Detection of transient synchrony across oscillating receptors by the central electrosensory system of mormyrid fish

  1. Alejandro Vélez
  2. Bruce A Carlson  Is a corresponding author
  1. Washington University in St. Louis, United States

Abstract

Recently, we reported evidence for a novel mechanism of peripheral sensory coding based on oscillatory synchrony. Spontaneously oscillating electroreceptors in weakly electric fish (Mormyridae) respond to electrosensory stimuli with a phase reset that results in transient synchrony across the receptor population (Baker et al., 2015). Here, we asked whether the central electrosensory system actually detects the occurrence of synchronous oscillations among receptors. We found that electrosensory stimulation elicited evoked potentials in the midbrain exterolateral nucleus at a short latency following receptor synchronization. Frequency tuning in the midbrain resembled peripheral frequency tuning, which matches the intrinsic oscillation frequencies of the receptors. These frequencies are lower than those in individual conspecific signals, and instead match those found in collective signals produced by groups of conspecifics. Our results provide further support for a novel mechanism for sensory coding based on the detection of oscillatory synchrony among peripheral receptors.

Article and author information

Author details

  1. Alejandro Vélez

    Department of Biology, Washington University in St. Louis, St. Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Bruce A Carlson

    Department of Biology, Washington University in St. Louis, St. Louis, United States
    For correspondence
    carlson.bruce@wustl.edu
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Animal experimentation: All procedures for housing, handling, and testing animals were performed in strict accordance with the guidelines established by the National Institutes of Health and were approved by the Institutional Animal Care and Use Committee (Animal Welfare Assurance Number: #A-3381-01) at Washington University in St. Louis. The protocol was approved by the Animal Studies Committee at Washington University in St. Louis (Approval Number: 20130265). Every effort was made to minimize pain and stress.

Copyright

© 2016, Vélez & Carlson

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

  • 791
    views
  • 140
    downloads
  • 13
    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. Alejandro Vélez
  2. Bruce A Carlson
(2016)
Detection of transient synchrony across oscillating receptors by the central electrosensory system of mormyrid fish
eLife 5:e16851.
https://doi.org/10.7554/eLife.16851

Share this article

https://doi.org/10.7554/eLife.16851

Further reading

    1. Neuroscience
    Frederick Federer, Justin Balsor ... Alessandra Angelucci
    Research Article

    In the mammalian neocortex, inhibition is important for dynamically balancing excitation and shaping the response properties of cells and circuits. The various computational functions of inhibition are thought to be mediated by different inhibitory neuron types, of which a large diversity exists in several species. Current understanding of the function and connectivity of distinct inhibitory neuron types has mainly derived from studies in transgenic mice. However, it is unknown whether knowledge gained from mouse studies applies to the non-human primate, the model system closest to humans. The lack of viral tools to selectively access inhibitory neuron types has been a major impediment to studying their function in the primate. Here, we have thoroughly validated and characterized several recently developed viral vectors designed to restrict transgene expression to GABAergic cells or their parvalbumin (PV) subtype, and identified two types that show high specificity and efficiency in marmoset V1. We show that in marmoset V1, AAV-h56D induces transgene expression in GABAergic cells with up to 91–94% specificity and 79% efficiency, but this depends on viral serotype and cortical layer. AAV-PHP.eB-S5E2 induces transgene expression in PV cells across all cortical layers with up to 98% specificity and 86–90% efficiency, depending on layer. Thus, these viral vectors are promising tools for studying GABA and PV cell function and connectivity in the primate cortex.

    1. Neuroscience
    Luis Alberto Bezares Calderón, Réza Shahidi, Gáspár Jékely
    Research Article

    Hydrostatic pressure is a dominant environmental cue for vertically migrating marine organisms but the physiological mechanisms of responding to pressure changes remain unclear. Here, we uncovered the cellular and circuit bases of a barokinetic response in the planktonic larva of the marine annelid Platynereis dumerilii. Increased pressure induced a rapid, graded, and adapting upward swimming response due to the faster beating of cilia in the head multiciliary band. By calcium imaging, we found that brain ciliary photoreceptors showed a graded response to pressure changes. The photoreceptors in animals mutant for ciliary opsin-1 had a smaller sensory compartment and mutant larvae showed diminished pressure responses. The ciliary photoreceptors synaptically connect to the head multiciliary band via serotonergic motoneurons. Genetic inhibition of the serotonergic cells blocked pressure-dependent increases in ciliary beating. We conclude that ciliary photoreceptors function as pressure sensors and activate ciliary beating through serotonergic signalling during barokinesis.