Elsevier

Neuroscience

Volume 134, Issue 4, 2005, Pages 1325-1341
Neuroscience

Neuroanatomy
Galanin and neurokinin-1 receptor immunoreactivity spinal neurons controlling the prostate and the bulbospongiosus muscle identified by transsynaptic labeling in the rat

https://doi.org/10.1016/j.neuroscience.2005.06.002Get rights and content

Abstract

Ejaculation requires the coordination of sympathetic, parasympathetic and somatic neural outputs. Timely occurrence of the emission and expulsion of sperm results from an interplay between spinal nuclei innervating the seminal tract and the sexual accessory glands including the prostate on the one hand, and on the other hand perineal striated muscles, particularly the bulbospongiosus muscle. A group of cells essential for ejaculation, located around the central canal and referred to as lumbar spinothalamic neurons have been recently identified. Lumbar spinothalamic neurons are immunoreactive for galanin and neurokinin-1 receptor. In order to investigate the anatomical relationships between lumbar spinothalamic neurons and both the prostate and the bulbospongiosus muscle, pseudorabies virus retrograde tracing technique was used combined with immunohistochemistry. Three to five days after pseudorabies virus injection in the bulbospongiosus muscle or the prostate in male rats, spinal cord sections were processed for double immunofluorescence against pseudorabies virus and galanin or neurokinin-1 receptor. Immunocytochemical experiments against pseudorabies virus and choline acetyltransferase were also performed to discriminate between motoneurons and preganglionic neurons, or interneurons. Spinal sections were examined with confocal laser scanning microscope. Three days after pseudorabies virus injection within the prostate and the bulbospongiosus muscle, sympathetic preganglionic neurons and motoneurons of the dorsomedial nucleus were retrogradely labeled, respectively. Five days after pseudorabies virus injection, transsynaptically labeled choline acetyltransferase-negative neurons were found mainly located in the medial gray surrounding the central canal from L1 to S1. At the L3–L4 level, most of transsynaptically labeled neurons were immunoreactive for galanin and to a lesser extent for neurokinin-1 receptor, strongly suggesting that they could be the lumbar spinothalamic cells. We have thus evidenced connections between these cells and motoneurons of the dorsomedial nucleus and both sympathetic and parasympathetic preganglionic neurons innervating the bulbospongiosus muscle and the prostate, respectively. These anatomical data reinforce the crucial role for lumbar spinothalamic cells in coordinating the spinal control of ejaculation.

Section snippets

Animals

Adult Sprague–Dawley male rats, body weight 250–330g (Harlan France, Gannat, France) were used for the experiments. Rats were kept in animal facilities under a 12-h light/dark cycle, light at 8:00 a.m., with food and water ad libitum. Twenty-two rats have received PRV injections into the BS muscle, and in 18 rats PRV injections were performed into the right ventral prostatic lobe. After PRV injections, rats were housed one per cage and observed daily. Rats were allowed to survive for 3 days (n

PRV spinal cord labeling following injection into the BS muscle

Three days after PRV injection, labeled neurons were only found in the ipsilateral dorsomedial nucleus (DM) located in the VH of the L5–L6 spinal segment (not shown). Labeled cells, presumably motoneurons innervating the right BS muscle, were large with long dendrites projecting ventrolaterally, medially and dorsally. Among five animals injected with PRV and killed after 3 days, only one animal displayed a single labeled neuron in the DGC at the L3 level.

After a survival period of 4 days,

Discussion

The BS muscle and the prostate are key pelvic–perineal anatomical structures involved in the ejaculation process respectively in the emission and the expulsion phases. We first describe in detail in the lumbar spinal cord the distribution of neurons which are retrogradely labeled by PRV after injection in these peripheric organs, and then demonstrate their relationship with spinal GAL and NK1-R neurons.

Several studies have previously described the neural pathways from the spinal cord to BS

Conclusion

We have identified a group of lumbar spinal neurons which expressed GAL or to a lesser extent NK1-R, located in lamina X of L3 and L4 levels which were in close connection with DM motoneurons innervating the BS muscle and both parasympathetic and sympathetic preganglionic neurons destined to the prostate. These data provide further anatomical evidence for a crucial role for LSt cells in coordinating the spinal control of ejaculation.

Acknowledgments

Pr. Lynn W. Enquist (Department of Molecular Biology, Princeton University, Princeton, NJ, USA) is warmly acknowledged for his contribution by providing the bartha strain of PRV and the antiserum against PRV.

References (32)

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