Facultative blood–brain barrier and neuronal adaptation to osmotic stress in a marine osmoconformer

Abstract

IN most vertebrate and higher invertebrate animals cellular functions are critically dependent on the relative stability of the chemical composition of the body fluids, a requirement epitomised by Claude Bernard's dictum: “la fixité du milieu intérieur c'est la condition de la vie libre”¹. In higher vertebrates^2,3, and in insects⁴, but not apparently other invertebrates^5,6, the ionic homeostasis of the neuronal environment is augmented by extremely effective blood–brain barrier systems. The nerve cells of euryhaline osmoconformers, however, are exposed to considerable fluctuation in the osmotic and ionic concentrations of the body fluids⁷. As an example we studied the serpulid worm, Mercierella enigmatica (Fauvel), which occurs in waters in which the salinities vary from 1 to 55‰ (refs 8–10) and which can withstand relatively rapid variations in the osmotic concentration of the blood of between 43 and 1,620 mOsm (ref. 11). We report here that in spite of such extreme variations in osmotic and ionic concentration, the axons of Mercierella function using ionic mechanisms which seem essentially similar to those of other marine invertebrates, such as the giant axons of the squid¹² or the polychaete, Myxicola infundibulum¹³. The resting potential approximates to an ideal potassium electrode (with 58.8 mV alteration for decade change in [K⁺]_o), the action potentials are sodium-mediated (exhibiting a 55.8 mV alteration for decade change in [Na⁺]_o) and are blocked by externally applied tetrodotoxin at about 10⁻⁷ M.