Glial and neuronal glutamine pools at glutamatergic synapses with distinct properties

The main pathway for transmitter glutamate turnover in excitatory synapses is thought to involve an uptake in glial processes, a conversion into glutamine, which recycles to the presynaptic terminal to serve as the main precursor for new synthesis of glutamate. To investigate whether the mechanisms of glutamine and glutamate turnover are linked with the properties of different glutamate synapses, the distribution of glutamine was studied in two types of glutamate synapse in the lamprey spinal cord using immunogold post-embedding electron microscopy. The synapses examined are formed by primary afferent axons (dorsal column axons), which predominantly exhibit a tonic firing pattern, and by giant reticulospinal axons, which primarily fire in brief bursts. Glial cell processes and postsynaptic dendrites displayed the highest density of glutamine labeling in both types of synapse. The level of glutamine was significantly higher in the glial cell processes surrounding the tonic dorsal column synapses, as compared to those surrounding the reticulospinal synapses. The axoplasmic matrix and presynaptic mitochondria, as well as postsynaptic dendrites, contained similar levels of glutamine labeling in both cases. The glutamate labeling in glial processes was also similar at the two types of synapse, while axoplasmic matrix and presynaptic mitochondria displayed four to six times higher levels in the tonic axons. In conjunction with our previous results, showing a different transport activity in glial processes of the two types of excitatory synapse, the results of the present study suggest that the glial pool of neurotransmitter precursor is linked to the rate of transmitter synthesis and release in adjacent synapses.