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Effects of learning on song preferences and Zenk expression in female songbirds
Available online at www.sciencedirect.com
Behavioural Processes 77 (2008) 278–284
Effects of learning on song preferences and Zenk expression in female songbirds Alexandra M. Hernandez a , Leslie S. Phillmore b , Scott A. MacDougall-Shackleton a,∗ a
Department of Psychology, University of Western Ontario, London, ON N6A 5C2, Canada b Department of Psychology, Dalhousie University, Halifax, NS B3H 4J1, Canada
Received 10 July 2007; received in revised form 6 November 2007; accepted 6 November 2007
Abstract Male songbirds learn to produce their songs, and females attend to these songs during mate choice. The evidence that female song preferences are learned early in life, however, is mixed. Here we review studies that have found effects of early song learning on adult song preferences, and those that have not. In at least some species, early experience with song can modify adult song preferences. Whether this learning needs to occur during an early sensitive phase, akin to male imitative vocal learning, or not remains an open question. Studies of the neural bases for female song preferences highlight activity (as measured by immediate-early gene induction) in regions of the auditory forebrain as often, but not always, being associated with song preferences. Immediate-early gene induction in these regions, however, is not specific to songs experienced early in life. On the whole, inherited factors, early experience, and adult experience all appear to play a role in shaping female songbirds preferences for male songs. © 2007 Elsevier B.V. All rights reserved. Keywords: Song learning; Birdsong; Zenk; Song preferences; Mate choice
The study of animal behavior has benefited tremendously from integration of a variety of approaches including psychology and behavioral ecology. Indeed, combining approaches has been critical for maintaining the study of birdsong as a leading example of integrative biology (Konishi, 1985). Integration of psychology and ecology has been an important movement in animal cognition in general and in birds in particular (e.g. Rowe and Skelhorn, 2004). Ron Weisman and colleagues have made many important contributions to this integration. These include the use of operant conditioning techniques to study the perception of natural signals: bird songs and calls (e.g. Sturdy et al., 2000), proposing a role for perceptual discrimination learning and the resultant ‘peak shift’ in the evolution of mating signals (Weary et al., 1993), and highlighting the importance of early learning for the development of adult perception of signals (Njegovan and Weisman, 1997; Sturdy et al., 2001; Phillmore et al., 2003a,b), and adult mate preferences (Weisman et al., 1994). In this review we highlight the importance of integrating approaches by reviewing the effects of early learning on adult female song preferences in songbirds. The neurobiology and
∗
Corresponding author. E-mail address: [email protected] (S.A. MacDougall-Shackleton).
0376-6357/$ – see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.beproc.2007.11.001
behavior of song production in males has been studied extensively, but song production by females (Riebel, 2003; Riebel et al., 2005), and the effects of learning on female song preferences have been studied far less. Below we review the evidence for early learning affecting female preferences for particular males’ songs and for songs from a particular geographic region. We then examine the potential auditory brain regions involved in female song preferences and how activity in these regions may be modulated by early experience. Further progress in this field will require continuation of an integrated approach to gain understanding of the effects of early learning on song preferences. 1. Female song preferences Song is a courtship signal involved in mate selection by female songbirds, and preferences for particular song features have been widely identified. In some species, females have a preference for greater song output, preferring males that sing for a longer duration (e.g., European starling, Sturnus vulgaris, Eens et al., 1991) or sing longer songs or at higher song rates (white-throated sparrow, Zonotrichia albicollis, Wasserman and Cigliano, 1991). Female songbirds have also been shown to have preferences for increased song complexity, preferring males that have larger song repertoires (sedge warbler, Acrocephalus
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schoenobaenus, Catchpole et al., 1984; song sparrow, Melospiza melodia, Searcy and Marler, 1981). In addition to preferences for specific song features, in species that exhibit geographic variation in song females often prefer songs from the geographic region in which they live over more distantly recorded song variants (brown-headed cowbird, Molothrus ater, O’Loghlen and Rothstein, 1995; song sparrow, Searcy et al., 2002; white-crowned sparrow Zonotrichia leucophrys, Baker et al., 1981; Casey and Baker, 1992; MacDougall-Shackleton et al., 2001). A female preference for the song of the local geographic area in these species suggests that female songbirds may learn song (Baker et al., 1981; Casey and Baker, 1992; MacDougall-Shackleton et al., 2001). 2. Female song learning? Male songbirds, the primary song producers, learn to sing their songs in a process akin to language production learning in humans (Thorpe, 1958; Marler, 1970; see Kuhl, 2003 for review). Birds pass through a sensory phase of song acquisition in early life where the songs they are exposed to become encoded as auditory memories. This is followed by a sensory-motor phase of song acquisition where young males begin to produce songs and eventually attempt to match their vocal output to the sensory representations of song, formed in the sensory phase, via auditory feedback. These phases of song acquisition fall within a sensitive phase early in development (Marler, 1970) whereby if either exposure to song or auditory feedback (Konishi, 1965) is disrupted the bird will fail to develop normal song. Thus normal song development in males is dependent on experience with song and the ability to match vocal output to the sensory memories of song via auditory feedback. Whether female song preferences for local song develop in a manner similar to song acquisition in males, where sensory representations of tutors’ songs are formed early in life, is less well understood. Laboratory studies controlling song exposure show mixed findings in terms of the importance of song exposure early in life on female song preference development. Some of the earliest experiments supporting the idea that females’ early experience affects song preferences in adulthood were performed by Miller (1979a,b). He showed that female zebra finches (Taeniopygia guttata) prefer the songs of their fathers or their mates compared to novel unfamiliar songs. Following this, in a double controlled study controlling for genetic influences, adult female zebra finches of two subspecies were shown to prefer the song of their tutor, over a non-tutor song, in adulthood (Clayton, 1990). Thus, at least in zebra finches, females exhibit preferences for songs to which they have been exposed over songs that are unfamiliar. However, whether there is a critical phase for this song learning is unknown. Moreover, in zebra finches each male in a colony sings a single unique song, so learning to recognize a particular male by his song would intuitively make adaptive sense. Furthermore, in species where males sing more than one song type the discrimination task would seem to be many times more difficult. How widespread, therefore, is female song recognition learning in species in which each male does not have a unique song?
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Canary males sing a variety of songs, and female domesticated canaries (Serinus canaria) prefer the songs to which they are exposed early in life (Nagle and Kreutzer, 1997a). However, these female canaries also demonstrate an experienceindependent preference for a specific song phrase (Vallet et al., 1998). Isolate, like aviary reared females, prefer broadband syllables produced at supernormal rates suggesting perceptual predispositions can drive preferences (Draganoiu et al., 2002), though song experience may modulate degree of responsiveness. In several other species of songbird, females do not show preferences for the songs heard early in life (swamp sparrow, M. georgiana, Balaban, 1988; chaffinch, Fringilla coelebs, Riebel and Slater, 1998; house finch, Carpodacus mexicanus, Hernandez and MacDougall-Shackleton, 2004; northern cardinal, Cardinalis cardinalis, Yamaguchi, 1999). Thus the effects of early learning on preferences for specific songs are mixed; the source of these mixed results is unclear. The question of female learning and song preferences has also been addressed in the study of preferences for local songs or song dialects. 3. Evidence of role of early experience on geographic song preference development Many species exhibit geographic variation in song. If this variation is discontinuous it is referred to as song dialects, but more continuous variation is common in many other species as well. Adult females commonly display preferences for local dialect songs, or songs from the local area (O’Loghlen and Rothstein, 1995; Searcy et al., 2002; Baker et al., 1981; Casey and Baker, 1992; MacDougall-Shackleton et al., 2001). Early auditory experience with song may play a role in the development of these local song preferences. Field reared whitecrowned sparrows captured as juveniles prefer songs from their location of capture in adulthood over songs from more distant regions (Baker et al., 1981; Casey and Baker, 1992; MacDougallShackleton et al., 2001). A female preference for the song of the local geographic area suggests that female songbirds of these species may, like males, learn song. However, these studies used only young birds tutored with the song of their location of capture and as such failed to control for possible genetic influences underlying local song preferences. House finches hand-reared in the laboratory and exposed to either local, foreign, or no song, preferred local song, independent of the songs with which they were tutored (Hernandez and MacDougall-Shackleton, 2004). Thus, there may be inherited components of song preferences. Demonstrating that geographic song preferences are learned independent of potential inherited preferences requires that a local bird exposed to a foreign song prefers the foreign song. Until recently, only Clayton’s (1990) study in zebra finches fully counterbalanced potential genetic influences. Hernandez (2007; dissertation) undertook a similarly designed study in song sparrows, a species where males, unlike male zebra finches, sing many song types. Females prefer larger song repertoires (Searcy and Marler, 1981) but also prefer songs from their local area (Searcy et al., 2002). Hernandez (2007; dissertation) hand reared birds captured from two locations in Ontario 450 km apart and tutored them with songs from the two sites in a fully
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Fig. 1. Song preferences of hand-reared female song sparrows. Birds were captured as nestlings from either eastern or western Ontario, hand-reared, and tutored with either songs from their natal location or from the other location. Song preference was measured in adulthood as time spent near playback speakers playing songs from the two locations. Females spent significantly more time near their tutor song, regardless of place of origin. Data from Hernandez (2007; dissertation).
