Integration of visual and antennal mechanosensory feedback during head stabilization in hawkmoths
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 tha...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-06-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/78410 |
| _version_ | 1811205130978066432 |
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| author | Payel Chatterjee Agnish Dev Prusty Umesh Mohan Sanjay P Sane |
| author_facet | Payel Chatterjee Agnish Dev Prusty Umesh Mohan Sanjay P Sane |
| author_sort | Payel Chatterjee |
| collection | DOAJ |
| description | 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 frequencies of body roll. |
| first_indexed | 2024-04-12T03:26:24Z |
| format | Article |
| id | doaj.art-aa2d5863fbec403ca5c534445fc6ee73 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T03:26:24Z |
| publishDate | 2022-06-01 |
| publisher | eLife Sciences Publications Ltd |
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| series | eLife |
| spelling | doaj.art-aa2d5863fbec403ca5c534445fc6ee732022-12-22T03:49:43ZengeLife Sciences Publications LtdeLife2050-084X2022-06-011110.7554/eLife.78410Integration of visual and antennal mechanosensory feedback during head stabilization in hawkmothsPayel Chatterjee0https://orcid.org/0000-0002-7019-6702Agnish Dev Prusty1https://orcid.org/0000-0002-4890-9163Umesh Mohan2https://orcid.org/0000-0002-1992-0558Sanjay P Sane3https://orcid.org/0000-0002-8274-1181National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, IndiaNational Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, IndiaNational Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, IndiaNational Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, IndiaDuring 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 frequencies of body roll.https://elifesciences.org/articles/78410Daphnis neriigaze stabilizationoptic flowhead stabilizationJohnston's organs |
| spellingShingle | Payel Chatterjee Agnish Dev Prusty Umesh Mohan Sanjay P Sane Integration of visual and antennal mechanosensory feedback during head stabilization in hawkmoths eLife Daphnis nerii gaze stabilization optic flow head stabilization Johnston's organs |
| title | Integration of visual and antennal mechanosensory feedback during head stabilization in hawkmoths |
| title_full | Integration of visual and antennal mechanosensory feedback during head stabilization in hawkmoths |
| title_fullStr | Integration of visual and antennal mechanosensory feedback during head stabilization in hawkmoths |
| title_full_unstemmed | Integration of visual and antennal mechanosensory feedback during head stabilization in hawkmoths |
| title_short | Integration of visual and antennal mechanosensory feedback during head stabilization in hawkmoths |
| title_sort | integration of visual and antennal mechanosensory feedback during head stabilization in hawkmoths |
| topic | Daphnis nerii gaze stabilization optic flow head stabilization Johnston's organs |
| url | https://elifesciences.org/articles/78410 |
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