Integration of Plasticity Mechanisms within a Single Sensory Neuron of C. elegans Actuates a Memory

Neuron. 2018 Jan 17;97(2):356-367.e4. doi: 10.1016/j.neuron.2017.12.027. Epub 2018 Jan 4.

Abstract

Neural plasticity, the ability of neurons to change their properties in response to experiences, underpins the nervous system's capacity to form memories and actuate behaviors. How different plasticity mechanisms act together in vivo and at a cellular level to transform sensory information into behavior is not well understood. We show that in Caenorhabditis elegans two plasticity mechanisms-sensory adaptation and presynaptic plasticity-act within a single cell to encode thermosensory information and actuate a temperature preference memory. Sensory adaptation adjusts the temperature range of the sensory neuron (called AFD) to optimize detection of temperature fluctuations associated with migration. Presynaptic plasticity in AFD is regulated by the conserved kinase nPKCε and transforms thermosensory information into a behavioral preference. Bypassing AFD presynaptic plasticity predictably changes learned behavioral preferences without affecting sensory responses. Our findings indicate that two distinct neuroplasticity mechanisms function together through a single-cell logic system to enact thermotactic behavior. VIDEO ABSTRACT.

Keywords: C. elegans; learning and memory; presynaptic plasticity; sensory adaptation; synaptic plasticity; thermotaxis behavior.

Publication types

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

MeSH terms

  • Animals
  • Animals, Genetically Modified
  • Caenorhabditis elegans / genetics
  • Caenorhabditis elegans / physiology*
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / physiology
  • Calcium / physiology
  • Memory / physiology*
  • Mutation
  • Neuronal Plasticity / physiology*
  • Patch-Clamp Techniques
  • Protein Kinase C / genetics
  • Protein Kinase C / physiology
  • Sensory Receptor Cells / physiology*
  • Single-Cell Analysis
  • Taxis Response / physiology*
  • Temperature
  • Thermosensing / physiology
  • Transgenes

Substances

  • Caenorhabditis elegans Proteins
  • Protein Kinase C
  • Calcium