Diversity amongst trigeminal neurons revealed by high throughput single cell sequencing

PLoS One. 2017 Sep 28;12(9):e0185543. doi: 10.1371/journal.pone.0185543. eCollection 2017.

Abstract

The trigeminal ganglion contains somatosensory neurons that detect a range of thermal, mechanical and chemical cues and innervate unique sensory compartments in the head and neck including the eyes, nose, mouth, meninges and vibrissae. We used single-cell sequencing and in situ hybridization to examine the cellular diversity of the trigeminal ganglion in mice, defining thirteen clusters of neurons. We show that clusters are well conserved in dorsal root ganglia suggesting they represent distinct functional classes of somatosensory neurons and not specialization associated with their sensory targets. Notably, functionally important genes (e.g. the mechanosensory channel Piezo2 and the capsaicin gated ion channel Trpv1) segregate into multiple clusters and often are expressed in subsets of cells within a cluster. Therefore, the 13 genetically-defined classes are likely to be physiologically heterogeneous rather than highly parallel (i.e., redundant) lines of sensory input. Our analysis harnesses the power of single-cell sequencing to provide a unique platform for in silico expression profiling that complements other approaches linking gene-expression with function and exposes unexpected diversity in the somatosensory system.

MeSH terms

  • Animals
  • Capsaicin / pharmacology
  • Ganglia, Spinal / cytology
  • High-Throughput Screening Assays*
  • Ion Channel Gating / drug effects
  • Mice
  • Neurons / cytology*
  • Single-Cell Analysis*
  • TRPV Cation Channels / drug effects
  • TRPV Cation Channels / physiology
  • Transcriptome
  • Trigeminal Nerve / cytology*

Substances

  • TRPV Cation Channels
  • TRPV1 protein, mouse
  • Capsaicin

Grant support

This work was supported by the Intramural program of the National Institutes of Health, National Institute of Dental and Craniofacial Research (N.J.P.R.) ZIA-DE000561. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.