counterbalanced design. In adulthood, these females showed a preference for songs of their tutor location, regardless of their genetic origin (Fig. 1). This clearly demonstrates a critical role for early experience in the development of geographic song preferences. Whether the influence of early experience has an early sensitive phase, as in male imitative vocal learning, remains an open question. In summary, the results of experiments on inherited and experiential influences on female song preferences are mixed, but in at least some species female song preferences appear to be shaped by prior experience with songs. Future work is required to determine how widespread this phenomenon is, the time course of this learning, and whether the time course varies across species as it does for song learning in males (so-called closeended versus open-ended song learners). The role of perceptual predispositions, early experience and adult experience may differ in their effect on song preferences among species. Future work is needed to better understand under what ecological circumstances different degrees of flexibility in the development of song preferences may be favored. 4. Neural correlates of song preferences The neural circuit underlying song learning and song production in male songbirds is well studied (see Ziegler and Marler, 2004; Nottebohm, 2005). This circuit consists of two descending pathways from the HVC. The anterior forebrain path consists of HVC projecting to area X, which projects to the medial portion of the dorsolateral nucleus of the thalamus (DLM) and the lateral portion of the magnocellular nucleus of the anterior nidopallium (LMAN), and on to the robust nucleus of the arcopallium (RA). Lesions to nuclei within this anterior forebrain pathway early in life disrupt song much more than do similar lesions to adults (Bottjer et al., 1984). The posterior descending pathway includes HVC, robust nucleus of the archistriatum (RA), and the tracheosyringeal part of the hypoglossal motor nucleus (nXI-
Its) which then innervates the muscles of the syrinx allowing song production. Although this song control system is critically important for imitative vocal learning and song production, its role in song perception and/or female song preferences is less clear. Studies of canaries, a species in which females sometimes sing, have shown that lesions to brain areas within the songcontrol system disrupt song perception and/or song preferences (Brenowitz, 1991; Burt et al., 2000; Del Negro et al., 1998). In contrast, lesions to HVC in female zebra finches (which never sing) failed to disrupt normal song preferences (MacDougallShackleton et al., 1998). This is perhaps not surprising given that HVC in female zebra finches is a small fraction the size of that in males (Nottebohm and Arnold, 1976) and exhibits cytoarchitecture and connectivity that differs from males (Fortune and Margoliash, 1995). In contrast, lesions to an auditory region CMM (caudal medial mesopallium) did disrupt song preferences in female zebra finches (MacDougall-Shackleton et al., 1998). While it is possible that differences seen in the involvement of the song-control system in song perception in females are due to damage to afferent projections from auditory regions, it can also be explained by species differences in song production by females. Evidence supporting the idea that auditory regions outside the traditional song circuit are specialized in perceptual processing of song includes the use of immediate-early gene (IEG) expression as a marker for neuronal activation, and electrophysiological studies. These studies point to the role of CMM and an adjacent structure, caudal medial nidopallium (NCM), in perceptual processing of song. The IEG Zenk (an acronym for Zif-268, Egr-1, NGIF-A, Krox-24), a transcription factor whose protein product is capable of binding to promoter regions on target genes upstream, has been widely used as an indicator of neural activation following song presentation. Zenk induction is thought to be an important step in a process that results in structural changes at the synapse, potentially changing the firing properties of the cell (see Tischmeyer and Grimm, 1999, for review), and as such is used to understand the neural correlates of learning and memory. Studies have found that NCM and CMM show highest levels of Zenk expression following the presentation of conspecific song over heterospecific song, and even less activation following tone bursts, followed by silence (Mello et al., 1992). Zenk activation within auditory areas also attenuates with repeated presentation of a particular song, with levels being raised once again following the presentation of a novel song (Mello et al., 1995). As well, different types of vocalizations can result in different levels of Zenk expression (Phillmore et al., 2003a,b). Thus studies looking at IEG expression demonstrate these structures play a role in processing biologically relevant auditory stimuli. Furthermore, electrophysiological studies that use microelectrodes to record activity of cells within these auditory areas have also shown habituation of activation after repeated presentation of the same song; this attenuated song specific response lasts for up to 2 days (Chew et al., 1995). Thus, auditory regions are involved in processing and discrimination of auditory stimuli, and may be critical to auditory perceptual learning.
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5. Auditory regions and female preferences Auditory regions in the avian forebrain involved in song perception have also been implicated in the expression of female song preferences. In female birds, greater activation in auditory regions has been demonstrated following the playback of several preferred song attributes. In a non-songbird, budgerigars (Melopsittacus undulatus), that prefers larger repertoires and more complex songs over less complex songs, these preferred songs result in greater IEG activation in a brain region similar to NCM (Eda-Fujiwara et al., 2003). Female European starlings, which prefer longer songs, also have higher activation in auditory regions following the playback of longer songs versus shorter songs (Gentner et al., 2001), even when overall amount of song to which females were exposed was controlled. Female whitecrowned sparrows show greater IEG activation in CMM and NCMd following local versus foreign song playback, and the strength of the IEG response was correlated to the number of solicitation displays performed (Maney et al., 2003). Thus, the auditory regions in the avian forebrain specialized in processing biologically relevant auditory stimuli, have been implicated in female preferences. How experience with song early in life and/or in adulthood modulates neural responses to song requires further investigation. 6. Evidence of the role of auditory regions in auditory learning Studies finding experience-dependent changes in neuronal activation in response to specific stimuli further support the idea that auditory regions are involved in perceptual learning. As discussed above, both electrophysiological (Chew et al., 1995) and IEG (Mello et al., 1995) activation in NCM habituate to the repeated presentation of a song, with dishabituation, or higher activation, occurring if a novel song is played. More recently, Sockman et al. (2002) found that in starlings recent previous exposure to long songs (which is preferred by the species studied, Gentner and Hulse, 2000) 1 day prior to playbacks, lead to even greater activation following exposure to long songs over short songs, than if no recent previous exposure to long songs occurred. In contrast, recent song exposure failed to lead to differential IEG expression in a study of adult female zebra finches. Miller (1979b) showed that female zebra finches behaviorally prefer their mate’s song over an unfamiliar song. However, playback of a male zebra finch’s song to his mate did not induce greater IEG activation than did playback of the same song to females that were not his mate (Phillmore, Kadis, Avey and MacDougall-Shackleton, unpublished; Fig. 2). Thus, experience with songs does not always lead to differential IEG expression. Determining when and why certain experiences with song modify IEG expression requires further study. Developmental studies looking at the neural correlates of song learning in maleshave implicated the auditory areas in song processing and memory. Jin and Clayton (1997) demonstrated Zenk within NCM becomes song inducible at an age when males begin to acquire song models. Though it seems
Fig. 2. Immediate-early gene induction by male song in female zebra finches. Females were either mated with the male in the playback or were unfamiliar with that male. Expression was measured in the dorsal caudomedial nidopallium (NCMd), ventral caudomedial nidopalium (NCMv), and caudomedial mesopallium (CMM). Data from Phillmore, Kadis, Avey and MacDougall-Shackleton (unpublished).
