The Foam Production System of the Male Japanese Quail: Characterization of Structure and Function

Abstract

The research described here characterizes a unique neuromuscular system involved in reproductive behavior – the foam production system of the male Japanese quail (Coturnix japonica). Male quail produce a large amount of foam that is transferred to the female during copulation, enhancing male fertilization success. The source is the foam gland complex, a large sexually dimorphic, androgen sensitive, external protuberance of the dorsal cloaca, consisting of glandular units interdigitated with striated muscle fibers of the sphincter cloacae muscle (mSC). Electromyographic (EMG) analysis of mSC activity in freely moving males interacting with females revealed different characteristics of the EMG signal during copulation, voiding of excreta, and other mSC movement. The amount of mSC activity and also the amount of foam produced were greatly increased by the presence of a female behind a screen. Denervation of mSC eliminated normal mSC movement and also abolished foam production, confirming that mSC activity is the mechanism for foam production. The spinal cord locations of the motoneurons innervating the major cloacal muscles, including mSC, were determined by injecting cholera-toxin conjugated horseradish peroxidase into each muscle. Labelled somata with multiple primary dendrites were located in Area IX of the lateral motor column of synsacral segments 7, 8, or 9 or 8, 9, and 10. The motoneurons serving mSC were intermingled with those projecting to the other cloacal muscles, but there were differences in the rostral-caudal placement of these neural populations. Thus mSC activity is an integral part of the male’s reproductive behavior, mSC activity can be socially stimulated, and mSC activity occurring in anticipation of copulation is likely to be functionally significant. Continued investigation of this highly accessible system has the potential to shed light on the mechanisms by which complex motor acts are produced and hormonally regulated.

Rapid effects of aromatase inhibition on male reproductive behaviors in Japanese quail

“…It has been shown previously (Seiwert, 1994;Seiwert and Adkins-Regan, 1998;Thompson, Goodson, Ruscio, and Adkins-Regan, 1998) that gonadally intact, sexually active males rapidly increase the rate of these movements when they are provided with visual access to a female. Interestingly, the RCSM rate is higher when a sexual mature male is presented with visual access to a female as compared to a male suggesting that these cloacal contractions are not simply triggered by visual cues of a general sort but are preferentially induced by visual access to a sexual partner (Seiwert, 1994;Seiwert and Adkins-Regan, 1998). Their expression depends on the endocrine status of the birds: the RCSM frequency decreases after castration but increases following a systemic treatment with exogenous testosterone (Balthazart, Absil, Gerard, Appeltants, and Ball, 1998).…”

“…Appetitive sexual behavior was quantified by two procedures: the measure of the learned social proximity response originally developed by Domjan and Hall (Domjan and Hall, 1986) and the measure of the rhythmic cloacal sphincter movements (RCSM). The rate of production of this response increases substantially in response to the visual presentation of a female Seiwert and Adkins-Regan, 1998). It thus can be considered as a response indicative of preparatory or appetitive responses in anticipation of copulation.…”

“…This foam is produced by the cloacal gland, a large sexually dimorphic, androgen-sensitive, external protuberance of the caudal lip of the cloaca (Sachs, 1967). It has been shown previously (Seiwert, 1994;Seiwert and Adkins-Regan, 1998;Thompson, Goodson, Ruscio, and Adkins-Regan, 1998) that gonadally intact, sexually active males rapidly increase the rate of these movements when they are provided with visual access to a female. Interestingly, the RCSM rate is higher when a sexual mature male is presented with visual access to a female as compared to a male suggesting that these cloacal contractions are not simply triggered by visual cues of a general sort but are preferentially induced by visual access to a sexual partner (Seiwert, 1994;Seiwert and Adkins-Regan, 1998).…”

“…These sphincter muscle movements are used by reproductively active males just before copulation to produce the stiff meringue-like foam that is transferred into the female's cloaca during copulation and that enhances the male fertilization success (Seiwert and Adkins-Regan, 1998). This foam is produced by the cloacal gland, a large sexually dimorphic, androgen-sensitive, external protuberance of the caudal lip of the cloaca (Sachs, 1967).…”

“…Previous work indicates that RCSM produced in reaction to the view of a female are an appetitive sexual response (i.e., they are indicative of the propensity of the animal to pursue a motivated consummatory behavior i.e. copulation), while those expressed in her absence are not; they are, for example, not affected by changes in plasma testosterone levels nor by lesions of the preoptic area Seiwert, 1994;Seiwert and Adkins-Regan, 1998). The low numbers of RCSM displayed when the female is not in view were thus considered as a control for the gland mobility in a non-sexual context.…”