Distinct protocerebral neuropils associated with attractive and aversive female-produced odorants in the male moth brain

  1. Jonas Hansen Kymre
  2. XiaoLan Liu
  3. Elena Ian
  4. Christoffer Nerland Berge
  5. GuiRong Wang
  6. Bente G Berg
  7. XinCheng Zhao  Is a corresponding author
  8. Xi Chu  Is a corresponding author
  1. Norwegian University of Science and Technology, Norway
  2. State Key Laboratory for Biology of Plant Disease and Insect Pests, Chinese Academy of Agricultural Sciences, China
  3. Institute of Plant Protection, Chinese Academy of Agricultural Sciences, China
  4. Henan Agricultural University, China

Abstract

The pheromone system of heliothine moths is an optimal model for studying principles underlying higher-order olfactory processing. In Helicoverpa armigera, three male-specific glomeruli receive input about three female-produced signals, the primary pheromone component, serving as an attractant, and two minor constituents, serving a dual function, i.e. attraction versus inhibition of attraction. From the antennal-lobe glomeruli, the information is conveyed to higher olfactory centers, including the lateral protocerebrum, via three main paths – of which the medial tract is the most prominent. In this study, we traced physiologically identified medial-tract projection neurons from each of the three male‑specific glomeruli with the aim of mapping their terminal branches in the lateral protocerebrum. Our data suggest that the neurons’ wide-spread projections are organized according to behavioral significance, including a spatial separation of signals representing attraction versus inhibition – however, with a unique capacity of switching behavioral consequence based on the amount of the minor components.

Data availability

All data generated or analysed during this study are included in the manuscript and supporting files.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Jonas Hansen Kymre

    Department of Psychology, Norwegian University of Science and Technology, Trondheim, Norway
    Competing interests
    The authors declare that no competing interests exist.
  2. XiaoLan Liu

    Institute of Plant Protection, State Key Laboratory for Biology of Plant Disease and Insect Pests, Chinese Academy of Agricultural Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Elena Ian

    Department of Psychology, Norwegian University of Science and Technology, Trondheim, Norway
    Competing interests
    The authors declare that no competing interests exist.
  4. Christoffer Nerland Berge

    Department of Psychology, Norwegian University of Science and Technology, Trondheim, Norway
    Competing interests
    The authors declare that no competing interests exist.
  5. GuiRong Wang

    State Key Laboratory for Biology of Plant Diseases and Insect Pests, Institute of Plant Protection, Chinese Academy of Agricultural Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Bente G Berg

    Department of Psychology, Chemosensory lab, Norwegian University of Science and Technology, Trondheim, Norway
    Competing interests
    The authors declare that no competing interests exist.
  7. XinCheng Zhao

    Department of Entomology, Henan Agricultural University, Zhengzhou, China
    For correspondence
    xincheng@henau.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9471-2222
  8. Xi Chu

    Department of Psychology, Norwegian University of Science and Technology, Trondheim, Norway
    For correspondence
    xi.chu@ntnu.no
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0889-6345

Funding

Norges Forskningsråd (287052)

  • Bente G Berg

National Natural Science Foundation of China (31861133019)

  • GuiRong Wang

Science and technology innovation talents in University of Henan province (19HASTIT011)

  • XinCheng Zhao

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

Reviewing Editor

  1. Christopher J Potter, Johns Hopkins University School of Medicine, United States

Ethics

Animal experimentation: According to Norwegian law of animal welfare, there are no restrictions regarding experimental use of Lepidoptera.

Version history

  1. Received: December 14, 2020
  2. Accepted: May 13, 2021
  3. Accepted Manuscript published: May 14, 2021 (version 1)
  4. Version of Record published: May 26, 2021 (version 2)

Copyright

© 2021, Kymre 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

  • 1,307
    views
  • 141
    downloads
  • 8
    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. Jonas Hansen Kymre
  2. XiaoLan Liu
  3. Elena Ian
  4. Christoffer Nerland Berge
  5. GuiRong Wang
  6. Bente G Berg
  7. XinCheng Zhao
  8. Xi Chu
(2021)
Distinct protocerebral neuropils associated with attractive and aversive female-produced odorants in the male moth brain
eLife 10:e65683.
https://doi.org/10.7554/eLife.65683

Share this article

https://doi.org/10.7554/eLife.65683

Further reading

    1. Neuroscience
    Songyao Zhang, Tuo Zhang ... Tianming Liu
    Research Article

    Cortical folding is an important feature of primate brains that plays a crucial role in various cognitive and behavioral processes. Extensive research has revealed both similarities and differences in folding morphology and brain function among primates including macaque and human. The folding morphology is the basis of brain function, making cross-species studies on folding morphology important for understanding brain function and species evolution. However, prior studies on cross-species folding morphology mainly focused on partial regions of the cortex instead of the entire brain. Previously, our research defined a whole-brain landmark based on folding morphology: the gyral peak. It was found to exist stably across individuals and ages in both human and macaque brains. Shared and unique gyral peaks in human and macaque are identified in this study, and their similarities and differences in spatial distribution, anatomical morphology, and functional connectivity were also dicussed.

    1. Neuroscience
    Avani Koparkar, Timothy L Warren ... Lena Veit
    Research Article

    Complex skills like speech and dance are composed of ordered sequences of simpler elements, but the neuronal basis for the syntactic ordering of actions is poorly understood. Birdsong is a learned vocal behavior composed of syntactically ordered syllables, controlled in part by the songbird premotor nucleus HVC (proper name). Here, we test whether one of HVC’s recurrent inputs, mMAN (medial magnocellular nucleus of the anterior nidopallium), contributes to sequencing in adult male Bengalese finches (Lonchura striata domestica). Bengalese finch song includes several patterns: (1) chunks, comprising stereotyped syllable sequences; (2) branch points, where a given syllable can be followed probabilistically by multiple syllables; and (3) repeat phrases, where individual syllables are repeated variable numbers of times. We found that following bilateral lesions of mMAN, acoustic structure of syllables remained largely intact, but sequencing became more variable, as evidenced by ‘breaks’ in previously stereotyped chunks, increased uncertainty at branch points, and increased variability in repeat numbers. Our results show that mMAN contributes to the variable sequencing of vocal elements in Bengalese finch song and demonstrate the influence of recurrent projections to HVC. Furthermore, they highlight the utility of species with complex syntax in investigating neuronal control of ordered sequences.