auditory experience, not actual song exposure, mediates normal Zenk responsiveness at a young age in that clutch reared isolate birds, but not solo isolates, show normal patterns of song induced Zenk. Bolhuis et al. (2000) found that IEG activation in NCM following playback of tutor song was correlated with strength of song learning (i.e. number of syllables copied from the tutor) in male zebra finches. These authors suggest that IEG expression in NCM is involved in the long-term representation of tutor songs. However, alternative explanations need to be ruled out including the possibility that if birds copy songs with high salience to them, this could in turn lead to greater activation when heard in adulthood due to its high salience. To better understand the role of NCM in auditory learning and memory, females serve as a good natural control since they do not produce song. In fact the strength of female song preferences and therefore presumably the strength of tutor song memory formation could be tested to see if it also correlates with the strength of IEG activation in NCM following tutor song playback. Developmental studies also examining IEG in juvenile females have been used to better understand the neural correlates of song learning and memory (Bailey and Wade, 2005). Recently, Tomaszycki et al. (2006) demonstrated that normal song reared males and females have higher levels of expression than untutored birds at 45 day, suggesting that exposure to song has general effects on Zenk responsiveness. Several studies have directly assessed whether early experience with song affects IEG activation in response to song in adult females. Hernandez and MacDougall-Shackleton (2004) showed that female house finches behaviorally preferred the local song regardless of which songs they were tutored with. In this study there was no difference in Zenk expression following song playback to either tutor or non-tutor song. This result is consistent with the level of song-induced Zenk activation reflecting the behavioral salience of the signal rather than auditory
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memories. Interestingly, females reared in isolation from song showed greater Zenk activation than the song tutored females. This finding, which may be analogous to findings of higher levels of Zenk when the sensitive period of song acquisition is open in zebra finch males (Jin and Clayton, 1997), suggests that isolate females may be in a more neuronally juvenile state, and that early song exposure may have general effects on Zenk neural responsivity. More recently Hernandez (2007; dissertation) found similar results in song sparrows. In this study, female song sparrows preferred their tutor songs regardless of their place of origin. However, Zenk activation did not differ in response to tutor versus non-tutor song. Again, Zenk activation was higher for isolate-reared females. Thus Zenk induction in the auditory forebrain is no greater following playback of songs learned early in life over novel songs. This finding is at odds with those in female zebra finch. Terpstra et al. (2006) found higher Zenk activation after the presentation of tutor song versus unfamiliar song in CMM in this species. While it is not clear what variables lead to these species differences in neural tuning to tutor song in auditory areas, it may be that in species where males only sing one song type (as in zebra finches) the cognitive demand of learning and remembering individual males’ songs is reduced. Interestingly, in female song sparrows, where behavioral evidence of females preferring tutor song clearly demonstrated females are able to learn many tutors songs (Hernandez, 2007; dissertation), we found no evidence that early experience tunes the neural responsiveness to tutor song in adulthood. Thus while it has been suggested that auditory regions are the site of tutor song memory storage (Gobes and Bolhuis, 2007), this is not the case for all species. Furthermore, although bilateral NCM lesions reduce the preferential response to tutor over novel song, birds still discriminate tutor from novel song following lesions (Gobes and Bolhuis, 2007). Given that ancestrally female songbirds were likely song producers (see Riebel et al., 2005), it may be that in species where females do not sing, as in zebra finches, the neuroanatomical distribution of auditory memories is different from species where females can sing, even if impoverished, songs. Furthermore, males and females may differ in their site of storage of auditory memories. Lauay et al. (2005) showed isolate reared male and female zebra finches differ in the degree to which deficits are seen in auditory regions versus song control nuclei. A more male-typical neuroanatomical distribution of tutor song may be present in species where females can sing and song nuclei are conserved. Thus, although a number of studies have shown a relation between the levels of Zenk induction in the auditory forebrain and song preferences (Eda-Fujiwara et al., 2003; Gentner et al., 2001; Leitner et al., 2005; Maney et al., 2003; Sockman et al., 2002), there is little direct evidence showing a connection between Zenk induction and early experience with songs. IEG induction in female songbirds’ auditory forebrain, then, appears to reflect the behavioral salience of the song, which can be modulated by recent experience (Sockman et al., 2002), social context (Vignal et al., 2005), sex steroids (Maney et al., 2006), among other factors, but does not seem to be specifically a marker of songs learned early in life.
6.1. Female song learning and song preferences While females of many temperate zone species do not sing, or sing less complex songs, song is still important in mate selection, and as such females may form long lasting representations of song. Several studies have shown that females respond preferentially to their mate’s song (song sparrows, O’Loghlen and Beecher, 1999; domesticated canaries, Serinus canaria, Beguin et al., 1998). Thus female songbirds are able to form lasting song memories regardless of song production. It has been suggested that sensory learning involved in recognition, and sensory learning involved in motor learning, may be dissociable (Riebel et al., 2002) and may rely on separate neural processes. Furthermore, it is not clear whether early sensory learning in females is distinct from recognition learning in adulthood, or whether females, like males of many species, possess a sensitive phase of song learning, beyond which the ability to learn new songs is reduced. Male songbirds, for example, have been shown to be able to recognize territorial neighbors and respond more aggressively to the song playback of a neighbor from an inappropriate boundary (Godard and Wiley, 1995), or to the song playback of a stranger versus a neighbor (Falls and Brooks, 1975). Yet in most species a male can only incorporate the songs they hear into their song repertoire when exposed to these songs within a limited window of time early in life. Therefore, sensory learning involved in song production, which occurs early in life, and sensory learning involved in song recognition learning in adulthood may be distinct in males. It is possible that female song recognition learning in adulthood could be distinct from sensory learning occurring early in life (Riebel, 2003). Whether females, like males, must hear song during an early sensitive phase to develop normal song preferences in adulthood requires further investigation. In female zebra finches, tutor songs that females were exposed to as juveniles were preferred to unfamiliar, but not tutor songs heard after sexual maturity, suggesting an enduring preference for songs heard earlier in life (Riebel, 2000). There is also evidence that the sensitive period may be shorter in female white-crowned sparrows, a species where females can sing (Nelson et al., 1997). However, experience with song in adulthood can also modify adult female white-crowned sparrow preferences (MacDougall-Shackleton et al., 2001), as is true in female domesticated canaries (Nagle and Kreutzer, 1997b). Recently, Lauay et al. (2004) demonstrated that early song exposure is critical for preferences for normal adult song over abnormal isolate song in female zebra finches. Isolate females also show deficits in dendritic spine density within auditory region NCM to a greater degree than males, who show larger deficits in song control nuclei HVC (Lauay et al., 2005). Furthermore it appears that at 45 days old differences are seen in Zenk response to normal versus isolate reared song in normal versus isolate reared birds (Tomaszycki et al., 2006). The long-term effect of absence of song exposure on Zenk responses in auditory regions in these birds is of interest. Whether isolate females have enduring deficits in auditory perception, song preferences, neuronal morphology and ZENK responses is of particular interest in understanding how early auditory learning differs from recognition learning in adulthood.
