1. Neuroscience

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
https://doi.org/10.7554/eLife.65683
Share this article
Cite this article
  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
  2. Download BibTeX
  3. Download .RIS

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.

Ethics

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

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.

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

Categories and tags

Further reading

    1. Neuroscience

    Parabrachial CGRP neurons modulate active defensive behavior under a naturalistic threat

    Gyeong Hee Pyeon, Hyewon Cho ... Yong Sang Jo
    Research Article Updated

    Recent studies suggest that calcitonin gene-related peptide (CGRP) neurons in the parabrachial nucleus (PBN) represent aversive information and signal a general alarm to the forebrain. If CGRP neurons serve as a true general alarm, their activation would modulate both passive nad active defensive behaviors depending on the magnitude and context of the threat. However, most prior research has focused on the role of CGRP neurons in passive freezing responses, with limited exploration of their involvement in active defensive behaviors. To address this, we examined the role of CGRP neurons in active defensive behavior using a predator-like robot programmed to chase mice. Our electrophysiological results revealed that CGRP neurons encode the intensity of aversive stimuli through variations in firing durations and amplitudes. Optogenetic activation of CGRP neurons during robot chasing elevated flight responses in both conditioning and retention tests, presumably by amplifying the perception of the threat as more imminent and dangerous. In contrast, animals with inactivated CGRP neurons exhibited reduced flight responses, even when the robot was programmed to appear highly threatening during conditioning. These findings expand the understanding of CGRP neurons in the PBN as a critical alarm system, capable of dynamically regulating active defensive behaviors by amplifying threat perception, and ensuring adaptive responses to varying levels of danger.

    1. Neuroscience

    Cortical tracking of hierarchical rhythms orchestrates the multisensory processing of biological motion

    Li Shen, Shuo Li ... Yi Jiang
    Research Article

    When observing others’ behaviors, we continuously integrate their movements with the corresponding sounds to enhance perception and develop adaptive responses. However, how the human brain integrates these complex audiovisual cues based on their natural temporal correspondence remains unclear. Using electroencephalogram (EEG), we demonstrated that rhythmic cortical activity tracked the hierarchical rhythmic structures in audiovisually congruent human walking movements and footstep sounds. Remarkably, the cortical tracking effects exhibit distinct multisensory integration modes at two temporal scales: an additive mode in a lower-order, narrower temporal integration window (step cycle) and a super-additive enhancement in a higher-order, broader temporal window (gait cycle). Furthermore, while neural responses at the lower-order timescale reflect a domain-general audiovisual integration process, cortical tracking at the higher-order timescale is exclusively engaged in the integration of biological motion cues. In addition, only this higher-order, domain-specific cortical tracking effect correlates with individuals’ autistic traits, highlighting its potential as a neural marker for autism spectrum disorder. These findings unveil the multifaceted mechanism whereby rhythmic cortical activity supports the multisensory integration of human motion, shedding light on how neural coding of hierarchical temporal structures orchestrates the processing of complex, natural stimuli across multiple timescales.

    1. Evolutionary Biology
    2. Neuroscience

    Vision: The inner workings of a miniature eye

    Gregor Belušič
    Insight

    The first complete 3D reconstruction of the compound eye of a minute wasp species sheds light on the nuts and bolts of size reduction.