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Published August 5, 2019 | Accepted Version + Submitted
Journal Article Open

Visual-olfactory integration in the human disease vector mosquito, Aedes aegypti

Abstract

Mosquitoes rely on the integration of multiple sensory cues, including olfactory, visual, and thermal stimuli, to detect, identify, and locate their hosts [1, 2, 3, 4]. Although we increasingly know more about the role of chemosensory behaviors in mediating mosquito-host interactions [1], the role of visual cues is comparatively less studied [3], and how the combination of olfactory and visual information is integrated in the mosquito brain remains unknown. In the present study, we used a tethered-flight light-emitting diode (LED) arena, which allowed for quantitative control over the stimuli, and a control theoretic model to show that CO_2 modulates mosquito steering responses toward vertical bars. To gain insight into the neural basis of this olfactory and visual coupling, we conducted two-photon microscopy experiments in a new GCaMP6s-expressing mosquito line. Imaging revealed that neuropil regions within the lobula exhibited strong responses to objects, such as a bar, but showed little response to a large-field motion. Approximately 20% of the lobula neuropil we imaged were modulated when CO2 preceded the presentation of a moving bar. By contrast, responses in the antennal (olfactory) lobe were not modulated by visual stimuli presented before or after an olfactory stimulus. Together, our results suggest that asymmetric coupling between these sensory systems provides enhanced steering responses to discrete objects.

Additional Information

© 2019 Elsevier Ltd. Received 7 January 2019, Revised 21 March 2019, Accepted 13 June 2019, Available online 18 July 2019. Comments from three anonymous reviewers greatly improved the manuscript and analyses. We thank B. Nguyen for mosquito colony maintenance; J. Tuthill, A. Mamiya, and P. Weir for comments and help with the arena and imaging experiments; G. Wolff for comments and imaging assistance; and D. Alonso San Alberto for technical support. We acknowledge the support of the Air Force Office of Scientific Research under grants FA9550-14-1-0398 and FA9550-16-1-0167, NIH under grants 1RO1DCO13693 and 1R21AI137947, an Endowed Professorship for Excellence in Biology (J.A.R.), and the University of Washington Innovation Award. O.S.A. was supported in part by NIH grants 5K22AI113060 and 1R21AI123937. Author Contributions: C.V., F.V.B., A.L.F., M.H.D., and J.A.R. conceived the study. C.V., F.V.B., L.T.L., and K.K.S.T. participated in the execution and analysis of the arena assays. O.S.A. generated the GCaMP6 mosquitoes. J.A.R. conducted the imaging assays, and C.V., F.V.B., and J.A.R. analyzed the imaging data. C.V., F.V.B., and J.A.R. wrote the paper, and all authors edited the manuscript. Declaration of Interests: The authors declare no competing interests.

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Accepted Version - nihms-1532558.pdf

Submitted - 512996.full.pdf

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Created:
August 22, 2023
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October 23, 2023