To understand the neural mechanisms of reproductive behaviour in the male cricket, we identified motor neurones innervating the muscles in each genital organ by backfilling with cobalt/nickel and recording their extracellular spike activity from nerve bundles of the terminal abdominal ganglion during tethered copulation and spermatophore formation. During tethered copulation, at least two motor neurones innervating two ipsilateral muscles were activated during projection of the guiding rod of the phallic dorsal pouch. Only one motor neurone, innervating four ipsilateral muscles of the dorsal pouch, was responsible for spermatophore extrusion by deforming the dorsal pouch. For spermatophore transfer, three motor neurones, singly innervating three epiphallus muscles, played a major role in opening passages for haemolymph to enter the ventral lobes and median pouch by bending the epiphallus. Two ventral lobe and 3–5 median pouch motor neurones seemed to play a role in expanding or folding the two membranous structures by relaxing or contracting their muscle fibres. After spermatophore transfer, most of the genital motor neurones exhibited a rhythmic burst of action potentials causing movement of the phallic complex coupled with strong abdominal contractions. For spermatophore formation, the genital motor neurones began to accelerate their rhythmic bursts approximately 30 s prior to subgenital plate opening and then changed their activity to tonic bursting or silence. The results have allowed us to describe the timing of the onset and termination of genital muscle contraction more precisely than before, to examine the neural mechanisms of copulatory motor control and to speculate on the neural organization of the reproductive centre for spermatophore extrusion and protrusion.

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