1. Neuroscience

Complexity of frequency receptive fields predicts tonotopic variability across species

  1. Quentin Gaucher
  2. Mariangela Panniello
  3. Aleksandar Z Ivanov
  4. Johannes C Dahmen
  5. Andrew J King
  6. Kerry M M Walker  Is a corresponding author
  1. University of Oxford, United Kingdom
https://doi.org/10.7554/eLife.53462
Share this article
Cite this article
  1. Quentin Gaucher
  2. Mariangela Panniello
  3. Aleksandar Z Ivanov
  4. Johannes C Dahmen
  5. Andrew J King
  6. Kerry M M Walker
(2020)
Complexity of frequency receptive fields predicts tonotopic variability across species
eLife 9:e53462.
https://doi.org/10.7554/eLife.53462
  2. Download BibTeX
  3. Download .RIS

Abstract

Primary cortical areas contain maps of sensory features, including sound frequency in primary auditory cortex (A1). Two-photon calcium imaging in mice has confirmed the presence of these global tonotopic maps, while uncovering an unexpected local variability in the stimulus preferences of individual neurons in A1 and other primary regions. Here we show that local heterogeneity of frequency preferences is not unique to rodents. Using two-photon calcium imaging in layers 2/3, we found that local variance in frequency preferences is equivalent in ferrets and mice. Neurons with multipeaked frequency tuning are less spatially organized than those tuned to a single frequency in both species. Furthermore, we show that microelectrode recordings may describe a smoother tonotopic arrangement due to a sampling bias towards neurons with simple frequency tuning. These results help explain previous inconsistencies in cortical topography across species and recording techniques.

Data availability

We have provided our data and Matlab scripts for generating our figures on Dryad: https://doi.org/10.5061/dryad.9ghx3ffd9.

The following data sets were generated

Article and author information

Author details

  1. Quentin Gaucher

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.

  2. Mariangela Panniello

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.

  3. Aleksandar Z Ivanov

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.

  4. Johannes C Dahmen

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9889-8303

  5. Andrew J King

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    Competing interests
    Andrew J King, Senior editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5180-7179

  6. Kerry M M Walker

    Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford, United Kingdom
    For correspondence
    kerry.walker@dpag.ox.ac.uk
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1043-5302

Funding

Biotechnology and Biological Sciences Research Council (BB/M010929/1)

  • Kerry M M Walker

University Of Oxford (DPAG Early Career Fellowship)

  • Kerry M M Walker

Wellcome (WT076508AIA)

  • Andrew J King

Wellcome (WT108369/Z/2015/Z)

  • Andrew J King

University Of Oxford (Christopher Welch Scholarship)

  • Aleksandar Z Ivanov

University Of Oxford (Newton-Abraham Scholarship)

  • Mariangela Panniello

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

Reviewing Editor

  1. Brice Bathellier, CNRS, France

Ethics

Animal experimentation: The animal procedures were approved by the University of Oxford Committee on Animal Care and Ethical Review and were carried out under license from the UK Home Office, in accordance with the Animals (Scientific Procedures) Act 1986 and in line with the 3Rs. Project licence PPL 30/3181 and PIL l23DD2122.

Version history

  1. Received: November 8, 2019
  2. Accepted: May 18, 2020
  3. Accepted Manuscript published: May 18, 2020 (version 1)
  4. Version of Record published: June 3, 2020 (version 2)

Copyright

© 2020, Gaucher 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

  • 2,065
    views
  • 260
    downloads
  • 17
    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. Quentin Gaucher
  2. Mariangela Panniello
  3. Aleksandar Z Ivanov
  4. Johannes C Dahmen
  5. Andrew J King
  6. Kerry M M Walker
(2020)
Complexity of frequency receptive fields predicts tonotopic variability across species
eLife 9:e53462.
https://doi.org/10.7554/eLife.53462

Share this article

https://doi.org/10.7554/eLife.53462

Categories and tags

Research organism

Further reading

    1. Developmental Biology
    2. Neuroscience

    Spatiotemporal changes in Netrin/Dscam1 signaling dictate axonal projection direction in Drosophila small ventral lateral clock neurons

    Jingjing Liu, Yuedong Wang ... Yao Tian
    Research Article

    Axon projection is a spatial- and temporal-specific process in which the growth cone receives environmental signals guiding axons to their final destination. However, the mechanisms underlying changes in axonal projection direction without well-defined landmarks remain elusive. Here, we present evidence showcasing the dynamic nature of axonal projections in Drosophila’s small ventral lateral clock neurons (s-LNvs). Our findings reveal that these axons undergo an initial vertical projection in the early larval stage, followed by a subsequent transition to a horizontal projection in the early-to-mid third instar larvae. The vertical projection of s-LNv axons correlates with mushroom body calyx expansion, while the s-LNv-expressed Down syndrome cell adhesion molecule (Dscam1) interacts with Netrins to regulate the horizontal projection. During a specific temporal window, locally newborn dorsal clock neurons secrete Netrins, facilitating the transition of axonal projection direction in s-LNvs. Our study establishes a compelling in vivo model to probe the mechanisms of axonal projection direction switching in the absence of clear landmarks. These findings underscore the significance of dynamic local microenvironments in the complementary regulation of axonal projection direction transitions.

    1. Neuroscience

    Cerebellum: Linking abnormal neural activity patterns to motor deficits

    David J Herzfeld
    Insight

    Abnormal activity in the cerebellar nuclei can be used to predict motor symptoms and induce them experimentally, pointing to potential therapeutic strategies.

    1. Cell Biology
    2. Neuroscience

    Presynaptic Rac1 in the hippocampus selectively regulates working memory

    Jaebin Kim, Edwin Bustamante ... Scott H Soderling
    Research Article

    One of the most extensively studied members of the Ras superfamily of small GTPases, Rac1 is an intracellular signal transducer that remodels actin and phosphorylation signaling networks. Previous studies have shown that Rac1-mediated signaling is associated with hippocampal-dependent working memory and longer-term forms of learning and memory and that Rac1 can modulate forms of both pre- and postsynaptic plasticity. How these different cognitive functions and forms of plasticity mediated by Rac1 are linked, however, is unclear. Here, we show that spatial working memory in mice is selectively impaired following the expression of a genetically encoded Rac1 inhibitor at presynaptic terminals, while longer-term cognitive processes are affected by Rac1 inhibition at postsynaptic sites. To investigate the regulatory mechanisms of this presynaptic process, we leveraged new advances in mass spectrometry to identify the proteomic and post-translational landscape of presynaptic Rac1 signaling. We identified serine/threonine kinases and phosphorylated cytoskeletal signaling and synaptic vesicle proteins enriched with active Rac1. The phosphorylated sites in these proteins are at positions likely to have regulatory effects on synaptic vesicles. Consistent with this, we also report changes in the distribution and morphology of synaptic vesicles and in postsynaptic ultrastructure following presynaptic Rac1 inhibition. Overall, this study reveals a previously unrecognized presynaptic role of Rac1 signaling in cognitive processes and provides insights into its potential regulatory mechanisms.