Neural pathways mediating control of reproductive behavior in male Japanese quail

Abstract

The sexually dimorphic medial preoptic nucleus (POM) in Japanese quail has for many years been the focus of intensive investigations into its role in reproductive behaviour. The present paper delineates a sequence of descending pathways that finally reach sacral levels of the spinal cord housing motor neurons innervating cloacal muscles involved in reproductive behaviour. We first retrogradely labeled the motor neurons innervating the large cloacal sphincter muscle (mSC) that forms part of the foam gland complex (Seiwert and Adkins-Regan, 1998, Brain Behav Evol 52:61–80) and then putative premotor nuclei in the brainstem, one of which was nucleus retroambigualis (RAm) in the caudal medulla. Anterograde tracing from RAm defined a bulbospinal pathway, terminations of which overlapped the distribution of mSC motor neurons and their extensive dorsally directed dendrites. Descending input to RAm arose from an extensive dorsomedial nucleus of the intercollicular complex (DM-ICo), electrical stimulation of which drove vocalizations. POM neurons were retrogradely labeled by injections of tracer into DM-ICo, but POM projections largely surrounded DM, rather than penetrated it. Thus, although a POM projection to ICo was shown, a POM projection to DM must be inferred. Nevertheless, the sequence of projections in the male quail from POM to cloacal motor neurons strongly resembles that in rats, cats and monkeys for the control of reproductive behaviour, as largely defined by Holstege and co-workers (e.g., Holstege et al., 1997, Neuroscience 80: 587–598).

The respiratory-vocal system of songbirds

“…It should be noted, however, that, like NRA, RAm is not just a respiratory premotor nucleus, but rather is functionally diverse. For instance, like NRA (VanderHorst and Holstege, 1997), it has premotor neurons that project upon motoneurons at lumbosacral spinal levels that innervate muscles involved in reproductive behavior (Wild and Balthazart, 2013). …”

Involvement of the avian song system in reproductive behaviour

“…To identify putative premotor neurons in the brainstem, two males and two females received air pressure injections of CTB in the ventral horn of one or two sacral spinal cord segments shown to house cloacal motoneurons. As in Japanese quail [11], the injections in canaries retrogradely labelled neurons in the caudal part of RAm (figure 2d), and in several other groups of neurons throughout the brainstem. Of these, only RAm receives a descending projection from the forebrain song system [16].…”

“…However, unlike RAm in non-songbirds or NRA in mammals, RAm neurons in canaries that project upon motoneurons involved in reproductive behaviour receive a putative direct projection from the output of the telencephalic song system, RA. Probably, as in all other birds [15], RAm in canaries also receives a projection from DM, which could mediate hypothalamic sexual drive, although further work is required to substantiate this [11]. In sum, we describe a neural pathway that putatively connects RA with cloacal motoneurons disynaptically, thereby providing the link between the song and reproductive systems necessary to mediate a continuum of appetitive and consummatory behaviours.…”

“…In fact, the representation of non-vocal-respiratory components of the CSD in the song system's motor pathway could suggest that vocal learning evolved within a motor circuit associated with reproductive behaviour. Specifically, the results show that RAm in canaries, like RAm in quail [11] and like the homologous nucleus retroambiguus (NRA) in mammals [17,18], is functionally diverse, housing not only respiratory and vocal premotor neurons [16,19], but also premotor neurons activating muscles involved in mating behaviour. However, unlike RAm in non-songbirds or NRA in mammals, RAm neurons in canaries that project upon motoneurons involved in reproductive behaviour receive a putative direct projection from the output of the telencephalic song system, RA.…”

“…Its external aperture (the vent) is enclosed by a sphincter muscle (mSC) [9], which in male Japanese quail has been shown electromyographically to be active during copulation and defaecation [10]. Furthermore, mSC motoneurons in quail receive a direct projection from RAm [11], but because quail are non-songbirds, they do not possess a forebrain song system. We ask here, therefore, whether the song system of songbirds is involved not only in appetitive aspects of reproductive behaviour (singing), but also in consummatory aspects of reproductive behaviour (copulation).…”