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The Journal of Neuroscience, August 15, 1998, 18(16):6059-6070

Synaptic Vesicular Localization and Exocytosis of L-Aspartate in Excitatory Nerve Terminals: A Quantitative Immunogold Analysis in Rat Hippocampus

Vidar Gundersen¹, Farrukh A. Chaudhry¹, Jan G. Bjaalie¹, Frode Fonnum², Ole Petter Ottersen¹, and Jon Storm-Mathisen¹

¹ Department of Anatomy, Institute of Basic Medical Sciences, University of Oslo, Blindern, N-0317 Oslo, Norway, and ² Vista, Norwegian Research Establishment, Division for Environmental Toxicology, N-2007 Kjeller, Norway

To elucidate the role of aspartate as a signal molecule in the brain, its localization and those of related amino acids were examined by light and electron microscopic quantitative immunocytochemistry using antibodies specifically recognizing the aldehyde-fixed amino acids. Rat hippocampal slices were incubated at physiological and depolarizing [K⁺] before glutaraldehyde fixation. At normal [K⁺], aspartate-like and glutamate-like immunoreactivities were colocalized in nerve terminals forming asymmetrical synapses on spines in stratum radiatum of CA1 and the inner molecular layer of fascia dentata (i.e., excitatory afferents from CA3 and hilus, respectively). During K⁺ depolarization there was a loss of aspartate and glutamate from these terminals. Simultaneously the immunoreactivities strongly increased in glial cells. These changes were Ca²⁺-dependent and tetanus toxin-sensitive and did not comprise taurine-like immunoreactivity. Adding glutamine at CSF concentration prevented the loss of aspartate and glutamate and revealed an enhancement of aspartate in the terminals at moderate depolarization.

In hippocampi from animals perfused with glutaraldehyde during insulin-induced hypoglycemia (to combine a strong aspartate signal with good ultrastructure) aspartate was colocalized with glutamate in excitatory terminals in stratum radiatum of CA1. The synaptic vesicle-to-cytoplasmic matrix ratios of immunogold particle density were similar for aspartate and glutamate, significantly higher than those observed for glutamine or taurine. Similar results were obtained in normoglycemic animals, although the nerve terminal contents of aspartate were lower. The results indicate that aspartate can be concentrated in synaptic vesicles and subject to sustained exocytotic release from the same nerve endings that contain and release glutamate.

Key words: immunogold localization; L-aspartate; L-glutamate; electron microscopy; synaptic vesicles; nerve endings; astroglia; glutamine; hypoglycemia

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Copyright © 1998 Society for Neuroscience  0270-6474/98/18166059-12$05.00/0

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