Dynamic encoding of perception, memory, and movement in a C. elegans chemotaxis circuit

Linjiao Luo; Quan Wen; Jing Ren; Michael Hendricks; Marc Gershow; Yuqi Qin; Joel Greenwood; Edward R Soucy; Mason Klein; Heidi K Smith-Parker; Ana C Calvo; Daniel A Colón-Ramos; Aravinthan D T Samuel; Yun Zhang

doi:10.1016/j.neuron.2014.05.010

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Dynamic encoding of perception, memory, and movement in a C. elegans chemotaxis circuit

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Dynamic encoding of perception, memory, and movement in a C. elegans chemotaxis circuit

Linjiao Luo, Quan Wen, Jing Ren, Michael Hendricks, Marc Gershow, Yuqi Qin, Joel Greenwood, Edward R Soucy, Mason Klein, Heidi K Smith-Parker, …

Neuron (Cambridge, Mass.), Vol.82(5), pp.1115-1128

2014-06-04

DOI: https://doi.org/10.1016/j.neuron.2014.05.010

PMCID: PMC4082684

PMID: 24908490

Abstract

Caenorhabditis elegans

Interneurons - physiology

Animals

Chemotaxis - physiology

Calcium - metabolism

Perception - physiology

Chemoreceptor Cells - physiology

Memory - physiology

Brain circuits endow behavioral flexibility. Here, we study circuits encoding flexible chemotaxis in C. elegans, where the animal navigates up or down NaCl gradients (positive or negative chemotaxis) to reach the salt concentration of previous growth (the set point). The ASER sensory neuron mediates positive and negative chemotaxis by regulating the frequency and direction of reorientation movements in response to salt gradients. Both salt gradients and set point memory are encoded in ASER temporal activity patterns. Distinct temporal activity patterns in interneurons immediately downstream of ASER encode chemotactic movement decisions. Different interneuron combinations regulate positive versus negative chemotaxis. We conclude that sensorimotor pathways are segregated immediately after the primary sensory neuron in the chemotaxis circuit, and sensory representation is rapidly transformed to motor representation at the first interneuron layer. Our study reveals compact encoding of perception, memory, and locomotion in an experience-dependent navigational behavior in C. elegans.

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Collaboration types: Domestic collaboration; International collaboration
Citation topics: 1 Clinical & Life Sciences; 1.264 Longevity; 1.264.618 Caenorhabditis Elegans
Web Of Science research areas: Neurosciences
ESI research areas: Neuroscience & Behavior

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Title: Dynamic encoding of perception, memory, and movement in a C. elegans chemotaxis circuit
Creators: Linjiao Luo - Key Laboratory of Modern Acoustics, Ministry of Education, Department of Physics, Nanjing University, China; Center for Brain Science, Harvard University, Cambridge, MA 02138, USA; Department of Physics, Harvard University, Cambridge, MA 02138, USA
Quan Wen - Center for Brain Science, Harvard University, Cambridge, MA 02138, USA; Department of Physics, Harvard University, Cambridge, MA 02138, USA; Department of Neurobiology and Biophysics, School of Life Sciences, University of Science and Technology of China, China
Jing Ren - Center for Brain Science, Harvard University, Cambridge, MA 02138, USA; Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA
Michael Hendricks - Center for Brain Science, Harvard University, Cambridge, MA 02138, USA; Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA
Marc Gershow - Center for Brain Science, Harvard University, Cambridge, MA 02138, USA; Department of Physics, Harvard University, Cambridge, MA 02138, USA
Yuqi Qin - Center for Brain Science, Harvard University, Cambridge, MA 02138, USA; Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA
Joel Greenwood - Center for Brain Science, Harvard University, Cambridge, MA 02138, USA
Edward R Soucy - Center for Brain Science, Harvard University, Cambridge, MA 02138, USA
Mason Klein - Center for Brain Science, Harvard University, Cambridge, MA 02138, USA; Department of Physics, Harvard University, Cambridge, MA 02138, USA
Heidi K Smith-Parker - Department of Biochemistry and Molecular Biophysics, Columbia University, New York, NY 10032, USA
Ana C Calvo - Program in Cellular Neuroscience, Neurodegeneration and Repair, Department of Cell Biology, Yale University School of Medicine, New Haven, CT 06536, USA
Daniel A Colón-Ramos - Program in Cellular Neuroscience, Neurodegeneration and Repair, Department of Cell Biology, Yale University School of Medicine, New Haven, CT 06536, USA
Aravinthan D T Samuel - Center for Brain Science, Harvard University, Cambridge, MA 02138, USA; Department of Physics, Harvard University, Cambridge, MA 02138, USA. Electronic address: samuel@physics.harvard.edu
Yun Zhang - Center for Brain Science, Harvard University, Cambridge, MA 02138, USA; Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA. Electronic address: yzhang@oeb.harvard.edu
Publication Details: Neuron (Cambridge, Mass.), Vol.82(5), pp.1115-1128
Publisher: United States
Grant note: 8DP1GM105383-05 / NCCDPHP CDC HHS P01 GM103770 / NIGMS NIH HHS P01GM103770 / NIGMS NIH HHS R01 NS076558 / NINDS NIH HHS R01DC009852 / NIDCD NIH HHS R01 DC009852 / NIDCD NIH HHS P40 OD010440 / NIH HHS 1P01GM103770 / NIGMS NIH HHS R01NS076558 / NINDS NIH HHS DP1 GM105383 / NIGMS NIH HHS
Academic Unit: College of A&S; A&S - Physics
Language: English
Resource Type: Journal article
PMID: 24908490
PMCID: PMC4082684
Record Identifier: 991031559279602976