Coding and Plasticity in the Mammalian Thermosensory System

Neuron. 2016 Dec 7;92(5):1079-1092. doi: 10.1016/j.neuron.2016.10.021. Epub 2016 Nov 10.

Abstract

Perception of the thermal environment begins with the activation of peripheral thermosensory neurons innervating the body surface. To understand how temperature is represented in vivo, we used genetically encoded calcium indicators to measure temperature-evoked responses in hundreds of neurons across the trigeminal ganglion. Our results show how warm, hot, and cold stimuli are represented by distinct population responses, uncover unique functional classes of thermosensory neurons mediating heat and cold sensing, and reveal the molecular logic for peripheral warmth sensing. Next, we examined how the peripheral somatosensory system is functionally reorganized to produce altered perception of the thermal environment after injury. We identify fundamental transformations in sensory coding, including the silencing and recruitment of large ensembles of neurons, providing a cellular basis for perceptual changes in temperature sensing, including heat hypersensitivity, persistence of heat perception, cold hyperalgesia, and cold analgesia.

Keywords: TRP channels; changes in peripheral coding; injury; sensory coding; temperature representation; warmth sensing.

MeSH terms

  • Animals
  • Burns / metabolism*
  • Burns / physiopathology
  • Cold Temperature
  • Hot Temperature
  • Hyperalgesia / metabolism*
  • Hyperalgesia / physiopathology
  • Hyperesthesia / metabolism*
  • Hyperesthesia / physiopathology
  • Mice
  • Mice, Knockout
  • Mice, Transgenic
  • Neuronal Plasticity
  • Neurons / metabolism*
  • Neurons / physiology
  • TRPA1 Cation Channel
  • TRPM Cation Channels / genetics
  • TRPM Cation Channels / metabolism
  • TRPV Cation Channels / genetics
  • TRPV Cation Channels / metabolism*
  • Thermosensing / physiology*
  • Transient Receptor Potential Channels / genetics
  • Transient Receptor Potential Channels / metabolism
  • Trigeminal Ganglion / cytology*
  • Trigeminal Ganglion / metabolism
  • Trigeminal Ganglion / physiology

Substances

  • TRPA1 Cation Channel
  • TRPM Cation Channels
  • TRPM8 protein, mouse
  • TRPV Cation Channels
  • TRPV1 protein, mouse
  • Transient Receptor Potential Channels
  • Trpa1 protein, mouse