Cytochemical and cytological properties of perineuronal oligodendrocytes in the mouse cortex

Abstract

Neuronal cell bodies are associated with glial cells collectively referred to as perineuronal satellite cells. One such satellite cell is the perineuronal oligodendrocyte, which is unmyelinating oligodendrocytes attaching to large neurons in various neural regions. However, little is known about their cellular characteristics and function. In this study, we identified perineuronal oligodendrocytes as 2′,3′‐cyclic nucleotide 3′‐phosphodiesterase‐positive cells attaching to neuronal perikarya immunostained for microtubule‐associated protein 2, and examined their cytochemical and cytological properties in the mouse cerebral cortex. 2′,3′‐Cyclic nucleotide 3′‐phosphodiesterase‐positive perineuronal oligodendrocytes were immunonegative to representative glial markers for astrocytes (brain‐type lipid binding protein and glial fibrillary acidic protein), microglia (Iba‐1) and NG2+ glia. However, almost all perineuronal oligodendrocytes expressed glia‐specific or glia‐enriched metabolic enzymes, i.e. the creatine synthetic enzyme S‐adenosylmethionine:guanidinoacetate N‐methyltransferase and l‐serine biosynthetic enzyme 3‐phosphoglycerate dehydrogenase. As to molecules participating in the glutamate–glutamine cycle, none of the perineuronal oligodendrocytes expressed the plasmalemmal glutamate transporters GLAST and GLT‐1, although nearly half of the perineuronal oligodendrocytes were immunopositive for glutamine synthetase. Cytologically, perineuronal oligodendrocytes were mainly distributed in deep cortical layers (layers IV–VI), and attached directly and tightly to neuronal cell bodies, making a long concave impression to the contacting neurons. Interestingly, they attached more to glutamatergic principal neurons than to GABAergic interneurons, and this became evident at postnatal day 14, when the cerebral cortex develops and maturates. These cytochemical and cytological properties suggest that perineuronal oligodendrocytes are so differentiated as to fulfill metabolic support to the associating principal cortical neurons, rather than to regulate their synaptic transmission.