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While song preferences may be influenced by early song exposure, determining whether they are also modified and shaped into adulthood will help characterize auditory learning in songbirds. Thus it is important to delineate the time frame when song exposure can influence song preferences in females. It is not clear whether there is a sensitive period in auditory learning; it may be that the sensitive period seen in males is associated only with motor production aspects of song learning. For this reason, a better characterization of auditory learning in female songbirds is needed. Understanding the mechanisms and timing of female song preference development will also further help understand how these variables have shaped male song evolution and structure. 7. Conclusions Though historically ignored, a growing number of studies have begun to address song learning in female songbirds, including studies of how experience influences song preferences, and the neural bases of such learning. It is becoming clear that song preferences involve both learned and unlearned components. That is, exposure to song is required for the expression of some song preferences, but not others, and this varies from species to species. It is also clear that the auditory regions such as CMM and NCM play a role in song perception in female songbirds, and there is good evidence that exposure to song early in life (compared to isolate rearing) has some general effects on IEG responses to song, as isolates have repeatedly been shown to have enhanced responses. It is likely however, that IEG responses in CMM and NCM reflect the saliency of a stimulus, or overall attention rather than reflecting memory per se. Further studies with females are required to better understand the similarities and differences in song learning in male and female songbirds. Acknowledgments Our research program has been supported by NSERC, the Canada Foundation for Innovation, the Ontario Innovation Trust, and a Premier’s Research Excellence Award from the Province of Ontario. References Bailey, D.J., Wade, J., 2005. FOS and ZENK responses in 45-day-old zebra finches vary with auditory stimulus and brain region, but not sex. Behav. Brain Res. 162 (1), 108–115. Baker, M.C., Spitlernabors, K.J., Bradley, D.C., 1981. Early experience determines song dialect responsiveness of female sparrows. Science 214 (4522), 819–821. Balaban, E., 1988. Cultural and genetic-variation in swamp sparrows (Melospiza-Georgiana). 2. Behavioral salience of geographic song variants. Behaviour 105, 292–322. Beguin, N., LeBoucher, G., Kreutzer, M., 1998. Sexual preferences for mate song in female canaries (Serinus canaria). Behaviour 135, 1185–1196. Bolhuis, J.J., Zijlstra, G.G.O., den Boer-Visser, A.M., Van der Zee, E.A., 2000. Localized neuronal activation in the zebra finch brain is related to the strength of song learning. Proc. Natl. Acad. Sci. U.S.A. 97 (5), 2282–2285. Bottjer, S.W., Miesner, E.A., Arnold, A.P., 1984. Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224 (4651), 901–903.
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Brenowitz, E.A., 1991. Altered perception of species-specific song by female birds after lesions of a forebrain nucleus. Science 251 (4991), 303–305. Burt, J.M., Lent, K.L., Beecher, M.D., Brenowitz, E.A., 2000. Lesions of the anterior forebrain song control pathway in female canaries affect song perception in an operant task. J. Neurobiol. 42 (1), 1–13. Casey, R.M., Baker, M.C., 1992. Early social tutoring influences female sexualresponse in white-crowned sparrows. Anim. Behav. 44 (5), 983–986. Catchpole, C.K., Dittami, J., Leisler, B., 1984. Differential responses to male song repertoires in female songbirds implanted with estradiol. Nature 312 (5994), 563–564. Chew, S.J., Mello, C., Nottebohm, F., Jarvis, E., Vicario, D.S., 1995. Decrements in auditory responses to a repeated conspecific song are long-lasting and require 2 periods of protein-synthesis in the songbird forebrain. Proc. Natl. Acad. Sci. U.S.A. 92 (8), 3406–3410. Clayton, N.S., 1990. Subspecies recognition and song learning in zebra finches. Anim. Behav. 40, 1009–1017. Del Negro, C., Gahr, M., Leboucher, G., Kreutzer, M., 1998. The selectivity of sexual responses to song displays: effects of partial chemical lesion of the HVC in female canaries. Behav. Brain Res. 96 (1–2), 151–159. Draganoiu, T.I., Nagle, L., Kreutzer, M., 2002. Directional female preference for an exaggerated male trait in canary (Serinus canaria) song. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 269 (1509), 2525–2531. Eda-Fujiwara, H., Satoh, R., Bolhuis, J.J., Kimura, T., 2003. Neuronal activation in female budgerigars is localized and related to male song complexity. Eur. J. Neurosci. 17 (1), 149–154. Eens, M., Pinxten, R., Verheyen, R.F., 1991. Male song as a cue for mate choice in the European Starling. Behaviour 116, 210–238. Falls, J.B., Brooks, R.J., 1975. Individual recognition by song in white-throated sparrows, II. Effects of location. Canad. J. Zool. 53, 412–420. Fortune, E.S., Margoliash, D., 1995. Parallel pathways and convergence onto HVC and adjacent neostriatum of adult zebra finches (Taeniopygia-Guttata). J. Compar. Neurol. 360 (3), 413–441. Gentner, T.Q., Hulse, S.H., 2000. Female European starling preference and choice for variation in conspecific male song. Anim. Behav. 59, 443–458. Gentner, T.Q., Hulse, S.H., Duffy, D., Ball, G.F., 2001. Response biases in auditory forebrain regions of female songbirds following exposure to sexually relevant variation in male song. J. Neurobiol. 46 (1), 48–58. Godard, R., Wiley, R.H., 1995. Individual recognition of song repertoires in 2 wood warblers. Behav. Ecol. Sociobiol. 37 (2), 119–123. Gobes, S.M.H., Bolhuis, J.J., 2007. Birdsong memory: A neural dissociation between song recognition and production. Current Biology 17 (9), 789–793. Hernandez, A.M., 2007. Development of Song Preferences and the Neural Responses to Local Geographic Song in Songbirds. University of Western Ontario, London, Canada. Hernandez, A.M., MacDougall-Shackleton, S.A., 2004. Effects of early song experience on song preferences and song control and auditory brain regions in female house finches (Carpodacus mexicanus). J. Neurobiol. 59 (2), 247–258. Jin, H., Clayton, D.F., 1997. Localized changes in immediate-early gene regulation during sensory and motor learning in zebra finches. Neuron 19 (5), 1049–1059. Konishi, M., 1965. The role of auditory feedback on the control of vocalizations in white-crowned sparrows. Zietschrift far Tierpsychologie 22, 770–783. Konishi, M., 1985. Birdsong – from behavior to neuron. Annu. Rev. Neurosci. 8, 125–170. Kuhl, P.K., 2003. Human speech and birdsong: Communication and the social brain. Proc. Natl. Acad. Sci. U.S.A. 100 (17), 9645–9646. Lauay, C., Gerlach, N.M., Adkins-Regan, E., DeVoogd, T.J., 2004. Female zebra finches require early song exposure to prefer high-quality song as adults. Anim. Behav. 68, 1249–1255. Lauay, C., Komorowski, R.W., Beadin, A.E., DeVoogd, T.J., 2005. Adult female and male zebra finches show distinct patterns of spine deficits in an auditory area and in the song system when reared without exposure to normal adult song. J. Compar. Neurol. 487, 119–126. Leitner, S., Voigt, C., Metzdorf, R., Catchpole, C.K., 2005. Immediate early gene (ZENK, Arc) expression in the auditory forebrain of female canaries varies in response to male song quality. J. Neurobiol. 64, 275–284.
284
A.M. Hernandez et al. / Behavioural Processes 77 (2008) 278–284
MacDougall-Shackleton, S.A., Hulse, S.H., Ball, G.F., 1998. Neural bases of song preferences in female zebra finches (Taeniopygia guttata). Neuroreport 9 (13), 3047–3052. MacDougall-Shackleton, S.A., MacDougall-Shackleton, E.A., Hahn, T.P., 2001. Physiological and behavioural responses of female mountain white-crowned sparrows to natal- and foreign-dialect songs. Canad. J. Zool.-Revue Canadienne De Zoologie 79 (2), 325–333. Maney, D.L., MacDougall-Shackleton, E.A., MacDougall-Shackleton, S.A., Ball, G.F., Hahn, T.P., 2003. Immediate early gene response to hearing song correlates with receptive behavior and depends on dialect in a female songbird. J. Compar. Physiol. A 189 (9), 667–674. Maney, D.L., Cho, E., Goode, C.T., 2006. Estrogen-dependent selectivity of genomic responses to bird song. Eur. J. Neurosci. 23 (6), 153–159. Marler, P., 1970. A comparative approach to vocal learning: song development in white-crowned sparrows. J. Compar. Physiol. Psychol. 71, 1–25. Mello, C., Nottebohm, F., Clayton, D., 1995. Repeated exposure to one song leads to a rapid and persistent decline in an immediate-early genes response to that song in zebra finch telencephalon. J. Neurosci. 15 (10), 6919–6925. Mello, C.V., Vicario, D.S., Clayton, D.F., 1992. Song presentation induces geneexpression in the songbird forebrain. Proc. Natl. Acad. Sci. U.S.A. 89 (15), 6818–6822. Miller, D.B., 1979a. The acoustic basis of mate recognition by female zebra finches (Taeniopygia guttata). Anim. Behav. 27, 376–380. Miller, D.B., 1979b. Long-term recognition of father’s song by female zebra finches. Nature 280, 389–391. Nagle, L., Kreutzer, M.L., 1997a. Adult female domesticated canaries can modify their song preferences. Canad. J. Zool.-Revue Canadienne De Zoologie 75 (8), 1346–1350. Nagle, L., Kreutzer, M.L., 1997b. Song tutoring influences female song preferences in domesticated canaries. Behaviour 134, 89–104. Nelson, D.A., Marler, P., Soha, J.A., Fullerton, A.L., 1997. The timing of song memorization differs in males and females: a new assay for avian vocal learning. Anim. Behav. 54, 587–597. Njegovan, M., Weisman, R., 1997. Pitch discrimination in field- and isolationreared black-capped chickadees (Parus atricapillus). J. Compar. Psychol. 111 (3), 294–301. Nottebohm, F., Arnold, A.P., 1976. Sexual dimorphism in vocal control areas of the songbird brain. Science 194, 211–213. Nottebohm, F., 2005. The neural basis of birdsong. PLoS Biol. 3, e164. O’Loghlen, A.L., Beecher, M.D., 1999. Mate, neighbor and stranger songs: a female song sparrow perspective. Anim. Behav. 58, 13–20. O’Loghlen, A.L., Rothstein, S.I., 1995. Culturally correct song dialects are correlated with male age and female song preferences in wild populations of brown-headed cowbirds. Behav. Ecol. Sociobiol. 36 (4), 251–259. Phillmore, L.S., Bloomfield, L.L., Weisman, R.G., 2003a. Effects of songs and calls on ZENK expression in the auditory telencephalon of fieldand isolate-reared black capped chickadees. Behav. Brain Res. 147 (1–2), 125–134. Phillmore, L.S., Sturdy, C.B., Weisman, R.G., 2003b. Does reduced social contact affect discrimination of distance cues and individual vocalizations? Anim. Behav. 65, 911–922. Riebel, K., 2000. Early experience leads to repeatable preferences for male song in female zebra finches. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 267, 2553–2558.
