Complexity of frequency receptive fields predicts tonotopic variability across species
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.
-
Complexity of frequency receptive fields predicts tonotopic variability across speciesDryad Digital Repository, doi:10.5061/dryad.9ghx3ffd9.
Article and author information
Author details
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.
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.
Reviewing Editor
- Brice Bathellier, CNRS, France
Version history
- Received: November 8, 2019
- Accepted: May 18, 2020
- Accepted Manuscript published: May 18, 2020 (version 1)
- 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
-
- 1,890
- Page views
-
- 242
- Downloads
-
- 7
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.
Download links
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)
Further reading
-
- Cell Biology
- Neuroscience
The amyloid beta (Aβ) plaques found in Alzheimer’s disease (AD) patients’ brains contain collagens and are embedded extracellularly. Several collagens have been proposed to influence Aβ aggregate formation, yet their role in clearance is unknown. To investigate the potential role of collagens in forming and clearance of extracellular aggregates in vivo, we created a transgenic Caenorhabditis elegans strain that expresses and secretes human Aβ1-42. This secreted Aβ forms aggregates in two distinct places within the extracellular matrix. In a screen for extracellular human Aβ aggregation regulators, we identified different collagens to ameliorate or potentiate Aβ aggregation. We show that a disintegrin and metalloprotease a disintegrin and metalloprotease 2 (ADM-2), an ortholog of ADAM9, reduces the load of extracellular Aβ aggregates. ADM-2 is required and sufficient to remove the extracellular Aβ aggregates. Thus, we provide in vivo evidence of collagens essential for aggregate formation and metalloprotease participating in extracellular Aβ aggregate removal.
-
- Computational and Systems Biology
- Neuroscience
The cerebellar granule cell layer has inspired numerous theoretical models of neural representations that support learned behaviors, beginning with the work of Marr and Albus. In these models, granule cells form a sparse, combinatorial encoding of diverse sensorimotor inputs. Such sparse representations are optimal for learning to discriminate random stimuli. However, recent observations of dense, low-dimensional activity across granule cells have called into question the role of sparse coding in these neurons. Here, we generalize theories of cerebellar learning to determine the optimal granule cell representation for tasks beyond random stimulus discrimination, including continuous input-output transformations as required for smooth motor control. We show that for such tasks, the optimal granule cell representation is substantially denser than predicted by classical theories. Our results provide a general theory of learning in cerebellum-like systems and suggest that optimal cerebellar representations are task-dependent.