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
Hauptverfasser: Giraldo, Ysabel Milton, Leitch, Katherine J, Ros, Ivo G, Warren, Timothy L, Weir, Peter T, Dickinson, Michael H
Format: Journal Article
Sprache:Englisch
Veröffentlicht: England 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.
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
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  givenname: Ysabel Milton
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  fullname: Giraldo, Ysabel Milton
  organization: Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA
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  givenname: Katherine J
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  fullname: Leitch, Katherine J
  organization: Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA
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  surname: Ros
  fullname: Ros, Ivo G
  organization: Division of Biology and Biological Engineering, California Institute of Technology, Pasadena, CA 91125, USA
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  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
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  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
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Keywords central complex
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sun compass
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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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