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

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

Neuron. 2014 Jun 4;82(5):1115-28. doi: 10.1016/j.neuron.2014.05.010.

Authors

Affiliations

¹ 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.
² 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.
³ Center for Brain Science, Harvard University, Cambridge, MA 02138, USA; Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA.
⁴ Center for Brain Science, Harvard University, Cambridge, MA 02138, USA; Department of Physics, Harvard University, Cambridge, MA 02138, USA.
⁵ Center for Brain Science, Harvard University, Cambridge, MA 02138, USA.
⁶ Department of Biochemistry and Molecular Biophysics, Columbia University, New York, NY 10032, USA.
⁷ Program in Cellular Neuroscience, Neurodegeneration and Repair, Department of Cell Biology, Yale University School of Medicine, New Haven, CT 06536, USA.
⁸ Center for Brain Science, Harvard University, Cambridge, MA 02138, USA; Department of Physics, Harvard University, Cambridge, MA 02138, USA. Electronic address: [email protected].
⁹ Center for Brain Science, Harvard University, Cambridge, MA 02138, USA; Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA. Electronic address: [email protected].

Abstract

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.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Caenorhabditis elegans
Calcium / metabolism
Chemoreceptor Cells / physiology
Chemotaxis / physiology*
Interneurons / physiology
Memory / physiology*
Perception / physiology*

Substances

Calcium

Abstract

Publication types

MeSH terms

Substances

Grants and funding