Literature DB >> 25583501

Hierarchical sparse coding in the sensory system of Caenorhabditis elegans.

Alon Zaslaver1, Idan Liani2, Oshrat Shtangel2, Shira Ginzburg2, Lisa Yee3, Paul W Sternberg4.   

Abstract

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.

Entities:  

Keywords:  calcium imagaing; neural circuits; sensory coding

Mesh:

Substances:

Year:  2015        PMID: 25583501      PMCID: PMC4313814          DOI: 10.1073/pnas.1423656112

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  36 in total

1.  Chemosensory neurons with overlapping functions direct chemotaxis to multiple chemicals in C. elegans.

Authors:  C I Bargmann; H R Horvitz
Journal:  Neuron       Date:  1991-11       Impact factor: 17.173

2.  High local genetic diversity and low outcrossing rate in Caenorhabditis elegans natural populations.

Authors:  Antoine Barrière; Marie-Anne Félix
Journal:  Curr Biol       Date:  2005-07-12       Impact factor: 10.834

3.  The fundamental role of pirouettes in Caenorhabditis elegans chemotaxis.

Authors:  J T Pierce-Shimomura; T M Morse; S R Lockery
Journal:  J Neurosci       Date:  1999-11-01       Impact factor: 6.167

4.  Metazoan operons accelerate recovery from growth-arrested states.

Authors:  Alon Zaslaver; L Ryan Baugh; Paul W Sternberg
Journal:  Cell       Date:  2011-06-10       Impact factor: 41.582

5.  The neural network for chemotaxis to tastants in Caenorhabditis elegans is specialized for temporal differentiation.

Authors:  Tod R Thiele; Serge Faumont; Shawn R Lockery
Journal:  J Neurosci       Date:  2009-09-23       Impact factor: 6.167

6.  Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis.

Authors:  Hiroshi Suzuki; Tod R Thiele; Serge Faumont; Marina Ezcurra; Shawn R Lockery; William R Schafer
Journal:  Nature       Date:  2008-07-03       Impact factor: 49.962

7.  Optical interrogation of neural circuits in Caenorhabditis elegans.

Authors:  Zengcai V Guo; Anne C Hart; Sharad Ramanathan
Journal:  Nat Methods       Date:  2009-11-08       Impact factor: 28.547

8.  High-throughput imaging of neuronal activity in Caenorhabditis elegans.

Authors:  Johannes Larsch; Donovan Ventimiglia; Cornelia I Bargmann; Dirk R Albrecht
Journal:  Proc Natl Acad Sci U S A       Date:  2013-10-21       Impact factor: 11.205

9.  Neuropeptide signaling remodels chemosensory circuit composition in Caenorhabditis elegans.

Authors:  Sarah G Leinwand; Sreekanth H Chalasani
Journal:  Nat Neurosci       Date:  2013-09-08       Impact factor: 24.884

10.  A novel molecular solution for ultraviolet light detection in Caenorhabditis elegans.

Authors:  Stacey L Edwards; Nicole K Charlie; Marie C Milfort; Brandon S Brown; Christen N Gravlin; Jamie E Knecht; Kenneth G Miller
Journal:  PLoS Biol       Date:  2008-08-05       Impact factor: 8.029

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  41 in total

1.  Multiple excitatory and inhibitory neural signals converge to fine-tune Caenorhabditis elegans feeding to food availability.

Authors:  Nicolas Dallière; Nikhil Bhatla; Zara Luedtke; Dengke K Ma; Jonathan Woolman; Robert J Walker; Lindy Holden-Dye; Vincent O'Connor
Journal:  FASEB J       Date:  2015-10-29       Impact factor: 5.191

2.  What about the males? the C. elegans sexually dimorphic nervous system and a CRISPR-based tool to study males in a hermaphroditic species.

Authors:  Jonathon D Walsh; Olivier Boivin; Maureen M Barr
Journal:  J Neurogenet       Date:  2020-07-10       Impact factor: 1.250

Review 3.  Multisensory integration in C. elegans.

Authors:  D Dipon Ghosh; Michael N Nitabach; Yun Zhang; Gareth Harris
Journal:  Curr Opin Neurobiol       Date:  2017-03-06       Impact factor: 6.627

4.  Circuit mechanisms encoding odors and driving aging-associated behavioral declines in Caenorhabditis elegans.

Authors:  Sarah G Leinwand; Claire J Yang; Daphne Bazopoulou; Nikos Chronis; Jagan Srinivasan; Sreekanth H Chalasani
Journal:  Elife       Date:  2015-09-22       Impact factor: 8.140

5.  A Single-Neuron Chemosensory Switch Determines the Valence of a Sexually Dimorphic Sensory Behavior.

Authors:  Kelli A Fagan; Jintao Luo; Ross C Lagoy; Frank C Schroeder; Dirk R Albrecht; Douglas S Portman
Journal:  Curr Biol       Date:  2018-03-08       Impact factor: 10.834

6.  Efficient One-Step Fusion PCR Based on Dual-Asymmetric Primers and Two-Step Annealing.

Authors:  Yilan Liu; Jinjin Chen; Anders Thygesen
Journal:  Mol Biotechnol       Date:  2018-02       Impact factor: 2.695

7.  Chemosensory signal transduction in Caenorhabditis elegans.

Authors:  Denise M Ferkey; Piali Sengupta; Noelle D L'Etoile
Journal:  Genetics       Date:  2021-03-31       Impact factor: 4.562

Review 8.  Olfactory circuits and behaviors of nematodes.

Authors:  Sophie Rengarajan; Elissa A Hallem
Journal:  Curr Opin Neurobiol       Date:  2016-09-23       Impact factor: 6.627

9.  A natural variant and engineered mutation in a GPCR promote DEET resistance in C. elegans.

Authors:  Emily J Dennis; May Dobosiewicz; Xin Jin; Laura B Duvall; Philip S Hartman; Cornelia I Bargmann; Leslie B Vosshall
Journal:  Nature       Date:  2018-09-26       Impact factor: 49.962

10.  Reliability of an interneuron response depends on an integrated sensory state.

Authors:  May Dobosiewicz; Qiang Liu; Cornelia I Bargmann
Journal:  Elife       Date:  2019-11-13       Impact factor: 8.140

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