Beating the competition: the reliability hypothesis for Mauthner axon size

Brain Behav Evol. 1995;45(4):183-94. doi: 10.1159/000113549.

Abstract

The Mauthner cell has an axon that is among the largest in diameter of any vertebrate neuron. It is commonly thought that the large size is needed for short latency escape responses involving a major contraction of the trunk musculature. Previous work, however, has shown that there is nothing unique about the strength of the Mauthner initiated response, compared to responses initiated by other smaller cells, and it is debatable that there is any important improvement in response latency due to Mauthner axon size. In this paper we advance an alternative explanation: although the Mauthner cell has a powerful excitatory influence on motoneurons, the large size of the Mauthner axon is most important in rapidly spreading an inhibitory signal that turns off other competing motor commands. Such competing commands are likely to arise in the presence of ongoing swimming behavior or ambiguous stimuli that could activate a fast turn either toward or away from the stimulus. These stimuli include apparent food items, or lures, presented by predators (such as anglerfish) and escape eliciting sounds which, in the presence of background noise, may have 180 degrees directional ambiguity. Thus, large size of the axon contributes most to the reliable expression of the escape behavior. We base this reliability hypothesis on a retrospective analysis of previous neurophysiological data and new anatomical measurements of the diameters of the large spinal cord axons from which we calculated conduction velocities. Our calculations show that the Mauthner-derived inhibition is fast enough that it allows an escape response to occur even when a conflicting motor command enters the spinal cord at the same time as the Mauthner axon impulse. The rapid spread of inhibitory influence, along with excitation, may be a general feature of motor system cells with large axonal diameters.

Publication types

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

MeSH terms

  • Animals
  • Axons / ultrastructure*
  • Brain Stem / anatomy & histology
  • Cell Size
  • Escape Reaction / physiology
  • Goldfish / anatomy & histology*
  • Motor Activity / physiology*
  • Motor Neurons / ultrastructure*
  • Neural Inhibition / physiology*
  • Neural Pathways / anatomy & histology
  • Reticular Formation / anatomy & histology
  • Spinal Cord / anatomy & histology*
  • Swimming
  • Synaptic Transmission / physiology*