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Visual Sensory Signals Dominate Tactile Cues during Docked Feeding in Hummingbirds

Animals living in and interacting with natural environments must monitor and respond to changing conditions and unpredictable situations. Using information from multiple sensory systems allows them to modify their behavior in response to their dynamic environment but also creates the challenge of in...

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Autores principales: Goller, Benjamin, Segre, Paolo S., Middleton, Kevin M., Dickinson, Michael H., Altshuler, Douglas L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5694540/
https://www.ncbi.nlm.nih.gov/pubmed/29184479
http://dx.doi.org/10.3389/fnins.2017.00622
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author Goller, Benjamin
Segre, Paolo S.
Middleton, Kevin M.
Dickinson, Michael H.
Altshuler, Douglas L.
author_facet Goller, Benjamin
Segre, Paolo S.
Middleton, Kevin M.
Dickinson, Michael H.
Altshuler, Douglas L.
author_sort Goller, Benjamin
collection PubMed
description Animals living in and interacting with natural environments must monitor and respond to changing conditions and unpredictable situations. Using information from multiple sensory systems allows them to modify their behavior in response to their dynamic environment but also creates the challenge of integrating different, and potentially contradictory, sources of information for behavior control. Understanding how multiple information streams are integrated to produce flexible and reliable behavior is key to understanding how behavior is controlled in natural settings. Natural settings are rarely still, which challenges animals that require precise body position control, like hummingbirds, which hover while feeding from flowers. Tactile feedback, available only once the hummingbird is docked at the flower, could provide additional information to help maintain its position at the flower. To investigate the role of tactile information for hovering control during feeding, we first asked whether hummingbirds physically interact with a feeder once docked. We quantified physical interactions between docked hummingbirds and a feeder placed in front of a stationary background pattern. Force sensors on the feeder measured a complex time course of loading that reflects the wingbeat frequency and bill movement of feeding hummingbirds, and suggests that they sometimes push against the feeder with their bill. Next, we asked whether the measured tactile interactions were used by feeding hummingbirds to maintain position relative to the feeder. We created two experimental scenarios—one in which the feeder was stationary and the visual background moved and the other where the feeder moved laterally in front of a white background. When the visual background pattern moved, docked hummingbirds pushed significantly harder in the direction of horizontal visual motion. When the feeder moved, and the background was stationary, hummingbirds generated aerodynamic force in the opposite direction of the feeder motion. These results suggest that docked hummingbirds are using visual information about the environment to maintain body position and orientation, and not actively tracking the motion of the feeder. The absence of flower tracking behavior in hummingbirds contrasts with the behavior of hawkmoths, and provides evidence that they rely primarily on the visual background rather than flower-based cues while feeding.
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spelling pubmed-56945402017-11-28 Visual Sensory Signals Dominate Tactile Cues during Docked Feeding in Hummingbirds Goller, Benjamin Segre, Paolo S. Middleton, Kevin M. Dickinson, Michael H. Altshuler, Douglas L. Front Neurosci Neuroscience Animals living in and interacting with natural environments must monitor and respond to changing conditions and unpredictable situations. Using information from multiple sensory systems allows them to modify their behavior in response to their dynamic environment but also creates the challenge of integrating different, and potentially contradictory, sources of information for behavior control. Understanding how multiple information streams are integrated to produce flexible and reliable behavior is key to understanding how behavior is controlled in natural settings. Natural settings are rarely still, which challenges animals that require precise body position control, like hummingbirds, which hover while feeding from flowers. Tactile feedback, available only once the hummingbird is docked at the flower, could provide additional information to help maintain its position at the flower. To investigate the role of tactile information for hovering control during feeding, we first asked whether hummingbirds physically interact with a feeder once docked. We quantified physical interactions between docked hummingbirds and a feeder placed in front of a stationary background pattern. Force sensors on the feeder measured a complex time course of loading that reflects the wingbeat frequency and bill movement of feeding hummingbirds, and suggests that they sometimes push against the feeder with their bill. Next, we asked whether the measured tactile interactions were used by feeding hummingbirds to maintain position relative to the feeder. We created two experimental scenarios—one in which the feeder was stationary and the visual background moved and the other where the feeder moved laterally in front of a white background. When the visual background pattern moved, docked hummingbirds pushed significantly harder in the direction of horizontal visual motion. When the feeder moved, and the background was stationary, hummingbirds generated aerodynamic force in the opposite direction of the feeder motion. These results suggest that docked hummingbirds are using visual information about the environment to maintain body position and orientation, and not actively tracking the motion of the feeder. The absence of flower tracking behavior in hummingbirds contrasts with the behavior of hawkmoths, and provides evidence that they rely primarily on the visual background rather than flower-based cues while feeding. Frontiers Media S.A. 2017-11-14 /pmc/articles/PMC5694540/ /pubmed/29184479 http://dx.doi.org/10.3389/fnins.2017.00622 Text en Copyright © 2017 Goller, Segre, Middleton, Dickinson and Altshuler. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Neuroscience
Goller, Benjamin
Segre, Paolo S.
Middleton, Kevin M.
Dickinson, Michael H.
Altshuler, Douglas L.
Visual Sensory Signals Dominate Tactile Cues during Docked Feeding in Hummingbirds
title Visual Sensory Signals Dominate Tactile Cues during Docked Feeding in Hummingbirds
title_full Visual Sensory Signals Dominate Tactile Cues during Docked Feeding in Hummingbirds
title_fullStr Visual Sensory Signals Dominate Tactile Cues during Docked Feeding in Hummingbirds
title_full_unstemmed Visual Sensory Signals Dominate Tactile Cues during Docked Feeding in Hummingbirds
title_short Visual Sensory Signals Dominate Tactile Cues during Docked Feeding in Hummingbirds
title_sort visual sensory signals dominate tactile cues during docked feeding in hummingbirds
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5694540/
https://www.ncbi.nlm.nih.gov/pubmed/29184479
http://dx.doi.org/10.3389/fnins.2017.00622
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