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Research Article

Eight pairs of descending visual neurons in the dragonfly give wing motor centers accurate population vector of prey direction

Paloma T. Gonzalez-Bellido, Hanchuan Peng, Jinzhu Yang, Apostolos P. Georgopoulos, and Robert M. Olberg
  1. aJanelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
  2. bProgram in Sensory Physiology and Behavior, Marine Biological Laboratory, Woods Hole, MA 02543;
  3. cDepartment of Neuroscience, University of Minnesota, Minneapolis, MN 55455; and
  4. dDepartment of Biology, Union College, Schenectady, NY 12308

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PNAS January 8, 2013 110 (2) 696-701; https://doi.org/10.1073/pnas.1210489109
Paloma T. Gonzalez-Bellido
aJanelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
bProgram in Sensory Physiology and Behavior, Marine Biological Laboratory, Woods Hole, MA 02543;
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  • For correspondence: paloma@mbl.edu
Hanchuan Peng
aJanelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
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Jinzhu Yang
aJanelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
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Apostolos P. Georgopoulos
cDepartment of Neuroscience, University of Minnesota, Minneapolis, MN 55455; and
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  • For correspondence: omega@umn.edu
Robert M. Olberg
aJanelia Farm Research Campus, Howard Hughes Medical Institute, Ashburn, VA 20147;
dDepartment of Biology, Union College, Schenectady, NY 12308
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  1. Edited by Richard A. Andersen, California Institute of Technology, Pasadena, CA, and approved October 26, 2012 (received for review June 20, 2012)

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Abstract

Intercepting a moving object requires prediction of its future location. This complex task has been solved by dragonflies, who intercept their prey in midair with a 95% success rate. In this study, we show that a group of 16 neurons, called target-selective descending neurons (TSDNs), code a population vector that reflects the direction of the target with high accuracy and reliability across 360°. The TSDN spatial (receptive field) and temporal (latency) properties matched the area of the retina where the prey is focused and the reaction time, respectively, during predatory flights. The directional tuning curves and morphological traits (3D tracings) for each TSDN type were consistent among animals, but spike rates were not. Our results emphasize that a successful neural circuit for target tracking and interception can be achieved with few neurons and that in dragonflies this information is relayed from the brain to the wing motor centers in population vector form.

  • vision
  • invertebrate
  • predatory behavior
  • electrophysiology
  • confocal microscopy

Footnotes

  • ↵1To whom correspondence may be addressed. E-mail: paloma{at}mbl.edu.
  • ↵2Present address: Allen Institute for Brain Science, Seattle, WA 98103.

  • ↵3Present address: Northeastern University, Shenyang 110819, China.

  • ↵4To whom correspondence should be addressed. E-mail: omega{at}umn.edu.
  • Author contributions: P.T.G.-B. and R.M.O. designed research; P.T.G.-B., H.P., and J.Y. performed research; P.T.G.-B., H.P., A.P.G., and R.M.O. analyzed data; and P.T.G.-B., H.P., A.P.G., and R.M.O. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • See Commentary on page 389.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1210489109/-/DCSupplemental.

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Directional population vector code in a dragonfly
Paloma T. Gonzalez-Bellido, Hanchuan Peng, Jinzhu Yang, Apostolos P. Georgopoulos, Robert M. Olberg
Proceedings of the National Academy of Sciences Jan 2013, 110 (2) 696-701; DOI: 10.1073/pnas.1210489109

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Directional population vector code in a dragonfly
Paloma T. Gonzalez-Bellido, Hanchuan Peng, Jinzhu Yang, Apostolos P. Georgopoulos, Robert M. Olberg
Proceedings of the National Academy of Sciences Jan 2013, 110 (2) 696-701; DOI: 10.1073/pnas.1210489109
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  • Biological Sciences
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