Specific kinematics and motor-related neurons for aversive chemotaxis in drosophila

Xiaojing J. Gao, Christopher J. Potter, Daryl M. Gohl, Marion Silies, Alexander Y. Katsov, Thomas R. Clandinin, Liqun Luo

Research output: Contribution to journalArticlepeer-review

20 Scopus citations

Abstract

Background Chemotaxis, the ability to direct movements according to chemical cues in the environment, is important for the survival of most organisms. The vinegar fly, Drosophila melanogaster, displays robust olfactory aversion and attraction, but how these behaviors are executed via changes in locomotion remains poorly understood. In particular, it is not clear whether aversion and attraction bidirectionally modulate a shared circuit or recruit distinct circuits for execution. Results Using a quantitative behavioral assay, we determined that both aversive and attractive odorants modulate the initiation and direction of turns but display distinct kinematics. Using genetic tools to perturb these behaviors, we identified specific populations of neurons required for aversion, but not for attraction. Inactivation of these populations of cells affected the completion of aversive turns, but not their initiation. Optogenetic activation of the same populations of cells triggered a locomotion pattern resembling aversive turns. Perturbations in both the ellipsoid body and the ventral nerve cord, two regions involved in motor control, resulted in defects in aversion. Conclusions Aversive chemotaxis in vinegar flies triggers ethologically appropriate kinematics distinct from those of attractive chemotaxis and requires specific motor-related neurons.

Original languageEnglish (US)
Pages (from-to)1163-1172
Number of pages10
JournalCurrent Biology
Volume23
Issue number13
DOIs
StatePublished - Jul 8 2013

Bibliographical note

Funding Information:
We thank D. Luginbuhl and J. Brown for technical assistance; R.L. Davis, S.E.J. de Vries, G.S.X.E. Jefferis, M. Prakash, and T. Rohlfing for advice; B.D. Pfeiffer, A. Jenett, G.M. Rubin, and J. Simpson from the Janelia Farm for generously sharing unpublished reagents; Bloomington Drosophila Stock Center for flies; Addgene for plasmids; and C.J. Guenthner, W. Joo, T.J. Mosca, O. Riabinina, A. Ward, and B.C. Weissbourd for critiques. X.J.G. is supported by an Enlight Foundation Bio-X Interdisciplinary Fellowship. D.M.G. was supported by a Ruth L. Kirschstein National Research Service Award Postdoctoral Fellowship (F32EY020040) from the National Eye Institute. M.S. is supported by a postdoctoral fellowship from the Jane Coffin Childs Memorial Fund for Medical Research. C.J.P. was an associate and L.L. is an investigator of the Howard Hughes Medical Institute. This study was also supported by National Institutes of Health (NIH) grants R01-DC005982 (L.L.) and R01-EY022638 (T.R.C.) and an NIH Director’s Pioneer Award, DP1 OD003530 (T.R.C.).

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