Dataset Information

Integration of parallel mechanosensory and visual pathways resolved through sensory conflict.

ABSTRACT: The acquisition of information from parallel sensory pathways is a hallmark of coordinated movement in animals. Insect flight, for example, relies on both mechanosensory and visual pathways. Our challenge is to disentangle the relative contribution of each modality to the control of behavior. Toward this end, we show an experimental and analytical framework leveraging sensory conflict, a means for independently exciting and modeling separate sensory pathways within a multisensory behavior. As a model, we examine the hovering flower-feeding behavior in the hawkmoth Manduca sexta In the laboratory, moths feed from a robotically actuated two-part artificial flower that allows independent presentation of visual and mechanosensory cues. Freely flying moths track lateral flower motion stimuli in an assay spanning both coupled motion, in which visual and mechanosensory cues follow the same motion trajectory, and sensory conflict, in which the two sensory modalities encode different motion stimuli. Applying a frequency-domain system identification analysis, we find that the tracking behavior is, in fact, multisensory and arises from a linear summation of visual and mechanosensory pathways. The response dynamics are highly preserved across individuals, providing a model for predicting the response to novel multimodal stimuli. Surprisingly, we find that each pathway in and of itself is sufficient for driving tracking behavior. When multiple sensory pathways elicit strong behavioral responses, this parallel architecture furnishes robustness via redundancy.

SUBMITTER: Roth E

PROVIDER: S-EPMC5111652 | biostudies-literature | 2016 Nov

REPOSITORIES: biostudies-literature

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Integration of parallel mechanosensory and visual pathways resolved through sensory conflict.

Roth Eatai E Hall Robert W RW Daniel Thomas L TL Sponberg Simon S

Proceedings of the National Academy of Sciences of the United States of America 20161024 45

The acquisition of information from parallel sensory pathways is a hallmark of coordinated movement in animals. Insect flight, for example, relies on both mechanosensory and visual pathways. Our challenge is to disentangle the relative contribution of each modality to the control of behavior. Toward this end, we show an experimental and analytical framework leveraging sensory conflict, a means for independently exciting and modeling separate sensory pathways within a multisensory behavior. As a ...[more]

PMID: 27791056

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Project 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.

Dataset Information

Integration of parallel mechanosensory and visual pathways resolved through sensory conflict.

Publications

Integration of parallel mechanosensory and visual pathways resolved through sensory conflict.

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