Extreme tolerance to ammonia fumes in African naked mole-rats: animals that naturally lack neuropeptides from trigeminal chemosensory nerve fibers

J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2009 May;195(5):419-27. doi: 10.1007/s00359-009-0420-0. Epub 2009 Feb 15.

Abstract

Naked mole-rats (Heterocephalus glaber) naturally lack neuropeptides associated with the signaling of chemical irritants from C type trigeminal nerve fibers. The goal of the present study was to assess behavioral responses of these animals to stimulation of the trigeminal chemosensory system, and to determine if stimulation would increase post-synaptic activity in the trigeminal nucleus, as seen in laboratory mice and rats. The results show that naked mole-rats are behaviorally insensitive to capsaicin solution applied to the nostrils and to ammonia fumes in a behavioral avoidance test. Centrally, the number of c Fos labeled cells in the spinal trigeminal nucleus increased from exposure to ammonia although the magnitude of the increase was less than for rats. The increase observed in naked mole-rats likely reflects activity from glutamate release, which appears insufficient to drive pain and aversion behaviors. The results support the idea that neuropeptides in the C fibers of the trigeminal system may be required to signal the aversive quality of specific chemical irritants. The natural lack of neuropeptides in naked mole-rats may be an adaptation to living in a challenging subterranean environment with extremely high levels of ammonia and carbon dioxide, stimuli known to excite trigeminal chemosensory C fibers.

Publication types

  • Comparative Study
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Ammonia / pharmacology*
  • Ammonia / toxicity
  • Animals
  • Capsaicin / pharmacology
  • Capsaicin / toxicity
  • Central Nervous System / chemistry
  • Discrimination Learning
  • Exploratory Behavior / drug effects
  • Glutamic Acid / metabolism
  • Irritants / pharmacology*
  • Irritants / toxicity
  • Mice
  • Mice, Inbred C57BL
  • Mole Rats / physiology*
  • Nerve Fibers, Unmyelinated / drug effects
  • Nerve Fibers, Unmyelinated / physiology*
  • Nerve Tissue Proteins / analysis
  • Neuropeptides
  • Nicotine / pharmacology
  • Nociceptors / drug effects*
  • Odorants
  • Olivary Nucleus / chemistry
  • Olivary Nucleus / drug effects*
  • Proto-Oncogene Proteins c-fos / analysis
  • Rats
  • Rats, Long-Evans
  • Rats, Sprague-Dawley
  • Single-Blind Method
  • Solitary Nucleus / chemistry
  • Solitary Nucleus / drug effects*
  • Species Specificity
  • Trigeminal Nucleus, Spinal / chemistry
  • Trigeminal Nucleus, Spinal / drug effects*

Substances

  • Irritants
  • Nerve Tissue Proteins
  • Neuropeptides
  • Proto-Oncogene Proteins c-fos
  • Glutamic Acid
  • Nicotine
  • Ammonia
  • Capsaicin