Compartmentation of glutamate and glutamine in the lateral cervical nucleus: Further evidence for glutamate as a spinocervical tract neurotransmitter

Abstract

Previous observations indicate that spinocervical tract terminals contain relatively high levels of glutamate. To examine whether these high glutamate levels are likely to represent a neurotransmitter pool or an elevated metabolic pool, the distributions of glutamate- and glutamine-like immunoreactivities were examined in adjacent immunogold-labeled sections of the lateral cervical nucleus. Spinocervical tract terminals were identified by anterograde transport of horseradish peroxidase and wheat germ agglutinin-horseradish peroxidase conjugate from the spinal cord. Spinocervical tract terminals were found to contain significantly higher levels of glutamate-like immunoreactivity than other examined tissue compartments (large neuronal cell bodies, terminals with pleomorphic vesicles, astrocytes, and average tissue level). In contrast, the highest levels of glutamine-like immunoreactivity were detected in astrocytes. The different analyzed tissue elements formed three groups with respect to glutamate:glutamine ratios: one high ratio group including spinocervical tract terminals, a second group with intermediate ratios consisting of neuronal cell bodies and terminals containing pleomorphic synaptic vesicles, and a third low ratio group including astrocytes. Our findings indicate the presence of a compartmentation of glutamate and glutamine in the lateral cervical nucleus, similar to that postulated in biochemical studies of the central nervous system. The results also show that spinocervical tract terminals have high glutamate: glutamine ratios, similar to those previously observed in putative glutamatergic terminals in the cerebellar cortex. Thus, spinocervical tract terminals display biochemical characteristics that would be expected of glutamatergic terminals and the present findings therefore provide further evidence for glutamate as a spinocervical tract neurotransmitter.

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“…Neurons in the lateral cervical nucleus relay sensory information from spinocervical tract neurons in the ipsilateral dorsal horn, to among other areas, the contralateral ventral posterior lateral nucleus of the thalamus (Giesler et al,1988; Zhang et al,2002). Previous studies in cats have demonstrated that terminals of the spinocervical tract contain high levels of glutamate associated with synaptic vesicles but low levels of glutamine (Broman et al,1990; Kechagias and Broman,1994,1995), making strong arguments for glutamate as a spinocervical tract neurotransmitter in cats. Our present demonstration that virtually all spinocervical tract terminations in rats are immunoreactive for VGLUT2 strongly supports glutamate as a spinocervical tract neurotransmitter also in rats and demonstrate that vesicular accumulation of glutamate in spinocervical tract terminals is sustained primarily if not exclusively by VGLUT2.…”