Expansion and contraction of resource allocation in sensory bottlenecks

  1. Laura R Edmondson
  2. Alejandro Jiménez Rodríguez
  3. Hannes P Saal  Is a corresponding author
  1. University of Sheffield, United Kingdom

Abstract

Topographic sensory representations often do not scale proportionally to the size of their input regions, with some expanded and others contracted. In vision, the foveal representation is magnified cortically, as are the fingertips in touch. What principles drive this allocation, and how should receptor density, e.g. the high innervation of the fovea or the fingertips, and stimulus statistics, e.g. the higher contact frequencies on the fingertips, contribute? Building on work in efficient coding, we address this problem using linear models that optimally decorrelate the sensory signals. We introduce a sensory bottleneck to impose constraints on resource allocation and derive the optimal neural allocation. We find that bottleneck width is a crucial factor in resource allocation, inducing either expansion or contraction. Both receptor density and stimulus statistics affect allocation and jointly determine convergence for wider bottlenecks. Furthermore, we show a close match between the predicted and empirical cortical allocations in a well-studied model system, the star-nosed mole. Overall, our results suggest that the strength of cortical magnification depends on resource limits.

Data availability

No data was generated for this study. All equations and model parameters are included in the manuscript and supporting files. Additionally, code implementing the model equations has been made available on Github at https://github.com/lauraredmondson/expansion_contraction_sensory_bottlenecks (see also Methods section in manuscript).

Article and author information

Author details

  1. Laura R Edmondson

    Department of Psychology, University of Sheffield, Sheffield, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9886-1121
  2. Alejandro Jiménez Rodríguez

    Sheffield Robotics, University of Sheffield, Sheffield, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Hannes P Saal

    Department of Psychology, University of Sheffield, Sheffield, United Kingdom
    For correspondence
    h.saal@sheffield.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7544-0196

Funding

Wellcome Trust (209998/Z/17/Z)

  • Hannes P Saal

European Commission (HBP-SGA2,785907)

  • Alejandro Jiménez Rodríguez

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

Reviewing Editor

  1. Stephanie E Palmer, University of Chicago, United States

Publication history

  1. Preprint posted: May 27, 2021 (view preprint)
  2. Received: May 28, 2021
  3. Accepted: July 29, 2022
  4. Accepted Manuscript published: August 4, 2022 (version 1)
  5. Version of Record published: August 19, 2022 (version 2)

Copyright

© 2022, Edmondson 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

  • 470
    Page views
  • 105
    Downloads
  • 0
    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. Laura R Edmondson
  2. Alejandro Jiménez Rodríguez
  3. Hannes P Saal
(2022)
Expansion and contraction of resource allocation in sensory bottlenecks
eLife 11:e70777.
https://doi.org/10.7554/eLife.70777

Further reading

    1. Neuroscience
    Simon Desch, Petra Schweinhardt ... Susanne Becker
    Research Article

    Relief of ongoing pain is a potent motivator of behavior, directing actions to escape from or reduce potentially harmful stimuli. Whereas endogenous modulation of pain events is well characterized, relatively little is known about the modulation of pain relief and its corresponding neurochemical basis. Here we studied pain modulation during a probabilistic relief-seeking task (a 'wheel of fortune' gambling task), in which people actively or passively received reduction of a tonic thermal pain stimulus. We found that relief perception was enhanced by active decisions and unpredictability, and greater in high novelty-seeking trait individuals, consistent with a model in which relief is tuned by its informational content. We then probed the roles of dopaminergic and opioidergic signaling, both of which are implicated in relief processing, by embedding the task in a double-blinded cross-over design with administration of the dopamine precursor levodopa and the opioid receptor antagonist naltrexone. We found that levodopa enhanced each of these information-specific aspects of relief modulation but no significant effects of the opioidergic manipulation. These results show that dopaminergic signaling has a key role in modulating the perception of pain relief to optimize motivation and behavior.

    1. Genetics and Genomics
    2. Neuroscience
    Colleen M Palmateer, Catherina Artikis ... Michelle N Arbeitman
    Research Article

    Drosophila melanogaster reproductive behaviors are orchestrated by fruitless neurons. We performed single-cell RNA-sequencing on pupal neurons that produce sex-specifically spliced fru transcripts, the fru P1-expressing neurons. Uniform Manifold Approximation and Projection (UMAP) with clustering generates an atlas containing 113 clusters. While the male and female neurons overlap in UMAP space, more than half the clusters have sex differences in neuron number, and nearly all clusters display sex-differential expression. Based on an examination of enriched marker genes, we annotate clusters as circadian clock neurons, mushroom body Kenyon cell neurons, neurotransmitter- and/or neuropeptide-producing, and those that express doublesex. Marker gene analyses also show that genes that encode members of the immunoglobulin superfamily of cell adhesion molecules, transcription factors, neuropeptides, neuropeptide receptors, and Wnts have unique patterns of enriched expression across the clusters. In vivo spatial gene expression links to the clusters are examined. A functional analysis of fru P1 circadian neurons shows they have dimorphic roles in activity and period length. Given that most clusters are comprised of male and female neurons indicates that the sexes have fru P1 neurons with common gene expression programs. Sex-specific expression is overlaid on this program, to build the potential for vastly different sex-specific behaviors.