Hierarchical sparse coding in the sensory system of Caenorhabditis elegans
Animals with compact sensory systems face an encoding problem where a small number of sensory neurons are required to encode information about its surrounding complex environment. Using Caenorhabditis elegans worms as a model, we ask how chemical stimuli are encoded by a small and highly connected sensory system. We first generated a comprehensive library of transgenic worms where each animal expresses a genetically encoded calcium indicator in individual sensory neurons. This library includes the vast majority of the sensory system in C. elegans. Imaging from individual sensory neurons while subjecting the worms to various stimuli allowed us to compile a comprehensive functional map of the sensory system at single neuron resolution. The functional map reveals that despite the dense wiring, chemosensory neurons represent the environment using sparse codes. Moreover, although anatomically closely connected, chemo- and mechano-sensory neurons are functionally segregated. In addition, the code is hierarchical, where few neurons participate in encoding multiple cues, whereas other sensory neurons are stimulus specific. This encoding strategy may have evolved to mitigate the constraints of a compact sensory system.
© 2015 National Academy of Sciences. Published ahead of print January 12, 2015. We thank Piali Sengupta for sharing the genetically ablated AWCON strain (PY7502). The research leading to these results has received funding from the European Research Council under the European Union's Seventh Framework Programme (FP/2007-2013) and European Research Council Grant Agreement 336803. Initial stages of this research were supported by the Caltech Center for Biological Circuit Design. P.W.S. is an investigator of the Howard Hughes Medical Institute, which supported this work. Author contributions: A.Z. and P.W.S. designed research; A.Z., I.L., O.S., S.G., and L.Y. performed research; A.Z. contributed new reagents/analytic tools; A.Z. analyzed data; and A.Z. and P.W.S. wrote the paper. The authors declare no conflict of interest. Freely available online through the PNAS open access option. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1423656112/-/DCSupplemental.
Correction for Zaslaver et al., Hierarchical sparse coding in the sensory system of Caenorhabditis elegans PNAS 2015 112 (13) E1688-E1689; published ahead of print March 11, 2015, doi:10.1073/pnas.1504344112
Published - PNAS-2015-Zaslaver-1185-9.pdf
Supplemental Material - pnas.201423656SI.pdf