A galanin-positive population of lumbar spinal cord neurons modulates sexual behavior and arousal

Abstract

Graphical abstractSummaryDuring sex, male arousal increases up to the ejaculatory threshold, allowing genital sensory input to trigger ejaculation. While copulation and arousal increase are thought to be centrally regulated, ejaculation is a reflex controlled by a spinal circuit, whose activity is strongly inhibited by descending input from the brain, bearing no role on the regulation of sexual behavior up until the arousal threshold. However, this hypothesis remains untested. To tackle this problem, we combined genetic approaches with electrophysiological and behavioral analysis to functionally map the spinal circuit controlling the main muscle involved in sperm expulsion, the bulbospongiosus muscle (BSM). We found that BSM motor neurons (BSM-MNs) receive direct synaptic input from a group of galanin-expressing (Gal+) interneurons located in the upper lumbar spinal cord. Furthermore, the Gal+ population is progressively activated during sexual behavior and receives genital sensory input. Electrical and optogenetic activation of the Gal+ neurons evoked activity in BSM-MNs and BSM after spinalization. Interestingly, these effects were dependent on the behavioral state of the male and drastically decreased with repeated stimulation. Moreover, genetic ablation of the Gal+ neurons severely impacted the latency to ejaculate and the structure of the copulatory sequence. Taken together, our results imply an unexpected involvement of the spinal cord in the control of copulatory behavior, sexual arousal and in the post-ejaculatory refractory period, in addition to its well established role in ejaculation.