CaMKI-dependent regulation of sensory gene expression mediates experience-dependent plasticity in the operating range of a thermosensory neuron

Neuron. 2014 Dec 3;84(5):919-926. doi: 10.1016/j.neuron.2014.10.046. Epub 2014 Nov 20.

Abstract

Sensory adaptation represents a form of experience-dependent plasticity that allows neurons to retain high sensitivity over a broad dynamic range. The mechanisms by which sensory neuron responses are altered on different timescales during adaptation are unclear. The threshold for temperature-evoked activity in the AFD thermosensory neurons (T*(AFD)) in C. elegans is set by the cultivation temperature (T(c)) and regulated by intracellular cGMP levels. We find that T*(AFD) adapts on both short and long timescales upon exposure to temperatures warmer than T(c), and that prolonged exposure to warmer temperatures alters expression of AFD-specific receptor guanylyl cyclase genes. These temperature-regulated changes in gene expression are mediated by the CMK-1 CaMKI enzyme, which exhibits T(c)-dependent nucleocytoplasmic shuttling in AFD. Our results indicate that CaMKI-mediated changes in sensory gene expression contribute to long-term adaptation of T*(AFD), and suggest that similar temporally and mechanistically distinct phases may regulate the operating ranges of other sensory neurons.

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

  • Adaptation, Physiological / genetics
  • Adaptation, Physiological / physiology*
  • Analysis of Variance
  • Animals
  • Animals, Genetically Modified
  • Caenorhabditis elegans
  • Caenorhabditis elegans Proteins / genetics
  • Caenorhabditis elegans Proteins / metabolism
  • Calcium / metabolism*
  • Computer Simulation
  • Cyclic GMP / metabolism
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Mitogen-Activated Protein Kinase 1 / genetics
  • Mitogen-Activated Protein Kinase 1 / metabolism*
  • Models, Neurological
  • Mutation / genetics
  • Neuronal Plasticity / genetics
  • Neuronal Plasticity / physiology*
  • Psychophysics
  • Sensory Receptor Cells / physiology*
  • Temperature
  • Thermosensing / genetics
  • Thermosensing / physiology*
  • Time Factors

Substances

  • Caenorhabditis elegans Proteins
  • Green Fluorescent Proteins
  • Mitogen-Activated Protein Kinase 1
  • Cyclic GMP
  • Calcium