Distinct protocerebral neuropils associated with attractive and aversive female-produced odorants in the male moth brain
- Norwegian University of Science and Technology, Norway
- State Key Laboratory for Biology of Plant Disease and Insect Pests, Chinese Academy of Agricultural Sciences, China
- Institute of Plant Protection, Chinese Academy of Agricultural Sciences, China
- 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.
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MGC_PNsInsect Brain Database.
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Data from: A Novel Major Output Target for Pheromone-Sensitive Projection Neurons in Male Mothswww.insectbrain.org; https://hdl.handle.net/20.500.12158/SIN-0000020.2.
Article and author information
Author details
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
- 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
- Received: December 14, 2020
- Accepted: May 13, 2021
- Accepted Manuscript published: May 14, 2021 (version 1)
- 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.
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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
Further reading
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- Biochemistry and Chemical Biology
- Neuroscience
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- Neuroscience
Midbrain dopamine neurons impact neural processing in the prefrontal cortex (PFC) through mesocortical projections. However, the signals conveyed by dopamine projections to the PFC remain unclear, particularly at the single-axon level. Here, we investigated dopaminergic axonal activity in the medial PFC (mPFC) during reward and aversive processing. By optimizing microprism-mediated two-photon calcium imaging of dopamine axon terminals, we found diverse activity in dopamine axons responsive to both reward and aversive stimuli. Some axons exhibited a preference for reward, while others favored aversive stimuli, and there was a strong bias for the latter at the population level. Long-term longitudinal imaging revealed that the preference was maintained in reward- and aversive-preferring axons throughout classical conditioning in which rewarding and aversive stimuli were paired with preceding auditory cues. However, as mice learned to discriminate reward or aversive cues, a cue activity preference gradually developed only in aversive-preferring axons. We inferred the trial-by-trial cue discrimination based on machine learning using anticipatory licking or facial expressions, and found that successful discrimination was accompanied by sharper selectivity for the aversive cue in aversive-preferring axons. Our findings indicate that a group of mesocortical dopamine axons encodes aversive-related signals, which are modulated by both classical conditioning across days and trial-by-trial discrimination within a day.