Riebel, K., 2003. The “mute” sex revisited: Vocal production and perception learning in female songbirds. Adv. Study Behav. 33, 49–86. Riebel, K., Hall, M.L., Langmore, N.E., 2005. Female songbirds still struggling to be heard. Trends Ecol. Evolut. 20 (8), 419–420. Riebel, K., Slater, P.J.B., 1998. Testing female chaffinch song preferences by operant conditioning. Anim. Behav. 56, 1443–1453. Riebel, K., Smallegange, I.M., Terpstra, N.J., Bolhuis, J.J., 2002. Sexual equality in zebra finch song preference: evidence for a dissociation between song recognition and production learning. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 269 (1492), 729–733. Rowe, C., Skelhorn, J., 2004. Avian psychology and communication. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 271 (1547), 1435–1442. Searcy, W.A., Marler, P., 1981. A test for responsiveness to song structure and programming in female sparrows. Science 213 (4510), 926–928. Searcy, W.A., Nowicki, S., Hughes, M., Peters, S., 2002. Geographic song discrimination in relation to dispersal distances in song sparrows. Am. Natural. 159 (3), 221–230. Sockman, K.W., Gentner, T.Q., Ball, G.F., 2002. Recent experience modulates forebrain gene-expression in response to mate-choice cues in European starlings. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 269 (1508), 2479–2485. Sturdy, C.B., Phillmore, L.S., Weisman, R.G., 2000. Call-note discriminations in black-capped chickadees (Poecile atricapillus). J. Compar. Psychol. 114, 357–364. Sturdy, C.B., Phillmore, L.S., Sartor, J.J., Weisman, R.G., 2001. Reduced social contact causes auditory perceptual deficits in zebra finches, Taeniopygia guttata. Anim. Behav. 62, 1207–1218. Terpstra, N.J., Bolhuis, J.J., Riebel, K., van der Burg, J.M.M., den Boer-Visser, A., 2006. Localized brain activation specific to auditory memory in a female songbird. J. Comp. Neurol. 494 (5), 784–791. Tischmeyer, W., Grimm, R., 1999. Activation of immediate early genes and memory formation. Cell. Molec. Life Sci. 55, 564–574. Thorpe, W.H., 1958. The learning of song patterns by birds with special reference to the song of the chaffinch Fringilla coelebs. IBIS 100, 535–570. Tomaszycki, M.L., Sluzas, E.M., Sundberg, K.A., Newman, S.W., DeVoogd, T.J., 2006. Immediate early gene (ZENK) responses to song in juvenile female and male zebra finches: Effects of rearing environment. J Neurobiol. 66 (11), 1175–1182. Vallet, E., Beme, I., Kreutzer, M., 1998. Two-note syllables in canary songs elicit high levels of sexual display. Anim. Behav. 55, 291–297. Vignal, C., Andru, J., Mathevon, N., 2005. Social context modulates behavioural and brain immediate early gene responses to sound in male songbird. Eur. J. Neurosci. 2, 949–955. Wasserman, F.E., Cigliano, J.A., 1991. Song output and stimulation of the female in white-throated sparrows. Behav. Ecol. Sociobiol. 29 (1), 55–59. Weary, D.M., Guilford, T.C., Weisman, R.G., 1993. A product of discriminative learning may lead to female preferences for elaborate males. Evolution 47 (1), 333–336. Weisman, R., Shackleton, S., Ratcliffe, L., Weary, D., Boag, P., 1994. Sexual preferences of female zebra finches – Imprinting on Beak Color. Behaviour 128, 15–24. Yamaguchi, A., 1999. Auditory experience does not shape sexual preferences for songs in female northern cardinals. Behaviour 136, 309–329. Ziegler, H.P., Marler, P., 2004. Behavioural neurobiology of birdsong. Annal. NY Acad. Sci. 1016.
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Effects of learning on song preferences and Zenk expression in female songbirds Alexandra M. Hernandez a , Leslie S. Phillmore b , Scott A. MacDougall-Shackleton a,∗ a
Department of Psychology, University of Western Ontario, London, ON N6A 5C2, Canada b Department of Psychology, Dalhousie University, Halifax, NS B3H 4J1, Canada
Received 10 July 2007; received in revised form 6 November 2007; accepted 6 November 2007
Abstract Male songbirds learn to produce their songs, and females attend to these songs during mate choice. The evidence that female song preferences are learned early in life, however, is mixed. Here we review studies that have found effects of early song learning on adult song preferences, and those that have not. In at least some species, early experience with song can modify adult song preferences. Whether this learning needs to occur during an early sensitive phase, akin to male imitative vocal learning, or not remains an open question. Studies of the neural bases for female song preferences highlight activity (as measured by immediate-early gene induction) in regions of the auditory forebrain as often, but not always, being associated with song preferences. Immediate-early gene induction in these regions, however, is not specific to songs experienced early in life. On the whole, inherited factors, early experience, and adult experience all appear to play a role in shaping female songbirds preferences for male songs. © 2007 Elsevier B.V. All rights reserved. Keywords: Song learning; Birdsong; Zenk; Song preferences; Mate choice
The study of animal behavior has benefited tremendously from integration of a variety of approaches including psychology and behavioral ecology. Indeed, combining approaches has been critical for maintaining the study of birdsong as a leading example of integrative biology (Konishi, 1985). Integration of psychology and ecology has been an important movement in animal cognition in general and in birds in particular (e.g. Rowe and Skelhorn, 2004). Ron Weisman and colleagues have made many important contributions to this integration. These include the use of operant conditioning techniques to study the perception of natural signals: bird songs and calls (e.g. Sturdy et al., 2000), proposing a role for perceptual discrimination learning and the resultant ‘peak shift’ in the evolution of mating signals (Weary et al., 1993), and highlighting the importance of early learning for the development of adult perception of signals (Njegovan and Weisman, 1997; Sturdy et al., 2001; Phillmore et al., 2003a,b), and adult mate preferences (Weisman et al., 1994). In this review we highlight the importance of integrating approaches by reviewing the effects of early learning on adult female song preferences in songbirds. The neurobiology and
∗
Corresponding author. E-mail address: [email protected] (S.A. MacDougall-Shackleton).
