Integration of visual and antennal mechanosensory feedback during head stabilization in hawkmoths

  1. Payel Chatterjee
  2. Agnish Dev Prusty
  3. Umesh Mohan
  4. Sanjay P Sane  Is a corresponding author
  1. Tata Institute of Fundamental Research, India

Abstract

During flight maneuvers, insects exhibit compensatory head movements which are essential for stabilizing the visual field on their retina, reducing motion blur, and supporting visual self-motion estimation. In Diptera, such head movements are mediated via visual feedback from their compound eyes that detect retinal slip, as well as rapid mechanosensory feedback from their halteres - the modified hindwings that sense the angular rates of body rotations. Because non-Dipteran insects lack halteres, it is not known if mechanosensory feedback about body rotations plays any role in their head stabilization response. Diverse non-Dipteran insects are known to rely on visual and antennal mechanosensory feedback for flight control. In hawkmoths, for instance, reduction of antennal mechanosensory feedback severely compromises their ability to control flight. Similarly, when the head movements of freely-flying moths are restricted, their flight ability is also severely impaired. The role of compensatory head movements as well as multimodal feedback in insect flight raises an interesting question: in insects that lack halteres, what sensory cues are required for head stabilization? Here, we show that in the nocturnal hawkmoth Daphnis nerii, compensatory head movements are mediated by combined visual and antennal mechanosensory feedback. We subjected tethered moths to open-loop body roll rotations under different lighting conditions, and measured their ability to maintain head angle in the presence or absence of antennal mechanosensory feedback. Our study suggests that head stabilization in moths is mediated primarily by visual feedback during roll movements at lower frequencies, whereas antennal mechanosensory feedback is required when roll occurs at higher frequency. These findings are consistent with the hypothesis that control of head angle results from a multimodal feedback loop that integrates both visual and antennal mechanosensory feedback, albeit at different latencies. At adequate light levels, visual feedback is sufficient for head stabilization primarily at low frequencies of body roll. However, under dark conditions, antennal mechanosensory feedback is essential for the control of head movements at high of body roll.

Data availability

All data related to this paper (both raw and processed) are available on the following link:https://data.mendeley.com/datasets/2trxj9gwsw/draft?a=89356c26-e581-40c6-935d-c1d4a0401074

Article and author information

Author details

  1. Payel Chatterjee

    National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  2. Agnish Dev Prusty

    National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  3. Umesh Mohan

    National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, India
    Competing interests
    The authors declare that no competing interests exist.
  4. Sanjay P Sane

    National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, India
    For correspondence
    sane@ncbs.res.in
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8274-1181

Funding

Air Force Office of Scientific Research (FA2386-11-1-4057)

  • Sanjay P Sane

Air Force Office of Scientific Research (FA9550-16-1-0155)

  • Sanjay P Sane

Department of Atomic Energy, Government of India (12-R&D-TFR-5.04-0800)

  • Sanjay P Sane

National Centre for Biological Sciences (12-R&D-TFR-5.04-0900)

  • Sanjay P Sane

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

Reviewing Editor

  1. Damon A Clark, Yale University, United States

Version history

  1. Received: March 6, 2022
  2. Preprint posted: March 18, 2022 (view preprint)
  3. Accepted: June 21, 2022
  4. Accepted Manuscript published: June 27, 2022 (version 1)
  5. Version of Record published: July 6, 2022 (version 2)

Copyright

© 2022, Chatterjee 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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  1. Payel Chatterjee
  2. Agnish Dev Prusty
  3. Umesh Mohan
  4. Sanjay P Sane
(2022)
Integration of visual and antennal mechanosensory feedback during head stabilization in hawkmoths
eLife 11:e78410.
https://doi.org/10.7554/eLife.78410

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https://doi.org/10.7554/eLife.78410

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