Integration of visual and antennal mechanosensory feedback during head stabilization in hawkmoths
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Evaluation Summary:
This paper will be of interest to neuroscientists who study navigation and multisensory integration. In it, the authors use several manipulations to convincingly show that hawkmoths use mechanosensory feedback from their antennae to stabilize their head when their body rotates quickly or when they have little visual input. The results are consistent with the hypothesis that control of head angle in insects that lack halteres results from a multimodal feedback loop that integrates visual and antennal mechanosensory feedback. This advances our understanding of how such stabilizing reflexes work beyond Dipteran flies, where much prior work has focused.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #3 agreed to share their name with the authors.)
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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 frequencies of body roll.
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Evaluation Summary:
This paper will be of interest to neuroscientists who study navigation and multisensory integration. In it, the authors use several manipulations to convincingly show that hawkmoths use mechanosensory feedback from their antennae to stabilize their head when their body rotates quickly or when they have little visual input. The results are consistent with the hypothesis that control of head angle in insects that lack halteres results from a multimodal feedback loop that integrates visual and antennal mechanosensory feedback. This advances our understanding of how such stabilizing reflexes work beyond Dipteran flies, where much prior work has focused.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the …
Evaluation Summary:
This paper will be of interest to neuroscientists who study navigation and multisensory integration. In it, the authors use several manipulations to convincingly show that hawkmoths use mechanosensory feedback from their antennae to stabilize their head when their body rotates quickly or when they have little visual input. The results are consistent with the hypothesis that control of head angle in insects that lack halteres results from a multimodal feedback loop that integrates visual and antennal mechanosensory feedback. This advances our understanding of how such stabilizing reflexes work beyond Dipteran flies, where much prior work has focused.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #3 agreed to share their name with the authors.)
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Reviewer #1 (Public Review):
This paper asks how hawkmoths stabilize their head during externally-imposed body rolls. It finds that when body rolls are fast or there is little light, moths use their antennae to stabilize their head. The authors use convincing manipulations to show the necessity of the antennae for these behaviors and for stable free flight. This finding expands beyond similar studies in dipteran flies, showing that mechanical sensing of rotation can be performed by Johnston's organ in the antennae in moths, while similar functions are performed by the halteres in dipteran flies.
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Reviewer #2 (Public Review):
This manuscript from Chaterjee and colleagues examines head-stabilization reflexes in the hawkmoth. Using light level manipulations and surgical manipulations of the antennae, they show that hawkmoths combine visual and mechanosensory feedback in order to stabilize the head over a wide range of temporal frequencies. Similar to other systems studied, such as flight stablization and antennal positioning, they find that visual feedback makes a stronger contribution at low frequencies while mechanosensory feedback contributes at higher frequencies. Finally they show that loss of head movement during flight contributes to flight instability, suggesting that an inability to stabilize the head might contribute to the effects of antennal manipulation on flight stability. Overall this is a nicely done study with …
Reviewer #2 (Public Review):
This manuscript from Chaterjee and colleagues examines head-stabilization reflexes in the hawkmoth. Using light level manipulations and surgical manipulations of the antennae, they show that hawkmoths combine visual and mechanosensory feedback in order to stabilize the head over a wide range of temporal frequencies. Similar to other systems studied, such as flight stablization and antennal positioning, they find that visual feedback makes a stronger contribution at low frequencies while mechanosensory feedback contributes at higher frequencies. Finally they show that loss of head movement during flight contributes to flight instability, suggesting that an inability to stabilize the head might contribute to the effects of antennal manipulation on flight stability. Overall this is a nicely done study with clear findings that support a general principle of multisensory integration for feedback control. One way in which the manuscript could be strengthened is by explicitly modeling the feedback controller shown in Figure 5, and quantitatively comparing results obtained from this model to experimental results. In addition, it might be helpful to further quantify flight trajectories in head-stabilized moths.
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Reviewer #3 (Public Review):
Payel Chatterjee et al. investigated how compensatory head movements in the nocturnal hawkmoth Daphnis nerii are controlled. This was done by subjecting tethered moths to open-loop body rotations under different light conditions, while simultaneously measuring their ability to main head angle in the presence or absence (achieved by antennal ablation) of antennal mechanosensory feedback. They find that head stabilization is mediated primarily by visual feedback during roll movements at lower frequencies, while antennal mechanosensory feedback is required when roll occurs at higher frequencies or under dark conditions. The findings add to our understanding of how non-dipteran insects (that lack halteres) stabilize their heads. Compensatory head-movements are essential for stabilizing the visual field on the …
Reviewer #3 (Public Review):
Payel Chatterjee et al. investigated how compensatory head movements in the nocturnal hawkmoth Daphnis nerii are controlled. This was done by subjecting tethered moths to open-loop body rotations under different light conditions, while simultaneously measuring their ability to main head angle in the presence or absence (achieved by antennal ablation) of antennal mechanosensory feedback. They find that head stabilization is mediated primarily by visual feedback during roll movements at lower frequencies, while antennal mechanosensory feedback is required when roll occurs at higher frequencies or under dark conditions. The findings add to our understanding of how non-dipteran insects (that lack halteres) stabilize their heads. Compensatory head-movements are essential for stabilizing the visual field on the retina, reducing motion blur and supporting visual self-motion estimation. These are all important parameters to control flight and allow for fast manoeuvres in air. The conclusions of the paper are well supported by the data.
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