0376-6357/$ – see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.beproc.2007.11.001
behavior of song production in males has been studied extensively, but song production by females (Riebel, 2003; Riebel et al., 2005), and the effects of learning on female song preferences have been studied far less. Below we review the evidence for early learning affecting female preferences for particular males’ songs and for songs from a particular geographic region. We then examine the potential auditory brain regions involved in female song preferences and how activity in these regions may be modulated by early experience. Further progress in this field will require continuation of an integrated approach to gain understanding of the effects of early learning on song preferences. 1. Female song preferences Song is a courtship signal involved in mate selection by female songbirds, and preferences for particular song features have been widely identified. In some species, females have a preference for greater song output, preferring males that sing for a longer duration (e.g., European starling, Sturnus vulgaris, Eens et al., 1991) or sing longer songs or at higher song rates (white-throated sparrow, Zonotrichia albicollis, Wasserman and Cigliano, 1991). Female songbirds have also been shown to have preferences for increased song complexity, preferring males that have larger song repertoires (sedge warbler, Acrocephalus
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schoenobaenus, Catchpole et al., 1984; song sparrow, Melospiza melodia, Searcy and Marler, 1981). In addition to preferences for specific song features, in species that exhibit geographic variation in song females often prefer songs from the geographic region in which they live over more distantly recorded song variants (brown-headed cowbird, Molothrus ater, O’Loghlen and Rothstein, 1995; song sparrow, Searcy et al., 2002; white-crowned sparrow Zonotrichia leucophrys, Baker et al., 1981; Casey and Baker, 1992; MacDougall-Shackleton et al., 2001). A female preference for the song of the local geographic area in these species suggests that female songbirds may learn song (Baker et al., 1981; Casey and Baker, 1992; MacDougall-Shackleton et al., 2001). 2. Female song learning? Male songbirds, the primary song producers, learn to sing their songs in a process akin to language production learning in humans (Thorpe, 1958; Marler, 1970; see Kuhl, 2003 for review). Birds pass through a sensory phase of song acquisition in early life where the songs they are exposed to become encoded as auditory memories. This is followed by a sensory-motor phase of song acquisition where young males begin to produce songs and eventually attempt to match their vocal output to the sensory representations of song, formed in the sensory phase, via auditory feedback. These phases of song acquisition fall within a sensitive phase early in development (Marler, 1970) whereby if either exposure to song or auditory feedback (Konishi, 1965) is disrupted the bird will fail to develop normal song. Thus normal song development in males is dependent on experience with song and the ability to match vocal output to the sensory memories of song via auditory feedback. Whether female song preferences for local song develop in a manner similar to song acquisition in males, where sensory representations of tutors’ songs are formed early in life, is less well understood. Laboratory studies controlling song exposure show mixed findings in terms of the importance of song exposure early in life on female song preference development. Some of the earliest experiments supporting the idea that females’ early experience affects song preferences in adulthood were performed by Miller (1979a,b). He showed that female zebra finches (Taeniopygia guttata) prefer the songs of their fathers or their mates compared to novel unfamiliar songs. Following this, in a double controlled study controlling for genetic influences, adult female zebra finches of two subspecies were shown to prefer the song of their tutor, over a non-tutor song, in adulthood (Clayton, 1990). Thus, at least in zebra finches, females exhibit preferences for songs to which they have been exposed over songs that are unfamiliar. However, whether there is a critical phase for this song learning is unknown. Moreover, in zebra finches each male in a colony sings a single unique song, so learning to recognize a particular male by his song would intuitively make adaptive sense. Furthermore, in species where males sing more than one song type the discrimination task would seem to be many times more difficult. How widespread, therefore, is female song recognition learning in species in which each male does not have a unique song?
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Canary males sing a variety of songs, and female domesticated canaries (Serinus canaria) prefer the songs to which they are exposed early in life (Nagle and Kreutzer, 1997a). However, these female canaries also demonstrate an experienceindependent preference for a specific song phrase (Vallet et al., 1998). Isolate, like aviary reared females, prefer broadband syllables produced at supernormal rates suggesting perceptual predispositions can drive preferences (Draganoiu et al., 2002), though song experience may modulate degree of responsiveness. In several other species of songbird, females do not show preferences for the songs heard early in life (swamp sparrow, M. georgiana, Balaban, 1988; chaffinch, Fringilla coelebs, Riebel and Slater, 1998; house finch, Carpodacus mexicanus, Hernandez and MacDougall-Shackleton, 2004; northern cardinal, Cardinalis cardinalis, Yamaguchi, 1999). Thus the effects of early learning on preferences for specific songs are mixed; the source of these mixed results is unclear. The question of female learning and song preferences has also been addressed in the study of preferences for local songs or song dialects. 3. Evidence of role of early experience on geographic song preference development Many species exhibit geographic variation in song. If this variation is discontinuous it is referred to as song dialects, but more continuous variation is common in many other species as well. Adult females commonly display preferences for local dialect songs, or songs from the local area (O’Loghlen and Rothstein, 1995; Searcy et al., 2002; Baker et al., 1981; Casey and Baker, 1992; MacDougall-Shackleton et al., 2001). Early auditory experience with song may play a role in the development of these local song preferences. Field reared whitecrowned sparrows captured as juveniles prefer songs from their location of capture in adulthood over songs from more distant regions (Baker et al., 1981; Casey and Baker, 1992; MacDougallShackleton et al., 2001). A female preference for the song of the local geographic area suggests that female songbirds of these species may, like males, learn song. However, these studies used only young birds tutored with the song of their location of capture and as such failed to control for possible genetic influences underlying local song preferences. House finches hand-reared in the laboratory and exposed to either local, foreign, or no song, preferred local song, independent of the songs with which they were tutored (Hernandez and MacDougall-Shackleton, 2004). Thus, there may be inherited components of song preferences. Demonstrating that geographic song preferences are learned independent of potential inherited preferences requires that a local bird exposed to a foreign song prefers the foreign song. Until recently, only Clayton’s (1990) study in zebra finches fully counterbalanced potential genetic influences. Hernandez (2007; dissertation) undertook a similarly designed study in song sparrows, a species where males, unlike male zebra finches, sing many song types. Females prefer larger song repertoires (Searcy and Marler, 1981) but also prefer songs from their local area (Searcy et al., 2002). Hernandez (2007; dissertation) hand reared birds captured from two locations in Ontario 450 km apart and tutored them with songs from the two sites in a fully
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Fig. 1. Song preferences of hand-reared female song sparrows. Birds were captured as nestlings from either eastern or western Ontario, hand-reared, and tutored with either songs from their natal location or from the other location. Song preference was measured in adulthood as time spent near playback speakers playing songs from the two locations. Females spent significantly more time near their tutor song, regardless of place of origin. Data from Hernandez (2007; dissertation).
