Small-amplitude head oscillations result from a multimodal head stabilization reflex in hawkmoths

Chatterjee, Payel; Mohan, Umesh; Sane, Sanjay P.

doi:10.1101/2022.04.24.489321

Cited by 2 publications

(3 citation statements)

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“…In all the recordings of head stabilization, we observed small-amplitude head oscillations (or head wobble; Chatterjee et al, 2022 ) at approximately 12 Hz, which did not correspond to the wingbeat or any other frequency that we have investigated. These regular oscillations are a predicted outcome of the multisensory negative feedback loop that we have proposed, and depends on the lag in the sensory acquisition ( Chatterjee et al, 2022 ), or its translation to motor commands in addition to the mechanical properties of head-neck apparatus. Alternatively, it may result from active head movements that the moth performs to ensure active visual feedback ( Cellini and Mongeau, 2020 ; Stamper et al, 2012 ).…”

Section: Discussionmentioning

confidence: 69%

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

Chatterjee

Prusty

Mohan

et al. 2022

eLife

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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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Section: Discussionmentioning

confidence: 69%

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

Chatterjee

Prusty

Mohan

et al. 2022

eLife

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“…All data are accessible at the following link: . Electronic supplementary material, figures S1–S3 accompany this paper [34].…”

Section: Data Accessibilitymentioning

confidence: 99%

“…All data are accessible at the following link: https:// data.mendeley.com/datasets/xndr5g45db/draft?a=1bb29b13-57fb-4ca6-9dd7-8db1cd903209. Electronic supplementary material, figures S1-S3 accompany this paper [34].…”

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confidence: 99%

Small-amplitude head oscillations result from a multimodal head stabilization reflex in hawkmoths

2022

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In flying insects, head stabilization is an essential reflex that helps to reduce motion blur during fast aerial manoeuvres. This reflex is multimodal and requires the integration of visual and antennal mechanosensory feedback in hawkmoths, each operating as a negative-feedback-control loop. As in any negative-feedback system, the head stabilization system possesses inherent oscillatory dynamics that depend on the rate at which the sensorimotor components of the reflex operate. Consistent with this expectation, we observed small-amplitude oscillations in the head motion (or head wobble) of the oleander hawkmoth, Daphnis nerii, which are accentuated when sensory feedback is aberrant. Here, we show that these oscillations emerge from the inherent dynamics of the multimodal reflex underlying gaze stabilization, and that the amplitude of head wobble is a function of both the visual feedback and antennal mechanosensory feedback from the Johnston's organs. Our data support the hypothesis that head wobble results from a multimodal, dynamically stabilized reflex loop that mediates head positioning.

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Small-amplitude head oscillations result from a multimodal head stabilization reflex in hawkmoths

Cited by 2 publications

References 24 publications

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

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

Small-amplitude head oscillations result from a multimodal head stabilization reflex in hawkmoths

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