Spontaneous and evoked activity patterns diverge over development

Abstract

The immature brain is highly spontaneously active. Over development this activity must be integrated with emerging patterns of stimulus-evoked activity, but little is known about how this occurs. Here we investigated this question by recording spontaneous and evoked neural activity in the larval zebrafish tectum from 4 to 15 days post fertilisation. Correlations within spontaneous and evoked activity epochs were comparable over development, and their neural assemblies properties refined in similar ways. However both the similarity between evoked and spontaneous assemblies, and also the geometric distance between spontaneous and evoked patterns, decreased over development. At all stages of development evoked activity was of higher dimension than spontaneous activity. Thus spontaneous and evoked activity do not converge over development in this system, and these results do not support the hypothesis that spontaneous activity evolves to form a Bayesian prior for evoked activity.

Data availability

The data has been made available on FigShare, under the DOI:10.6084/m9.figshare.14402543

The following data sets were generated

Article and author information

Author details

  1. Lilach Avitan

    Queensland Brain Institute, The University of Queensland, St Lucia, Australia
    Competing interests
    The authors declare that no competing interests exist.
  2. Zac Pujic

    Australian Institute for Bioengineering and Nanotechnology, The University of Queensland, St Lucia, Australia
    Competing interests
    The authors declare that no competing interests exist.
  3. Jan Mölter

    Queensland Brain Institute, The University of Queensland, St Lucia, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5964-6207
  4. Shuyu Zhu

    Queensland Brain Institute, The University of Queensland, ST LUCIA, Australia
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3791-8400
  5. Biao Sun

    Queensland Brain Institute, The University of Queensland, St Lucia, Australia
    Competing interests
    The authors declare that no competing interests exist.
  6. Geoffrey J Goodhill

    Queensland Brain Institute, The University of Queensland, St Lucia, Australia
    For correspondence
    g.goodhill@uq.edu.au
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9789-9355

Funding

Australian Research Council (DP170102263)

  • Geoffrey J Goodhill

Australian Research Council (DP180100636)

  • Geoffrey J Goodhill

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

Ethics

Animal experimentation: All procedures were performed with approval from The University of Queensland Animal Ethics Committee (QBI/152/16/ARC).

Copyright

© 2021, Avitan 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

  • 3,124
    views
  • 450
    downloads
  • 27
    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. Lilach Avitan
  2. Zac Pujic
  3. Jan Mölter
  4. Shuyu Zhu
  5. Biao Sun
  6. Geoffrey J Goodhill
(2021)
Spontaneous and evoked activity patterns diverge over development
eLife 10:e61942.
https://doi.org/10.7554/eLife.61942

Share this article

https://doi.org/10.7554/eLife.61942

Further reading

    1. Neuroscience
    Patricia E Phelps, Sung Min Ha ... Xia Yang
    Research Article

    Olfactory ensheathing cells (OECs) are unique glial cells found in both central and peripheral nervous systems where they support continuous axonal outgrowth of olfactory sensory neurons to their targets. Previously, we reported that following severe spinal cord injury, OECs transplanted near the injury site modify the inhibitory glial scar and facilitate axon regeneration past the scar border and into the lesion. To better understand the mechanisms underlying the reparative properties of OECs, we used single-cell RNA-sequencing of OECs from adult rats to study their gene expression programs. Our analyses revealed five diverse OEC subtypes, each expressing novel marker genes and pathways indicative of progenitor, axonal regeneration, secreted molecules, or microglia-like functions. We found substantial overlap of OEC genes with those of Schwann cells, but also with microglia, astrocytes, and oligodendrocytes. We confirmed established markers on cultured OECs, and localized select top genes of OEC subtypes in olfactory bulb tissue. We also show that OECs secrete Reelin and Connective tissue growth factor, extracellular matrix molecules which are important for neural repair and axonal outgrowth. Our results support that OECs are a unique hybrid glia, some with progenitor characteristics, and that their gene expression patterns indicate functions related to wound healing, injury repair, and axonal regeneration.

    1. Immunology and Inflammation
    2. Neuroscience
    Jeremy M Shea, Saul A Villeda
    Research Article

    During aging, microglia – the resident macrophages of the brain – exhibit altered phenotypes and contribute to age-related neuroinflammation. While numerous hallmarks of age-related microglia have been elucidated, the progression from homeostasis to dysfunction during the aging process remains unresolved. To bridge this gap in knowledge, we undertook complementary cellular and molecular analyses of microglia in the mouse hippocampus across the adult lifespan and in the experimental aging model of heterochronic parabiosis. Single-cell RNA-Seq and pseudotime analysis revealed age-related transcriptional heterogeneity in hippocampal microglia and identified intermediate states of microglial aging that also emerge following heterochronic parabiosis. We tested the functionality of intermediate stress response states via TGFβ1 and translational states using pharmacological approaches in vitro to reveal their modulation of the progression to an activated state. Furthermore, we utilized single-cell RNA-Seq in conjunction with in vivo adult microglia-specific Tgfb1 conditional genetic knockout mouse models to demonstrate that microglia advancement through intermediate aging states drives transcriptional inflammatory activation and hippocampal-dependent cognitive decline.