counterbalanced design. In adulthood, these females showed a preference for songs of their tutor location, regardless of their genetic origin (Fig. 1). This clearly demonstrates a critical role for early experience in the development of geographic song preferences. Whether the influence of early experience has an early sensitive phase, as in male imitative vocal learning, remains an open question. In summary, the results of experiments on inherited and experiential influences on female song preferences are mixed, but in at least some species female song preferences appear to be shaped by prior experience with songs. Future work is required to determine how widespread this phenomenon is, the time course of this learning, and whether the time course varies across species as it does for song learning in males (so-called closeended versus open-ended song learners). The role of perceptual predispositions, early experience and adult experience may differ in their effect on song preferences among species. Future work is needed to better understand under what ecological circumstances different degrees of flexibility in the development of song preferences may be favored. 4. Neural correlates of song preferences The neural circuit underlying song learning and song production in male songbirds is well studied (see Ziegler and Marler, 2004; Nottebohm, 2005). This circuit consists of two descending pathways from the HVC. The anterior forebrain path consists of HVC projecting to area X, which projects to the medial portion of the dorsolateral nucleus of the thalamus (DLM) and the lateral portion of the magnocellular nucleus of the anterior nidopallium (LMAN), and on to the robust nucleus of the arcopallium (RA). Lesions to nuclei within this anterior forebrain pathway early in life disrupt song much more than do similar lesions to adults (Bottjer et al., 1984). The posterior descending pathway includes HVC, robust nucleus of the archistriatum (RA), and the tracheosyringeal part of the hypoglossal motor nucleus (nXI-
Its) which then innervates the muscles of the syrinx allowing song production. Although this song control system is critically important for imitative vocal learning and song production, its role in song perception and/or female song preferences is less clear. Studies of canaries, a species in which females sometimes sing, have shown that lesions to brain areas within the songcontrol system disrupt song perception and/or song preferences (Brenowitz, 1991; Burt et al., 2000; Del Negro et al., 1998). In contrast, lesions to HVC in female zebra finches (which never sing) failed to disrupt normal song preferences (MacDougallShackleton et al., 1998). This is perhaps not surprising given that HVC in female zebra finches is a small fraction the size of that in males (Nottebohm and Arnold, 1976) and exhibits cytoarchitecture and connectivity that differs from males (Fortune and Margoliash, 1995). In contrast, lesions to an auditory region CMM (caudal medial mesopallium) did disrupt song preferences in female zebra finches (MacDougall-Shackleton et al., 1998). While it is possible that differences seen in the involvement of the song-control system in song perception in females are due to damage to afferent projections from auditory regions, it can also be explained by species differences in song production by females. Evidence supporting the idea that auditory regions outside the traditional song circuit are specialized in perceptual processing of song includes the use of immediate-early gene (IEG) expression as a marker for neuronal activation, and electrophysiological studies. These studies point to the role of CMM and an adjacent structure, caudal medial nidopallium (NCM), in perceptual processing of song. The IEG Zenk (an acronym for Zif-268, Egr-1, NGIF-A, Krox-24), a transcription factor whose protein product is capable of binding to promoter regions on target genes upstream, has been widely used as an indicator of neural activation following song presentation. Zenk induction is thought to be an important step in a process that results in structural changes at the synapse, potentially changing the firing properties of the cell (see Tischmeyer and Grimm, 1999, for review), and as such is used to understand the neural correlates of learning and memory. Studies have found that NCM and CMM show highest levels of Zenk expression following the presentation of conspecific song over heterospecific song, and even less activation following tone bursts, followed by silence (Mello et al., 1992). Zenk activation within auditory areas also attenuates with repeated presentation of a particular song, with levels being raised once again following the presentation of a novel song (Mello et al., 1995). As well, different types of vocalizations can result in different levels of Zenk expression (Phillmore et al., 2003a,b). Thus studies looking at IEG expression demonstrate these structures play a role in processing biologically relevant auditory stimuli. Furthermore, electrophysiological studies that use microelectrodes to record activity of cells within these auditory areas have also shown habituation of activation after repeated presentation of the same song; this attenuated song specific response lasts for up to 2 days (Chew et al., 1995). Thus, auditory regions are involved in processing and discrimination of auditory stimuli, and may be critical to auditory perceptual learning.
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5. Auditory regions and female preferences Auditory regions in the avian forebrain involved in song perception have also been implicated in the expression of female song preferences. In female birds, greater activation in auditory regions has been demonstrated following the playback of several preferred song attributes. In a non-songbird, budgerigars (Melopsittacus undulatus), that prefers larger repertoires and more complex songs over less complex songs, these preferred songs result in greater IEG activation in a brain region similar to NCM (Eda-Fujiwara et al., 2003). Female European starlings, which prefer longer songs, also have higher activation in auditory regions following the playback of longer songs versus shorter songs (Gentner et al., 2001), even when overall amount of song to which females were exposed was controlled. Female whitecrowned sparrows show greater IEG activation in CMM and NCMd following local versus foreign song playback, and the strength of the IEG response was correlated to the number of solicitation displays performed (Maney et al., 2003). Thus, the auditory regions in the avian forebrain specialized in processing biologically relevant auditory stimuli, have been implicated in female preferences. How experience with song early in life and/or in adulthood modulates neural responses to song requires further investigation. 6. Evidence of the role of auditory regions in auditory learning Studies finding experience-dependent changes in neuronal activation in response to specific stimuli further support the idea that auditory regions are involved in perceptual learning. As discussed above, both electrophysiological (Chew et al., 1995) and IEG (Mello et al., 1995) activation in NCM habituate to the repeated presentation of a song, with dishabituation, or higher activation, occurring if a novel song is played. More recently, Sockman et al. (2002) found that in starlings recent previous exposure to long songs (which is preferred by the species studied, Gentner and Hulse, 2000) 1 day prior to playbacks, lead to even greater activation following exposure to long songs over short songs, than if no recent previous exposure to long songs occurred. In contrast, recent song exposure failed to lead to differential IEG expression in a study of adult female zebra finches. Miller (1979b) showed that female zebra finches behaviorally prefer their mate’s song over an unfamiliar song. However, playback of a male zebra finch’s song to his mate did not induce greater IEG activation than did playback of the same song to females that were not his mate (Phillmore, Kadis, Avey and MacDougall-Shackleton, unpublished; Fig. 2). Thus, experience with songs does not always lead to differential IEG expression. Determining when and why certain experiences with song modify IEG expression requires further study. Developmental studies looking at the neural correlates of song learning in maleshave implicated the auditory areas in song processing and memory. Jin and Clayton (1997) demonstrated Zenk within NCM becomes song inducible at an age when males begin to acquire song models. Though it seems
Fig. 2. Immediate-early gene induction by male song in female zebra finches. Females were either mated with the male in the playback or were unfamiliar with that male. Expression was measured in the dorsal caudomedial nidopallium (NCMd), ventral caudomedial nidopalium (NCMv), and caudomedial mesopallium (CMM). Data from Phillmore, Kadis, Avey and MacDougall-Shackleton (unpublished).
auditory experience, not actual song exposure, mediates normal Zenk responsiveness at a young age in that clutch reared isolate birds, but not solo isolates, show normal patterns of song induced Zenk. Bolhuis et al. (2000) found that IEG activation in NCM following playback of tutor song was correlated with strength of song learning (i.e. number of syllables copied from the tutor) in male zebra finches. These authors suggest that IEG expression in NCM is involved in the long-term representation of tutor songs. However, alternative explanations need to be ruled out including the possibility that if birds copy songs with high salience to them, this could in turn lead to greater activation when heard in adulthood due to its high salience. To better understand the role of NCM in auditory learning and memory, females serve as a good natural control since they do not produce song. In fact the strength of female song preferences and therefore presumably the strength of tutor song memory formation could be tested to see if it also correlates with the strength of IEG activation in NCM following tutor song playback. Developmental studies also examining IEG in juvenile females have been used to better understand the neural correlates of song learning and memory (Bailey and Wade, 2005). Recently, Tomaszycki et al. (2006) demonstrated that normal song reared males and females have higher levels of expression than untutored birds at 45 day, suggesting that exposure to song has general effects on Zenk responsiveness. Several studies have directly assessed whether early experience with song affects IEG activation in response to song in adult females. Hernandez and MacDougall-Shackleton (2004) showed that female house finches behaviorally preferred the local song regardless of which songs they were tutored with. In this study there was no difference in Zenk expression following song playback to either tutor or non-tutor song. This result is consistent with the level of song-induced Zenk activation reflecting the behavioral salience of the signal rather than auditory
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memories. Interestingly, females reared in isolation from song showed greater Zenk activation than the song tutored females. This finding, which may be analogous to findings of higher levels of Zenk when the sensitive period of song acquisition is open in zebra finch males (Jin and Clayton, 1997), suggests that isolate females may be in a more neuronally juvenile state, and that early song exposure may have general effects on Zenk neural responsivity. More recently Hernandez (2007; dissertation) found similar results in song sparrows. In this study, female song sparrows preferred their tutor songs regardless of their place of origin. However, Zenk activation did not differ in response to tutor versus non-tutor song. Again, Zenk activation was higher for isolate-reared females. Thus Zenk induction in the auditory forebrain is no greater following playback of songs learned early in life over novel songs. This finding is at odds with those in female zebra finch. Terpstra et al. (2006) found higher Zenk activation after the presentation of tutor song versus unfamiliar song in CMM in this species. While it is not clear what variables lead to these species differences in neural tuning to tutor song in auditory areas, it may be that in species where males only sing one song type (as in zebra finches) the cognitive demand of learning and remembering individual males’ songs is reduced. Interestingly, in female song sparrows, where behavioral evidence of females preferring tutor song clearly demonstrated females are able to learn many tutors songs (Hernandez, 2007; dissertation), we found no evidence that early experience tunes the neural responsiveness to tutor song in adulthood. Thus while it has been suggested that auditory regions are the site of tutor song memory storage (Gobes and Bolhuis, 2007), this is not the case for all species. Furthermore, although bilateral NCM lesions reduce the preferential response to tutor over novel song, birds still discriminate tutor from novel song following lesions (Gobes and Bolhuis, 2007). Given that ancestrally female songbirds were likely song producers (see Riebel et al., 2005), it may be that in species where females do not sing, as in zebra finches, the neuroanatomical distribution of auditory memories is different from species where females can sing, even if impoverished, songs. Furthermore, males and females may differ in their site of storage of auditory memories. Lauay et al. (2005) showed isolate reared male and female zebra finches differ in the degree to which deficits are seen in auditory regions versus song control nuclei. A more male-typical neuroanatomical distribution of tutor song may be present in species where females can sing and song nuclei are conserved. Thus, although a number of studies have shown a relation between the levels of Zenk induction in the auditory forebrain and song preferences (Eda-Fujiwara et al., 2003; Gentner et al., 2001; Leitner et al., 2005; Maney et al., 2003; Sockman et al., 2002), there is little direct evidence showing a connection between Zenk induction and early experience with songs. IEG induction in female songbirds’ auditory forebrain, then, appears to reflect the behavioral salience of the song, which can be modulated by recent experience (Sockman et al., 2002), social context (Vignal et al., 2005), sex steroids (Maney et al., 2006), among other factors, but does not seem to be specifically a marker of songs learned early in life.
