Many animals use their olfactory systems to learn to avoid dangers, but how neural circuits encode naive and learned olfactory preferences, and switch between those preferences, is poorly understood. Here, we map an olfactory network, from sensory input to motor output, which regulates the learned olfactory aversion of Caenorhabditis elegans for the smell of pathogenic bacteria. Naive animals prefer smells of pathogens but animals trained with pathogens lose this attraction. We find that two different neural circuits subserve these preferences, with one required for the naive preference and the other specifically for the learned preference. Calcium imaging and behavioral analysis reveal that the naive preference reflects the direct transduction of the activity of olfactory sensory neurons into motor response, whereas the learned preference involves modulations to signal transduction to downstream neurons to alter motor response. Thus, two different neural circuits regulate a behavioral switch between naive and learned olfactory preferences.
Bibliographical noteFunding Information:
We thank Caenorhabditis Genetics Center for C. elegans strains; Dr. Cori Bargmann, Dr. Piali Sengupta, Dr. Kyuhyung Kim, and Harvard Center for Nanoscale Systems for helps with the microfluidics system; Dr. Linjiao Luo and Dr. Mi Zhang for helps with the femtosecond laser apparatus; Dr. Edward Soucy and Dr. Joel Greenwood at Center for Brain Science Neuroengineering Facility at Harvard University for technical supports; and Dr. Junichi Nakai for the recombinant DNA clone pN1-G-CaMP. We thank Dr. Joshua Sanes, Dr. Cori Bargmann, Dr. Kenneth Blum, Dr. Catherine Dulac, and Zhang laboratory members for thoughtful comments on the manuscript. This work was supported by the funding from Howard Hughes Medical Institute (K.S.), NIH grant 4R00NS57931 (D.C.-R.), The Esther A. and Joseph Klingenstein Fund, March of Dimes Foundation, The Alfred P. Sloan Foundation, The John Merck Fund, NIH (Y.Z.) and the McKnight Foundation, NSF, and NIH (A.D.T.S.). Author contributions are as follows: Y.Z. conceived of the study; H.H., M.H., A.D.T.S., and Y.Z. designed experiments; H.H., M.H., Y.S., Y.Q., and Y.Z. performed experiments; C.V.G., C.F-Y., and A.D.T.S. provided experimental and analytical tools; D.C-R. and K.S. contributed to genetic reagents; and H.H., M.H., A.D.T.S., and Y.Z. analyzed data and wrote the article.
ASJC Scopus subject areas