Axon‐glia interactions in the crayfish: Glial cell oxygen consumption is tightly coupled to axon metabolism

Abstract

Oxygen consumption (QO2) of single isolated axons and their associated glial cell sheath was investigated under a variety of conditions to determine the contribution of each cell type to whole tissue QO2. It was found that the QO2 of the sheath, in the absence of a functional axon, represented approximately 30% of the total tissue QO2. When the axon was injected with carboxyatractyloside, an inhibitor of mitochondrial oxidative phosphorylation that is membrane impermeant, electrophysiological properties of the axon were not affected and glial sheath respiratory activity was stimulated by 1.7 to 2.7 times the untreated control level. These results suggest that glial cell metabolic activity is regulated by the metabolic activity of the axon. Depending on the experimental conditions the glial sheath accounts for 30% to nearly 100% of the QO2 of axon-glial cell tissue. On the basis of these and morphometric measurements we estimate that in a normally functioning axon-glial cell system the glial sheath accounts for 90% of the tissue QO2.

Activity‐dependent change in morphology of the glial tubular lattice of the crayfish medial giant nerve fiber

“…Consistent with the high metabolic activity of the adaxonal glial layer and its postulated role in ion transport and adaxonal space homeostasis (Hargittai and Lieberman, 1991;Lieberman et al, 1994) mitochondria, as a volume fraction (percentage of total glial cytoplasmic volume), was 3.8 6 0.5% and approximately 2 times that found in the outer glial layers.…”

Hypothesis of an Energetic Function for Myelin

“…In a normally functioning axon-glial cell system, the glial sheath was estimated to account for 90% of the absorbed O 2 [43]. Hypoxic lesions during the perinatal period in humans were shown to be limited to areas of primary myelination [44].…”

Synthesis and release of N-acetylaspartylglutamate (NAAG) by crayfish nerve fibers: implications for axon–glia signaling

“…Based upon our previous studies, the thickness of the nerve ¢ber's wall (i.e. of the periaxonal glial sheath) was taken to be 8 Wm and the volume of glial cytoplasm was taken to be 45% of the total volume of glial sheath (Hargittai and Lieberman, 1991). Although glial cytoplasm represents only 5% of the total volume of axoplasm and gliaplasm combined, glia account for 75% of radiolabeled glutamate uptake (Kane et al, 2000) and 95% of O 2 consumption of the MGNF (Hargittai and Lieberman, 1991).…”

“…of the periaxonal glial sheath) was taken to be 8 Wm and the volume of glial cytoplasm was taken to be 45% of the total volume of glial sheath (Hargittai and Lieberman, 1991). Although glial cytoplasm represents only 5% of the total volume of axoplasm and gliaplasm combined, glia account for 75% of radiolabeled glutamate uptake (Kane et al, 2000) and 95% of O 2 consumption of the MGNF (Hargittai and Lieberman, 1991). To insure that comparisons of radiolabel uptake and distribution between axons and glia were representative of the true metabolic capacity of these two cellular compartments, volume calculations of axoplasm and glial cytoplasm were made and radiolabel content was normalized and expressed in units of counts/min/Wl cytoplasm.…”