Expression of vesicular glutamate transporters in rat lumbar spinal cord, with a note on dorsal root ganglia

Abstract

Three vesicular glutamate transporters (VGLUTs) have been recently identified and their distribution has been mapped in various brain areas. In the present study, we used morphological approaches to investigate their expression in the rat lumbar spinal cord and dorsal root ganglia. Our results show a complementary distribution of VGLUT-expressing fibers in the spinal cord, with no overlapping in nerve endings. In the dorsal horn, VGLUT1 is most abundant in mechanosensory/proprioceptive deep afferent fibers. VGLUT2 and VGLUT3 are expressed only at moderate levels in primary sensory afferent fibers and are not used by central projections of nociceptive neurons. VGLUT1 and VGLUT2 mRNAs are mainly segregated in superficial laminae but colocalized in deeper laminae. Weak expression of VGLUT3 mRNA is only detected in deep laminae. The colocalization of VGLUT1 and VGLUT2 transcripts in most sensory neurons of the dorsal root ganglia is not in agreement with the clear segregation between the proteins in their spinal projections. Such a discrepancy suggests targeting mechanisms specific for each transporter and/or a distinct regulation of their translation. In the ventral horn, the expression of VGLUT1 and VGLUT2 mRNAs in motoneuron perikarya suggests the possible unexpected role of glutamate in the vertebrate neuromuscular junction. These results demonstrate the existence of different subpopulations of glutamate nerve terminals in the rat lumbar spinal cord and suggest that functionally distinct subsets of excitatory glutamatergic neuronal networks are involved in sensory processing and motor control.

Spinal neurons activated in response to pudendal or pelvic nerve stimulation in female rats

“…As previously reported, [2,34,53] VGlut2 labeling was found to be distributed throughout the spinal gray matter and was particularly abundant in the superficial dorsal horn (laminae I and II; figure 3A) and in lamina IV. Therefore, some overlap of labeling of fos-I nuclei and VGlut2 was found in all regions after pudendal and pelvic nerve stimulation, but this overlap was most prominent in the dorsal horn and DGC (figure 3H).…”

“…The present study examined the relationship of VGlut2, VGlut3 transporters and NKI receptors with fos-I nuclei as both glutamate and NKI receptors have been shown to regulate pelvic reflexes [64,69]. Glutamate is the major excitatory neurotransmitter and recent studies have documented the distribution of glutamate transporters in the lumbosacral cord [2,34,38,51,57,63]. Studies have suggested that VGlut1 and VGlut2 expression is restricted to glutaminergic neurons; however, VGlut3 expression is found not only in glutaminergic neurons but also neurons that contain acetylcholine and serotonin [28].…”

“…The distribution of VGlut3 was more specific compared to VGlut2 [34]. VGlut3 labeling was primarily found in the deeper layers of the dorsal horn (laminae III/IV) which was ventral to the majority of fos-I nuclei (figure 3B).…”

“…VGlut2 and VGlut1 immunoreactivity are widely distributed in the central nervous system and are found in some overlapping regions [34,53,63]. Neurons synthesizing VGlut2 have been identified in the ventral medulla, a region that projects to the lumbosacral spinal cord and is involved in regulating pelvic function [42,60].…”

Glutamatergic reinnervation through peripheral nerve graft dictates assembly of glutamatergic synapses at rat skeletal muscle

“…Three types of VGluTs, VGluT-1, -2, and -3, have been identified in the CNS (23). Although VGluT-1͞2 transcripts have been detected in rat spinal motoneurons (28,29), no VGluT-1͞2 proteins have been found to colocalize with VAChT (28,30) or ChAT (31). Recent studies demonstrating VGluT-2 immunostaining in motoneuron collateral axons projecting to layer VII of the spinal cord (28,32) confirmed the lack of VGluT-2 and glutamatergic transmission in the cholinergic projections to the NMJ.…”