Sun Navigation Requires Compass Neurons in Drosophila
Despite their small brains, insects can navigate over long distances by orienting using visual landmarks [1], skylight polarization [2-9], and sun position [3, 4, 6, 10]. Although Drosophila are not generally renowned for their navigational abilities, mark-and-recapture experiments in Death Valley r...
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| Veröffentlicht in: | Current biology Jg. 28; H. 17; S. 2845 |
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10.09.2018
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| Abstract | Despite their small brains, insects can navigate over long distances by orienting using visual landmarks [1], skylight polarization [2-9], and sun position [3, 4, 6, 10]. Although Drosophila are not generally renowned for their navigational abilities, mark-and-recapture experiments in Death Valley revealed that they can fly nearly 15 km in a single evening [11]. To accomplish such feats on available energy reserves [12], flies would have to maintain relatively straight headings, relying on celestial cues [13]. Cues such as sun position and polarized light are likely integrated throughout the sensory-motor pathway [14], including the highly conserved central complex [4, 15, 16]. Recently, a group of Drosophila central complex cells (E-PG neurons) have been shown to function as an internal compass [17-19], similar to mammalian head-direction cells [20]. Using an array of genetic tools, we set out to test whether flies can navigate using the sun and to identify the role of E-PG cells in this behavior. Using a flight simulator, we found that Drosophila adopt arbitrary headings with respect to a simulated sun, thus performing menotaxis, and individuals remember their heading preference between successive flights-even over several hours. Imaging experiments performed on flying animals revealed that the E-PG cells track sun stimulus motion. When these neurons are silenced, flies no longer adopt and maintain arbitrary headings relative to the sun stimulus but instead exhibit frontal phototaxis. Thus, without the compass system, flies lose the ability to execute menotaxis and revert to a simpler, reflexive behavior. |
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| AbstractList | Despite their small brains, insects can navigate over long distances by orienting using visual landmarks [1], skylight polarization [2-9], and sun position [3, 4, 6, 10]. Although Drosophila are not generally renowned for their navigational abilities, mark-and-recapture experiments in Death Valley revealed that they can fly nearly 15 km in a single evening [11]. To accomplish such feats on available energy reserves [12], flies would have to maintain relatively straight headings, relying on celestial cues [13]. Cues such as sun position and polarized light are likely integrated throughout the sensory-motor pathway [14], including the highly conserved central complex [4, 15, 16]. Recently, a group of Drosophila central complex cells (E-PG neurons) have been shown to function as an internal compass [17-19], similar to mammalian head-direction cells [20]. Using an array of genetic tools, we set out to test whether flies can navigate using the sun and to identify the role of E-PG cells in this behavior. Using a flight simulator, we found that Drosophila adopt arbitrary headings with respect to a simulated sun, thus performing menotaxis, and individuals remember their heading preference between successive flights-even over several hours. Imaging experiments performed on flying animals revealed that the E-PG cells track sun stimulus motion. When these neurons are silenced, flies no longer adopt and maintain arbitrary headings relative to the sun stimulus but instead exhibit frontal phototaxis. Thus, without the compass system, flies lose the ability to execute menotaxis and revert to a simpler, reflexive behavior.Despite their small brains, insects can navigate over long distances by orienting using visual landmarks [1], skylight polarization [2-9], and sun position [3, 4, 6, 10]. Although Drosophila are not generally renowned for their navigational abilities, mark-and-recapture experiments in Death Valley revealed that they can fly nearly 15 km in a single evening [11]. To accomplish such feats on available energy reserves [12], flies would have to maintain relatively straight headings, relying on celestial cues [13]. Cues such as sun position and polarized light are likely integrated throughout the sensory-motor pathway [14], including the highly conserved central complex [4, 15, 16]. Recently, a group of Drosophila central complex cells (E-PG neurons) have been shown to function as an internal compass [17-19], similar to mammalian head-direction cells [20]. Using an array of genetic tools, we set out to test whether flies can navigate using the sun and to identify the role of E-PG cells in this behavior. Using a flight simulator, we found that Drosophila adopt arbitrary headings with respect to a simulated sun, thus performing menotaxis, and individuals remember their heading preference between successive flights-even over several hours. Imaging experiments performed on flying animals revealed that the E-PG cells track sun stimulus motion. When these neurons are silenced, flies no longer adopt and maintain arbitrary headings relative to the sun stimulus but instead exhibit frontal phototaxis. Thus, without the compass system, flies lose the ability to execute menotaxis and revert to a simpler, reflexive behavior. Despite their small brains, insects can navigate over long distances by orienting using visual landmarks [1], skylight polarization [2-9], and sun position [3, 4, 6, 10]. Although Drosophila are not generally renowned for their navigational abilities, mark-and-recapture experiments in Death Valley revealed that they can fly nearly 15 km in a single evening [11]. To accomplish such feats on available energy reserves [12], flies would have to maintain relatively straight headings, relying on celestial cues [13]. Cues such as sun position and polarized light are likely integrated throughout the sensory-motor pathway [14], including the highly conserved central complex [4, 15, 16]. Recently, a group of Drosophila central complex cells (E-PG neurons) have been shown to function as an internal compass [17-19], similar to mammalian head-direction cells [20]. Using an array of genetic tools, we set out to test whether flies can navigate using the sun and to identify the role of E-PG cells in this behavior. Using a flight simulator, we found that Drosophila adopt arbitrary headings with respect to a simulated sun, thus performing menotaxis, and individuals remember their heading preference between successive flights-even over several hours. Imaging experiments performed on flying animals revealed that the E-PG cells track sun stimulus motion. When these neurons are silenced, flies no longer adopt and maintain arbitrary headings relative to the sun stimulus but instead exhibit frontal phototaxis. Thus, without the compass system, flies lose the ability to execute menotaxis and revert to a simpler, reflexive behavior. |
| Author | Giraldo, Ysabel Milton Leitch, Katherine J Warren, Timothy L Weir, Peter T Dickinson, Michael H Ros, Ivo G |
| Author_xml | – sequence: 1 givenname: Ysabel Milton surname: Giraldo fullname: Giraldo, Ysabel Milton organization: Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA – sequence: 2 givenname: Katherine J surname: Leitch fullname: Leitch, Katherine J organization: Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA – sequence: 3 givenname: Ivo G surname: Ros fullname: Ros, Ivo G organization: Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA – sequence: 4 givenname: Timothy L surname: Warren fullname: Warren, Timothy L organization: Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA; Institute of Neuroscience, University of Oregon, Eugene, OR 97401, USA; Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR 97331, USA – sequence: 5 givenname: Peter T surname: Weir fullname: Weir, Peter T organization: Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA – sequence: 6 givenname: Michael H surname: Dickinson fullname: Dickinson, Michael H email: flyman@caltech.edu organization: Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA. Electronic address: flyman@caltech.edu |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30174187$$D View this record in MEDLINE/PubMed |
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| Snippet | Despite their small brains, insects can navigate over long distances by orienting using visual landmarks [1], skylight polarization [2-9], and sun position... Despite their small brains, insects can navigate over long distances by orienting using visual landmarks [1], skylight polarization [2-9], and sun position [3,... |
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| SubjectTerms | Animals Brain - physiology Cues Drosophila melanogaster - physiology Neurons - physiology Orientation - physiology Orientation, Spatial - physiology Sunlight |
| Title | Sun Navigation Requires Compass Neurons in Drosophila |
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