Research reportThe selectivity of sexual responses to song displays: effects of partial chemical lesion of the HVC in female canaries
Introduction
In songbirds, males and females exhibit different patterns of behavior, especially in contexts related to courtship and reproduction. Adult males of the oscine suborder of passerine birds such as male canaries have a complex song repertoire learned by reference to auditory information, which conveys sexual information used by females to select a mate 9, 17, 35. In contrast, the songs of female canaries as well as of other female songbirds differ in temporal structure from male song and their exact function remains unknown [40]. Studies on female songbirds have focused on their sexual receptivity to song displays as a means of determining the particular salient attributes of male song. In canaries, a large repertoire and song diversity have been shown to be important in female mate choice [16]. Females are also able to discriminate between conspecific and heterospecific song [15]and gain information about their own breed identity from both phonology and song segmentation [37]. Particular song phrases in male songs have a high probability of stimulating courtship solicitation displays (CSD) in receptive female canaries while other phrases have a low sexual potential [39]. This special type of song phrase is a powerful sexual releaser in whatever acoustic context it is sung [39]. A sexually-stimulating phrase contains at least several essential features such as bipartite syllables, the rapid frequency modulation of elements (abrupt frequency fall) and short silences (15–25 ms). Whereas, phrases made of monopartite brief syllables are very common in male canary song [13], the sexually-stimulating phrases of bipartite syllables were found only in 50% of male songs [40]and were never recorded in any female song, even when the females were implanted with testosterone and sang male-like songs [40]. Because female canaries in visual isolation from the singing male respond to sexually-stimulating song phrases with courtship solicitation displays, it can be deduced that auditory properties alone are sufficient to induce this type of sexual response. The sexual responsiveness of female songbirds to auditory stimulation depends on the presence in the birds of high levels of estrogens and, thus, is limited to the period of nest-building and egg-laying 5, 18, 29, 35.
Therefore, the neural basis for the estrogen dependent discrimination of conspecific songs could be implemented either in the auditory system, or in the motor system that controls CSD movements, or at some auditory-motor interface. In an analogous situation (i.e. the estrogen dependent lordosis response of female rats to tactile stimulations), estrogens seems to change the motivation to respond with CSDs by acting on the sensory system and integrative hypothalamic and midbrain areas but not on the motor system that drives lordosis [33]. In songbirds, the ascending auditory system of birds has been well analysed, whereas, the motor components (wing control, tail and body posture) involved in CSD have not. Furthermore, in the brainstem of songbirds, estrogen receptors are mainly found in the nucleus solitarius but not in motonuclei [11]. For these reasons, we focused on brain areas which are estrogen sensitive and auditory.
The ascending auditory system of birds ends in the forebrain area Field L which is analogous to the primary auditory cortex of mammals [1]. There are several further auditory fields in the forebrain such as the caudomedial hyperstriatum adjacent to and partially receiving input from Field L that contain, like Field L, neurons that respond to complex auditory features of species-specific vocalization 19, 27, 41. The song-induced expression of an immediate early gene (ZENK) in the auditory pathway (including subfields of Field L), the caudiomedial hyperstriatum and the caudal neostriatum are high when birds hear a conspecific song and lower when birds hear the song of a different species [25]. These areas could be responsible for the discrimination among conspecific songs. However, none of these areas nor the areas of the ascending auditory pathway contain estrogen receptors and thus are sensitive to estrogens ([11], Gahr, unpublished).
Besides purely auditory areas, the forebrain vocal control nuclei of songbirds contains neurons that respond to complex sound stimuli 8, 20, 21. These nuclei are part of a neural circuit which mediates vocal learning and production 32, 43and are present in both males and females despite large sexual differences in the vocal pattern generation in many songbird species. One of these areas, the caudal nucleus of the ventral hyperstriatum or high vocal center (HVC) contains high levels of estrogen receptors [11]and thus makes the HVC one of the foremost candidates for the discrimination among conspecific songs. Furthermore, the HVC was already shown to be important in the species-specific perception of song in female canaries [3]. However, since Brenowitz [3]did not distinguish between highly sexually attractive and weakly sexually attractive canary songs, his study provides no information about the neural basis of sexual responsiveness to features of canary song.
Because of these considerations, the aim of the present study was to determine if the influence of song phrase architecture on sexual responsiveness depends on the integrity of the HVC. For this purpose we created two kinds of canary songs: a highly sexually-stimulating song composed of conspecific phrases including stimulating phrase types which were previously found to elicit a great number of sexual responses and a weakly sexually-stimulating song without any of these very stimulating phrases in order to test the sexual potential of both songs before and after selective lesions of HVC. We provoked chemical lesions of the HVC by injecting ibotenic acid. This procedure created small lesions which were mostly restricted to the HVC and did not damage the fibers of passage. Since axons projecting from lateral magnocellular nucleus of the anterior neostriatum (MAN) to robust nucleus of the archistriatum (RA) travel lateral and ventral to HVC (Gahr, unpublished observation), electrolytic lesions as carried out by Brenowitz [3]could act by disrupting connexions between MAN and RA. Furthermore, because auditory areas are in close proximity to HVC-localized lesions, it is important to avoid damage to these adjacent auditive areas while lesioning the HVC. For these reasons, we produced relatively small chemical lesions in the HVC. Since this lesion technique is different from the previous study on the role of the HVC in the discrimination between conspecific and heterospecific song [3], we also tested courtship responses of female canaries to heterospecific song before and after HVC lesions.
Section snippets
Methods
We tested the sexual responsiveness of female canaries to the playback of the highly sexually-stimulating canary song, the weakly sexually-stimulating canary song and a heterospecific (greenfinch) song before and after selective lesions of the HVC.
Behavioral results
During both breeding periods, all 20 females exhibited CSD during song test sessions. CSD scores in relation to the three different types of songs were summed up. Fig. 2 shows the mean CSD scores recorded for each song before and after the HVC lesions (Fig. 2A) or sham lesions (Fig. 2B).
Before surgical procedures, the conspecific stimulating song (S+) elicited a high level of sexual displays in all females. The conspecific poorly-stimulating song (s−) elicited about three times less CSD and
Discussion
On the basis of previous experiments we created two kinds of canary songs: song (S+) partly with stimulating phrases that elicited CSD and songs (s−) without stimulating phrases. With regard to the effect of songs on sexual displays, the results of the present experiment are unequivocal: song (S+) elicited a high level of sexual displays in the females, song (s−) had an intermediate potential and the song of another species (gr) stimulated only a few displays. The structural features of the
Acknowledgements
This work was supported by the Procop grant 96032 to M. Kreutzer and M. Gahr.
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