TitleIntegration of visual and antennal mechanosensory feedback during head stabilization in hawkmoths.
Publication TypeJournal Article
Year of Publication2022
AuthorsChatterjee P, Prusty ADev, Mohan U, Sane SP
JournalElife
Volume11
Date Published2022 Jun 27
ISSN2050-084X
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 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 , 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, 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.

DOI10.7554/eLife.78410
Alternate JournalElife
PubMed ID35758646
Grant ListFA2386-11-1-4057 / / Air Force Office of Scientific Research /
FA9550-16-1-0155 / / Air Force Office of Scientific Research /
12-R&D-TFR-5.04-0800 / / Department of Atomic Energy, Government of India /
12-R&D-TFR-5.04-0900 / / National Centre for Biological Sciences /