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Neural evidence supports a dual sensory-motor role for insect wings

Flying insects use feedback from various sensory modalities including vision and mechanosensation to navigate through their environment. The rapid speed of mechanosensory information acquisition and processing compensates for the slower processing times associated with vision, particularly under low...

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Autores principales: Pratt, Brandon, Deora, Tanvi, Mohren, Thomas, Daniel, Thomas
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5597827/
https://www.ncbi.nlm.nih.gov/pubmed/28904136
http://dx.doi.org/10.1098/rspb.2017.0969
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author Pratt, Brandon
Deora, Tanvi
Mohren, Thomas
Daniel, Thomas
author_facet Pratt, Brandon
Deora, Tanvi
Mohren, Thomas
Daniel, Thomas
author_sort Pratt, Brandon
collection PubMed
description Flying insects use feedback from various sensory modalities including vision and mechanosensation to navigate through their environment. The rapid speed of mechanosensory information acquisition and processing compensates for the slower processing times associated with vision, particularly under low light conditions. While halteres in dipteran species are well known to provide such information for flight control, less is understood about the mechanosensory roles of their evolutionary antecedent, wings. The features that wing mechanosensory neurons (campaniform sensilla) encode remains relatively unexplored. We hypothesized that the wing campaniform sensilla of the hawkmoth, Manduca sexta, rapidly and selectively extract mechanical stimulus features in a manner similar to halteres. We used electrophysiological and computational techniques to characterize the encoding properties of wing campaniform sensilla. To accomplish this, we developed a novel technique for localizing receptive fields using a focused IR laser that elicits changes in the neural activity of mechanoreceptors. We found that (i) most wing mechanosensors encoded mechanical stimulus features rapidly and precisely, (ii) they are selective for specific stimulus features, and (iii) there is diversity in the encoding properties of wing campaniform sensilla. We found that the encoding properties of wing campaniform sensilla are similar to those for haltere neurons. Therefore, it appears that the neural architecture that underlies the haltere sensory function is present in wings, which lends credence to the notion that wings themselves may serve a similar sensory function. Thus, wings may not only function as the primary actuator of the organism but also as sensors of the inertial dynamics of the animal.
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spelling pubmed-55978272017-09-18 Neural evidence supports a dual sensory-motor role for insect wings Pratt, Brandon Deora, Tanvi Mohren, Thomas Daniel, Thomas Proc Biol Sci Morphology and Biomechanics Flying insects use feedback from various sensory modalities including vision and mechanosensation to navigate through their environment. The rapid speed of mechanosensory information acquisition and processing compensates for the slower processing times associated with vision, particularly under low light conditions. While halteres in dipteran species are well known to provide such information for flight control, less is understood about the mechanosensory roles of their evolutionary antecedent, wings. The features that wing mechanosensory neurons (campaniform sensilla) encode remains relatively unexplored. We hypothesized that the wing campaniform sensilla of the hawkmoth, Manduca sexta, rapidly and selectively extract mechanical stimulus features in a manner similar to halteres. We used electrophysiological and computational techniques to characterize the encoding properties of wing campaniform sensilla. To accomplish this, we developed a novel technique for localizing receptive fields using a focused IR laser that elicits changes in the neural activity of mechanoreceptors. We found that (i) most wing mechanosensors encoded mechanical stimulus features rapidly and precisely, (ii) they are selective for specific stimulus features, and (iii) there is diversity in the encoding properties of wing campaniform sensilla. We found that the encoding properties of wing campaniform sensilla are similar to those for haltere neurons. Therefore, it appears that the neural architecture that underlies the haltere sensory function is present in wings, which lends credence to the notion that wings themselves may serve a similar sensory function. Thus, wings may not only function as the primary actuator of the organism but also as sensors of the inertial dynamics of the animal. The Royal Society 2017-09-13 2017-09-13 /pmc/articles/PMC5597827/ /pubmed/28904136 http://dx.doi.org/10.1098/rspb.2017.0969 Text en © 2017 The Authors. http://creativecommons.org/licenses/by/4.0/ Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.
spellingShingle Morphology and Biomechanics
Pratt, Brandon
Deora, Tanvi
Mohren, Thomas
Daniel, Thomas
Neural evidence supports a dual sensory-motor role for insect wings
title Neural evidence supports a dual sensory-motor role for insect wings
title_full Neural evidence supports a dual sensory-motor role for insect wings
title_fullStr Neural evidence supports a dual sensory-motor role for insect wings
title_full_unstemmed Neural evidence supports a dual sensory-motor role for insect wings
title_short Neural evidence supports a dual sensory-motor role for insect wings
title_sort neural evidence supports a dual sensory-motor role for insect wings
topic Morphology and Biomechanics
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5597827/
https://www.ncbi.nlm.nih.gov/pubmed/28904136
http://dx.doi.org/10.1098/rspb.2017.0969
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