Dataset Information

Active vision shapes and coordinates flight motor responses in flies.

ABSTRACT: Animals use active sensing to respond to sensory inputs and guide future motor decisions. In flight, flies generate a pattern of head and body movements to stabilize gaze. How the brain relays visual information to control head and body movements and how active head movements influence downstream motor control remains elusive. Using a control theoretic framework, we studied the optomotor gaze stabilization reflex in tethered flight and quantified how head movements stabilize visual motion and shape wing steering efforts in fruit flies (Drosophila). By shaping visual inputs, head movements increased the gain of wing steering responses and coordination between stimulus and wings, pointing to a tight coupling between head and wing movements. Head movements followed the visual stimulus in as little as 10 ms-a delay similar to the human vestibulo-ocular reflex-whereas wing steering responses lagged by more than 40 ms. This timing difference suggests a temporal order in the flow of visual information such that the head filters visual information eliciting downstream wing steering responses. Head fixation significantly decreased the mechanical power generated by the flight motor by reducing wingbeat frequency and overall thrust. By simulating an elementary motion detector array, we show that head movements shift the effective visual input dynamic range onto the sensitivity optimum of the motion vision pathway. Taken together, our results reveal a transformative influence of active vision on flight motor responses in flies. Our work provides a framework for understanding how to coordinate moving sensors on a moving body.

SUBMITTER: Cellini B

PROVIDER: S-EPMC7502703 | biostudies-literature | 2020 Sep

REPOSITORIES: biostudies-literature

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Publications

Active vision shapes and coordinates flight motor responses in flies.

Cellini Benjamin B Mongeau Jean-Michel JM

Proceedings of the National Academy of Sciences of the United States of America 20200901 37

Animals use active sensing to respond to sensory inputs and guide future motor decisions. In flight, flies generate a pattern of head and body movements to stabilize gaze. How the brain relays visual information to control head and body movements and how active head movements influence downstream motor control remains elusive. Using a control theoretic framework, we studied the optomotor gaze stabilization reflex in tethered flight and quantified how head movements stabilize visual motion and sh ...[more]

PMID: 32873637

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Project description:Photoreceptor neurons are surrounded by an extracellular matrix, called the interphotoreceptor matrix (IPM). Activities crucial to vision occur within the IPM, including trafficking of nutrients and metabolites, retinal attachment, and interactions needed for normal outer segment phagocytosis. The IPM includes the following two unique proteoglycans: IPM proteoglycan 1 (IMPG1) and IMPG2. Patients with mutations in IMPG1/IMPG2 develop visual deficits with subretinal material accumulation, highlighting the critical role of the IPM in vision. To determine the role of these proteoglycans in retinal physiology and the pathologic mechanisms that lead to vision loss, we generated mouse models lacking IMPG1/IMPG2. In normal retina, IMPG1 and IMPG2 occupy distinct IPM compartments, represent the main source of chondroitin sulfate and are fundamental for the constitution of the cone-specific glycocalyx stained by the PNA (peanut agglutinin) lectin marker. No evident morphologic or functional deficits were found in mice lacking IMPG1. In the absence of IMPG2, IMPG1 abnormally accumulated at the subretinal space need, likely leading to the formation of subretinal lesions and reduced visual function. Interestingly, mice lacking both IMPG1 and IMPG2, regardless of sex, showed normal retinal structure and function, demonstrating that the aberrant IMPG1 distribution is the main cause of the visual alterations observed in the absence of IMPG2. In conclusion, our results show the dependence of secreted proteoglycans such as IMPG1 on the extracellular environment to properly integrate into the matrix, demonstrate the role of IMPG2 in shaping the IPM, and shed light on the potential mechanisms leading to the development of subretinal lesions and vision loss.SIGNIFICANCE STATEMENT The photoreceptors are specialized neurons that drive phototransduction in the mammalian retina. These cells are organized and surrounded by an extracellular matrix, the interphotoreceptor matrix (IPM). Mutations in IPM proteoglycans are associated with blindness in humans. Our studies show that two specific proteoglycans of the IPM, IPM proteoglycan 1 (IMPG1) and IMPG2, form a dynamic structure with distinct localization and dependency. When IMPG2 is absent, IMPG1 cannot integrate into the IPM, leading to abnormal proteoglycan accumulation and visual deficits. This work adds a new layer of understanding to IPM physiology and describes the pathologic events following deficits in proteoglycans, providing novel possibilities for visual restoration in patients with IMPG-related pathologies.

Dataset Information

Active vision shapes and coordinates flight motor responses in flies.

Publications

Active vision shapes and coordinates flight motor responses in flies.

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