Organization and function of Drosophila odorant binding proteins

  1. Nikki K Larter
  2. Jennifer S Sun
  3. John R Carlson  Is a corresponding author
  1. Yale University, United States

Abstract

Odorant binding proteins (Obps) are remarkable in their number, diversity, and abundance, yet their role in olfactory coding remains unclear. They are widely believed to be required for transporting hydrophobic odorants through an aqueous lymph to odorant receptors. We construct a map of the Drosophila antenna, in which the abundant Obps are mapped to olfactory sensilla with defined functions. The results lay a foundation for an incisive analysis of Obp function. The map identifies a sensillum type that contains a single abundant Obp, Obp28a. Surprisingly, deletion of the sole abundant Obp in these sensilla does not reduce the magnitude of their olfactory responses. The results suggest that this Obp is not required for odorant transport and that this sensillum does not require an abundant Obp. The results further suggest a novel role for this Obp in buffering changes in the odor environment, perhaps providing a molecular form of gain control.

Article and author information

Author details

  1. Nikki K Larter

    Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1938-1929
  2. Jennifer S Sun

    Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4274-0504
  3. John R Carlson

    Department of Molecular, Cellular and Developmental Biology, Yale University, New Haven, United States
    For correspondence
    john.carlson@yale.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0244-5180

Funding

National Institute on Deafness and Other Communication Disorders

  • John R Carlson

National Science Foundation

  • Nikki K Larter
  • Jennifer S Sun

National Institutes of Health

  • Jennifer S Sun

Dwight N. and Noyes D. Clark Scholarship Fund

  • Jennifer S Sun

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

Copyright

© 2016, Larter 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

  • 4,556
    views
  • 1,035
    downloads
  • 182
    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. Nikki K Larter
  2. Jennifer S Sun
  3. John R Carlson
(2016)
Organization and function of Drosophila odorant binding proteins
eLife 5:e20242.
https://doi.org/10.7554/eLife.20242

Share this article

https://doi.org/10.7554/eLife.20242

Further reading

    1. Computational and Systems Biology
    2. Neuroscience
    Brian DePasquale, Carlos D Brody, Jonathan W Pillow
    Research Article Updated

    Accumulating evidence to make decisions is a core cognitive function. Previous studies have tended to estimate accumulation using either neural or behavioral data alone. Here, we develop a unified framework for modeling stimulus-driven behavior and multi-neuron activity simultaneously. We applied our method to choices and neural recordings from three rat brain regions—the posterior parietal cortex (PPC), the frontal orienting fields (FOF), and the anterior-dorsal striatum (ADS)—while subjects performed a pulse-based accumulation task. Each region was best described by a distinct accumulation model, which all differed from the model that best described the animal’s choices. FOF activity was consistent with an accumulator where early evidence was favored while the ADS reflected near perfect accumulation. Neural responses within an accumulation framework unveiled a distinct association between each brain region and choice. Choices were better predicted from all regions using a comprehensive, accumulation-based framework and different brain regions were found to differentially reflect choice-related accumulation signals: FOF and ADS both reflected choice but ADS showed more instances of decision vacillation. Previous studies relating neural data to behaviorally inferred accumulation dynamics have implicitly assumed that individual brain regions reflect the whole-animal level accumulator. Our results suggest that different brain regions represent accumulated evidence in dramatically different ways and that accumulation at the whole-animal level may be constructed from a variety of neural-level accumulators.

    1. Neuroscience
    Kayson Fakhar, Fatemeh Hadaeghi ... Claus C Hilgetag
    Research Article

    Efficient communication in brain networks is foundational for cognitive function and behavior. However, how communication efficiency is defined depends on the assumed model of signaling dynamics, e.g., shortest path signaling, random walker navigation, broadcasting, and diffusive processes. Thus, a general and model-agnostic framework for characterizing optimal neural communication is needed. We address this challenge by assigning communication efficiency through a virtual multi-site lesioning regime combined with game theory, applied to large-scale models of human brain dynamics. Our framework quantifies the exact influence each node exerts over every other, generating optimal influence maps given the underlying model of neural dynamics. These descriptions reveal how communication patterns unfold if regions are set to maximize their influence over one another. Comparing these maps with a variety of brain communication models showed that optimal communication closely resembles a broadcasting regime in which regions leverage multiple parallel channels for information dissemination. Moreover, we found that the brain’s most influential regions are its rich-club, exploiting their topological vantage point by broadcasting across numerous pathways that enhance their reach even if the underlying connections are weak. Altogether, our work provides a rigorous and versatile framework for characterizing optimal brain communication, and uncovers the most influential brain regions, and the topological features underlying their influence.