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Proc Natl Acad Sci U S A. 2015 Jan 13;112(2):E220-9. doi: 10.1073/pnas.1416212112. Epub 2014 Dec 30.

Sensory determinants of behavioral dynamics in Drosophila thermotaxis.

Author information

  • 1Department of Physics and Center for Brain Science, Harvard University, Cambridge, MA 02138;
  • 2Department of Physics and Center for Brain Science, Harvard University, Cambridge, MA 02138; Janelia Farm Research Campus, Ashburn, VA 20147;
  • 3Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, CT 06511; The John B. Pierce Laboratory, Inc., New Haven, CT 06519;
  • 4Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, CT 06511; Department of Genetics and Program in Cellular Neuroscience, Neurodegeneration, and Repair, Yale School of Medicine, New Haven, CT 06520;
  • 5Janelia Farm Research Campus, Ashburn, VA 20147;
  • 6Janelia Farm Research Campus, Ashburn, VA 20147; Institute of Cell and Developmental Biology, Department of Biology, University of Fribourg, 1700 Fribourg, Switzerland; and.
  • 7Department of Biology, Brandeis University, Waltham, MA 02435.
  • 8Department of Physics and Center for Brain Science, Harvard University, Cambridge, MA 02138; Janelia Farm Research Campus, Ashburn, VA 20147; samuel@physics.harvard.edu.

Abstract

Complex animal behaviors are built from dynamical relationships between sensory inputs, neuronal activity, and motor outputs in patterns with strategic value. Connecting these patterns illuminates how nervous systems compute behavior. Here, we study Drosophila larva navigation up temperature gradients toward preferred temperatures (positive thermotaxis). By tracking the movements of animals responding to fixed spatial temperature gradients or random temperature fluctuations, we calculate the sensitivity and dynamics of the conversion of thermosensory inputs into motor responses. We discover three thermosensory neurons in each dorsal organ ganglion (DOG) that are required for positive thermotaxis. Random optogenetic stimulation of the DOG thermosensory neurons evokes behavioral patterns that mimic the response to temperature variations. In vivo calcium and voltage imaging reveals that the DOG thermosensory neurons exhibit activity patterns with sensitivity and dynamics matched to the behavioral response. Temporal processing of temperature variations carried out by the DOG thermosensory neurons emerges in distinct motor responses during thermotaxis.

KEYWORDS:

calcium imaging; navigation; reverse correlation; temperature; voltage imaging

PMID:
25550513
PMCID:
PMC4299240
DOI:
10.1073/pnas.1416212112
[PubMed - indexed for MEDLINE]
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