Anatomical evidence for glutamatergic transmission in primary sensory neurons and onto postganglionic neurons controlling penile erection in rats: an ultrastructural study with neuronal tracing and immunocytochemistry

Abstract

In male rats, the dorsal penile nerve (DPN) conveys sensory information from the genitals to the lumbosacral spinal segments of the spinal cord. DPN is the afferent limb of a reflex loop that supports reflexive erections, and that includes a network of spinal interneurons and autonomic and somatic motoneurons to the penis and perineal striated muscles. Autonomic efferent pathways to the penis relay in the major pelvic ganglion (MPG). Glutamate (Glu) is a likely candidate as a neurotransmitter of reflexive erections. Both AMPA and NMDA glutamatergic receptor subunits are present in the lumbosacral spinal cord, and AMPA and NMDA receptor antagonists block reflexive erections. In the present study, we used tract-tracing experiments combined with immunohistochemical and immunocytochemical techniques to ascertain the presence of Glu at two different levels of the network controlling reflexive erections. DPN afferents were localized in the dorsal horn of the lumbosacral cord and displayed the characteristics of either C-fibers or Adelta fibers. DPN terminals (some of them glutamatergic) were mainly distributed in the medial edge of the dorsal horn in the L6 spinal segment. GluR1 subunits were present in some DPN afferents, suggesting that they could be autoreceptors. DPN fibers were also present in the MPG, as were Glu terminals and GluR4 subunits. The results reveal the presence of Glu in DPN fibers and terminals and suggest that both the spinal cord and the MPG use glutamatergic transmission to control reflexive erections.

Dynamic expression patterns of leucine‐rich repeat containing protein 10 in the heart

“…Markers of glutamatergic axons, in conjunction with peripherin (a Class III intermediate filament subunit protein that identifies small DRG neurons and their processes) (Parysek and Goldman, 1988; Goldstein et al, 1991; Lee et al, 2002), were shown in sensory nerves of the cervix. Retrograde tracing in the present study supports the idea that sensory glutamatergic neurons extend axons to innervate visceral pelvic organs (Keast and Stephensen, 2000; Aioun and Rampin, 2006) and that glutamate is localized, and presumably synthesized, in primary afferent neurons of DRG (Wanaka et al, 1987; Battaglia and Rustioni, 1988; Kai‐Kai and Howe, 1991; Miller et al, 1993; Keast and Stephenson, 2000; Ghosh et al, 2006). Nerve‐crush studies indicate glutamate is transported peripherally and centrally from DRG cell bodies (Keast and Stephensen, 2000).…”

Some lumbar sympathetic neurons develop a glutamatergic phenotype after peripheral axotomy with a note on VGLUT2-positive perineuronal baskets

“…The present results support the notion of expression of glutamate in nerve fibers innervating the MPG and also forming perineuronal baskets. Finally, in their study, Aïoun and Rampin also reported that the distribution and appearance of glutamatergic terminals in the MPG was similar to those of retrogradely traced penile sensory nerve terminals in this ganglion, targeting a specific subset of MPG neurons (Aïoun and Rampin 2006). Whether this is the case in our present work in mouse requires further investigation.…”

“…These are typically cholinergic, and often coexpress other transmitters, including neuropeptides (de Groat 1987; Wanigasekara et al, 2003; Keast 2006). Evidence of a glutamatergic trait in MPG perineuronal baskets has not been reported previously, with the exception of an electron microscopy study in rat showing glutamate in axons and terminals in the MPG, also containing large dense core vesicles (Aïoun and Rampin 2006). However, and possibly because of the nature of the experimental approach (electron microscopy), the authors did not assess the presence of perineuronal baskets containing glutamate in the MPG.…”

Activation of NMDA Receptors in Lumbar Spinothalamic Cells is Required for Ejaculation

“…The afferent inputs that trigger activation of NMDA receptors in LSt cells are currently unknown, although the most likely activation of LSt cells is via DPN nerve fibers. The densest distribution of DPN sensory afferent terminals is located in the superficial laminae of the L5 and L6 lumbar segments [17] and glutamate is expressed in DPN sensory afferents in male rats [12]. Stimulation of the pudendal nerve results in increased Fos‐immunoreactive nuclei in the L5‐S1 spinal segments, with the majority of these nuclei being located in the superficial dorsal horn and the central gray area in the DGC [18].…”