NTE/SWS or human NTE in the sws mutant background fully rescues surface glial organization and partially restores BBB integrity, suggesting a conserved function of NTE/SWS. Interestingly, sws mutant glia showed abnormal organization of plasma membrane domains and tight junction rafts accompanied by the accumulation of lipid droplets, lysosomes, and multilamellar bodies. Since the observed cellular phenotypes closely resemble the characteristics described in a group of metabolic disorders known as lysosomal storage diseases (LSDs), our data established a novel connection between NTE/SWS and these conditions. We found that mutants with defective BBB exhibit elevated levels of fatty acids, which are precursors of eicosanoids and are involved in the inflammatory response. Also, as a consequence of a permeable BBB, several innate immunity factors are upregulated in an age-dependent manner, while BBB glia-specific expression of NTE/SWS normalizes inflammatory response. Treatment with anti-inflammatory agents prevents the abnormal architecture of the BBB, suggesting that inflammation contributes to the maintenance of a healthy brain barrier. Considering the link between a malfunctioning BBB and various neurodegenerative diseases, gaining a deeper understanding of the molecular mechanisms causing inflammation due to a defective BBB could help to promote the use of anti-inflammatory therapies for age-related neurodegeneration.