Research report
Noradrenergic control of auditory information processing in female canaries

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Abstract

An ethological procedure, based on the study of the sexual responsiveness of female canaries (Serinus canaria) to song playbacks was used to investigate the function of central noradrenergic inputs in the processing of auditory information. The effects of a noradrenergic denervation on sexual responses was analyzed in females exposed to playbacks of biological relevant auditory stimuli, i.e. sexually stimulating songs, presented alone or masked by auditory distractors. A decrease in behavioral responsiveness was observed as a function of the amount of masking distractors indicating that female canaries have the perceptual ability to discriminate and selectively attend to biologically relevant songs. After the systemic administration of DSP-4, a specific noradrenergic neurotoxin, females exhibited an overall decrease in sexual responsiveness to songs masked or not by distractors. No effect of DSP-4 were detected on the motor activity nor on reproductive behaviors. These results indicate that central noradrenergic inputs modulate the sexual behavior of female canaries by affecting the auditory processing of relevant information contained in sexually stimulating songs.

Introduction

Since Nottebohm et al. [56] identified in the canary brain a network of interconnected nuclei that controls the learning and expression in adulthood of complex vocalizations, this so-called song control system has been the object of intensive studies. Major progress has been achieved in identifying the neuroanatomical substrate controlling specific aspects of song production and learning (for reviews see Refs. [46], [53], [73]). During the last decade, the song system has emerged as a powerful model to study the neural correlates of complex cognitive abilities that involve learning, auditory stimuli processing and motor control (for review see Ref. [8]). Many questions remain however open and, in particular, major gaps are still present in our understanding of the neurochemical organization and control of the song system. Although some information has been gathered on the presence of neurotransmitters, neuropeptides and their receptors in the song control nuclei (for review see Refs. [5], [6], [22]), few pharmacological studies have been performed to investigate the functional significance of these neurochemical systems.

Chemical neuroanatomy has in particular demonstrated that the song control nuclei receive specialized catecholaminergic projections and contain high densities of noradrenergic and dopaminergic receptors (e.g. in zebra finches, Taeniopygia guttata: [10], [11], [16], [49], [62], [67]; in European starlings, Sturnus vulgaris: [5], [15], [19]). In the canary brain (Serinus canaria), the telencephalic song control nuclei are characterized by a dense and specific catecholaminergic innervation as revealed by immunocytochemistry for tyrosine hydroxylase [2]. Accordingly, tract tracing studies indicate that, in both male and female canaries, song control nuclei such as the high vocal center (HVc) or the nucleus robustus archistriatalis (RA) that play a major role in the perception and production of song receive dopaminergic inputs from the mesencephalic central gray (GCt; homologous to the mammalian A11 cell group) and from the area ventralis of Tsai (AVT) and, noradrenergic inputs from the complex of the locus coeruleus [1](Appeltants, Ball and Balthazart, unpublished data) whereas area X appears to receive catecholaminergic inputs originating mostly or exclusively in AVT in zebra finches [41].

Numerous studies have highlighted the importance of the catecholaminergic transmission in the control of complex cognitive abilities in humans [59], [60], [61], as well as in other vertebrates [4], [30]. Specifically, the noradrenergic system would play a role in stimulus selection and attention and animals with noradrenergic lesions would be unduly distractible as a result of a failure to screen out or habituate to irrelevant stimuli. In songbirds, a few studies only have investigated the effects of manipulations of the noradrenergic systems on song production or perception so that the functional significance of these noradrenergic inputs to the song control nuclei is poorly understood. In zebra finches, the pharmacological depletion of central norepinephrine levels obtained by injection of the noradrenergic neurotoxin DSP-4 decreases male courtship behavior including female-directed singing [12], [13]. This effect appears to result from attention deficits rather than from impairments of the motor aspects of song because in DSP-4 treated birds the latency to initiate singing was increased but once song began it was quite normal. Dave et al. [24] also demonstrated that norepinephrine regulates, in a gate-like fashion, the auditory responsiveness of RA neurons (that receive a prominent projection from HVc).

Male canaries produce an abundance of complex vocalizations whereas females only sing rarely [57] and the size of their song control nuclei is substantially smaller [54], [55]. The specific function of the song control system of female canaries is largely enigmatic but recent data suggest that parts of this system, together with other brain areas, are involved in auditory processing of song information (e.g. [18], [25], [26]). In songbirds, auditory processing of song information plays an important function in the context of mate choice [38], [64]. In canaries specifically, females in visual isolation exhibit copulation solicitation displays (CSDs) in response to song playbacks. Female canaries are able to discriminate between conspecific and heterospecific songs [37] and are especially responsive to a particular short sexually stimulating song phrase, called phrase A, essentially characterized by the presence of abrupt frequency falls and short silences [69], [70].

In natural conditions, males may produce songs in a rich acoustic environment, composed of songs of other species and of different types of noise. To discriminate and to respond selectively to a sexually stimulating song in such an environment, selective attention must be at work to enable the female canary to pay specific attention to the auditory features of interest and ignore the irrelevant ones [35]. Based on the hypothetical role of the noradrenergic system in selective attention, it can be assumed that noradrenergic inputs to the song control system and/or other brain regions may participate in the control of the auditory processing underlying the sexual responsiveness to song displays.

In the present study, the induction of sexual courtships was quantified in females exposed to sexually stimulating song segments that were mixed with different kinds of auditory distractors to ascertain the ability of females to detect the relevant stimuli when masked by irrelevant sounds. One group of females was then treated with the specific noradrenergic neurotoxin DSP-4 to produce a central noradrenergic depletion and investigate its functional consequences on sound processing.

Section snippets

General experimental design

The present study is based on an ethological procedure that measures the sexual responsiveness of female canaries to the playback of a biological relevant auditory object, i.e. the sexually stimulating conspecific song. This song was presented alone or associated with and partly masked by two kinds of auditory stimuli: non sexually stimulating song segments or white noise (WN). Based on previously described protocols [36], [71]), photostimulated females were allowed to build nests and to lay

Effects of DSP-4 on behavioral responses to the mixture of sexually stimulating and NS songs

During both breeding periods, domesticated canary songs including a sexually stimulating phrase A elicited sexual responses from female canaries. The mean number and average duration of the CSD displayed by female canaries in response to the playback of the sexually stimulating song mixed with an increasing number of NS song segments are presented in Fig. 3. The analysis of these data by three-way ANOVA (groups, breeding cycle and amount of superimposed songs as factors) identified significant

Discussion

The present data confirm that, during the breeding period, adult female canaries exposed to conspecific song segments including the sexually stimulating phrase A reliably respond by showing CSDs. When this stimulating song segment was associated with different kinds of distractors, a decreased responsiveness was observed that was a function of the amount of distractors. These data demonstrate that female canaries are able to identify and selectively attend to one biologically relevant auditory

Acknowledgements

This work was supported by grants from the NINDS (NS 35467) to Gregory F Ball and JB, and by grants from the Belgian FRFC (no. 2.4555.01), the French Community of Belgium (ARC 99/04–241), and the University of Liège (Crédits spéciaux) to JB. The collaboration between JB and CDN was supported by a grant from the CGRI-FNRS-CNRS. DA is research fellow with the National Fund for Scientific Research (Belgium).

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