Neuronal control of locomotor handedness in Drosophila
Edited by Ralph J. Greenspan, University of California, San Diego, La Jolla, CA, and accepted by the Editorial Board April 16, 2015 (received for review January 13, 2015)
Research Article
May 7, 2015
Significance
Genetically identical individuals display variability in their behaviors even when reared in essentially identical environments. This variation underlies both personality and individuality, but there is little mechanistic understanding of how such differences arise. Here, we investigated individual-to-individual variation in locomotor behaviors of fruit flies. Surprisingly, individual flies exhibit significant bias in their left vs. right locomotor choices during exploratory locomotion, with some flies being strongly left biased or right biased. Using the Drosophila genetic toolkit, we find that the magnitude of locomotor handedness is under the control of neurons within a brain region implicated in motor planning and execution. This observation intriguingly implies that the brain may be able to dynamically regulate behavioral individuality.
Abstract
Genetically identical individuals display variability in their physiology, morphology, and behaviors, even when reared in essentially identical environments, but there is little mechanistic understanding of the basis of such variation. Here, we investigated whether Drosophila melanogaster displays individual-to-individual variation in locomotor behaviors. We developed a new high-throughout platform capable of measuring the exploratory behavior of hundreds of individual flies simultaneously. With this approach, we find that, during exploratory walking, individual flies exhibit significant bias in their left vs. right locomotor choices, with some flies being strongly left biased or right biased. This idiosyncrasy was present in all genotypes examined, including wild-derived populations and inbred isogenic laboratory strains. The biases of individual flies persist for their lifetime and are nonheritable: i.e., mating two left-biased individuals does not yield left-biased progeny. This locomotor handedness is uncorrelated with other asymmetries, such as the handedness of gut twisting, leg-length asymmetry, and wing-folding preference. Using transgenics and mutants, we find that the magnitude of locomotor handedness is under the control of columnar neurons within the central complex, a brain region implicated in motor planning and execution. When these neurons are silenced, exploratory laterality increases, with more extreme leftiness and rightiness. This observation intriguingly implies that the brain may be able to dynamically regulate behavioral individuality.
Acknowledgments
We thank Mike Burns, Chris Stokes, and other members of The Rowland Institute for fruitful scientific discussions and technical assistance, as well as Julien Ayroles, Kit Longden, Frank Hirth, Tom Maniatis, Charles Zuker, and members of their laboratories for helpful feedback. We thank Shmuel Raz, Roland Strauss, Michael Reiser, Aravi Samuel, Sam Kunes, Chuntao Dan, Douglas Armstrong, and Hiromu Tanimoto for sharing fly lines. We thank the Janelia Farm FlyLight consortium for allowing us to reuse and modify their GAL4 expression images. This research was funded in part by the Junior Fellows Program at The Rowland Institute at Harvard.
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Published online: May 7, 2015
Published in issue: May 26, 2015
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Acknowledgments
We thank Mike Burns, Chris Stokes, and other members of The Rowland Institute for fruitful scientific discussions and technical assistance, as well as Julien Ayroles, Kit Longden, Frank Hirth, Tom Maniatis, Charles Zuker, and members of their laboratories for helpful feedback. We thank Shmuel Raz, Roland Strauss, Michael Reiser, Aravi Samuel, Sam Kunes, Chuntao Dan, Douglas Armstrong, and Hiromu Tanimoto for sharing fly lines. We thank the Janelia Farm FlyLight consortium for allowing us to reuse and modify their GAL4 expression images. This research was funded in part by the Junior Fellows Program at The Rowland Institute at Harvard.
Notes
This article is a PNAS Direct Submission. R.J.G. is a guest editor invited by the Editorial Board.
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The authors declare no conflict of interest.
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