6.1. Female song learning and song preferences While females of many temperate zone species do not sing, or sing less complex songs, song is still important in mate selection, and as such females may form long lasting representations of song. Several studies have shown that females respond preferentially to their mate’s song (song sparrows, O’Loghlen and Beecher, 1999; domesticated canaries, Serinus canaria, Beguin et al., 1998). Thus female songbirds are able to form lasting song memories regardless of song production. It has been suggested that sensory learning involved in recognition, and sensory learning involved in motor learning, may be dissociable (Riebel et al., 2002) and may rely on separate neural processes. Furthermore, it is not clear whether early sensory learning in females is distinct from recognition learning in adulthood, or whether females, like males of many species, possess a sensitive phase of song learning, beyond which the ability to learn new songs is reduced. Male songbirds, for example, have been shown to be able to recognize territorial neighbors and respond more aggressively to the song playback of a neighbor from an inappropriate boundary (Godard and Wiley, 1995), or to the song playback of a stranger versus a neighbor (Falls and Brooks, 1975). Yet in most species a male can only incorporate the songs they hear into their song repertoire when exposed to these songs within a limited window of time early in life. Therefore, sensory learning involved in song production, which occurs early in life, and sensory learning involved in song recognition learning in adulthood may be distinct in males. It is possible that female song recognition learning in adulthood could be distinct from sensory learning occurring early in life (Riebel, 2003). Whether females, like males, must hear song during an early sensitive phase to develop normal song preferences in adulthood requires further investigation. In female zebra finches, tutor songs that females were exposed to as juveniles were preferred to unfamiliar, but not tutor songs heard after sexual maturity, suggesting an enduring preference for songs heard earlier in life (Riebel, 2000). There is also evidence that the sensitive period may be shorter in female white-crowned sparrows, a species where females can sing (Nelson et al., 1997). However, experience with song in adulthood can also modify adult female white-crowned sparrow preferences (MacDougall-Shackleton et al., 2001), as is true in female domesticated canaries (Nagle and Kreutzer, 1997b). Recently, Lauay et al. (2004) demonstrated that early song exposure is critical for preferences for normal adult song over abnormal isolate song in female zebra finches. Isolate females also show deficits in dendritic spine density within auditory region NCM to a greater degree than males, who show larger deficits in song control nuclei HVC (Lauay et al., 2005). Furthermore it appears that at 45 days old differences are seen in Zenk response to normal versus isolate reared song in normal versus isolate reared birds (Tomaszycki et al., 2006). The long-term effect of absence of song exposure on Zenk responses in auditory regions in these birds is of interest. Whether isolate females have enduring deficits in auditory perception, song preferences, neuronal morphology and ZENK responses is of particular interest in understanding how early auditory learning differs from recognition learning in adulthood.
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While song preferences may be influenced by early song exposure, determining whether they are also modified and shaped into adulthood will help characterize auditory learning in songbirds. Thus it is important to delineate the time frame when song exposure can influence song preferences in females. It is not clear whether there is a sensitive period in auditory learning; it may be that the sensitive period seen in males is associated only with motor production aspects of song learning. For this reason, a better characterization of auditory learning in female songbirds is needed. Understanding the mechanisms and timing of female song preference development will also further help understand how these variables have shaped male song evolution and structure. 7. Conclusions Though historically ignored, a growing number of studies have begun to address song learning in female songbirds, including studies of how experience influences song preferences, and the neural bases of such learning. It is becoming clear that song preferences involve both learned and unlearned components. That is, exposure to song is required for the expression of some song preferences, but not others, and this varies from species to species. It is also clear that the auditory regions such as CMM and NCM play a role in song perception in female songbirds, and there is good evidence that exposure to song early in life (compared to isolate rearing) has some general effects on IEG responses to song, as isolates have repeatedly been shown to have enhanced responses. It is likely however, that IEG responses in CMM and NCM reflect the saliency of a stimulus, or overall attention rather than reflecting memory per se. Further studies with females are required to better understand the similarities and differences in song learning in male and female songbirds. Acknowledgments Our research program has been supported by NSERC, the Canada Foundation for Innovation, the Ontario Innovation Trust, and a Premier’s Research Excellence Award from the Province of Ontario. References Bailey, D.J., Wade, J., 2005. FOS and ZENK responses in 45-day-old zebra finches vary with auditory stimulus and brain region, but not sex. Behav. Brain Res. 162 (1), 108–115. Baker, M.C., Spitlernabors, K.J., Bradley, D.C., 1981. Early experience determines song dialect responsiveness of female sparrows. Science 214 (4522), 819–821. Balaban, E., 1988. Cultural and genetic-variation in swamp sparrows (Melospiza-Georgiana). 2. Behavioral salience of geographic song variants. Behaviour 105, 292–322. Beguin, N., LeBoucher, G., Kreutzer, M., 1998. Sexual preferences for mate song in female canaries (Serinus canaria). Behaviour 135, 1185–1196. Bolhuis, J.J., Zijlstra, G.G.O., den Boer-Visser, A.M., Van der Zee, E.A., 2000. Localized neuronal activation in the zebra finch brain is related to the strength of song learning. Proc. Natl. Acad. Sci. U.S.A. 97 (5), 2282–2285. Bottjer, S.W., Miesner, E.A., Arnold, A.P., 1984. Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224 (4651), 901–903.
283
Brenowitz, E.A., 1991. Altered perception of species-specific song by female birds after lesions of a forebrain nucleus. Science 251 (4991), 303–305. Burt, J.M., Lent, K.L., Beecher, M.D., Brenowitz, E.A., 2000. Lesions of the anterior forebrain song control pathway in female canaries affect song perception in an operant task. J. Neurobiol. 42 (1), 1–13. Casey, R.M., Baker, M.C., 1992. Early social tutoring influences female sexualresponse in white-crowned sparrows. Anim. Behav. 44 (5), 983–986. Catchpole, C.K., Dittami, J., Leisler, B., 1984. Differential responses to male song repertoires in female songbirds implanted with estradiol. Nature 312 (5994), 563–564. Chew, S.J., Mello, C., Nottebohm, F., Jarvis, E., Vicario, D.S., 1995. Decrements in auditory responses to a repeated conspecific song are long-lasting and require 2 periods of protein-synthesis in the songbird forebrain. Proc. Natl. Acad. Sci. U.S.A. 92 (8), 3406–3410. Clayton, N.S., 1990. Subspecies recognition and song learning in zebra finches. Anim. Behav. 40, 1009–1017. Del Negro, C., Gahr, M., Leboucher, G., Kreutzer, M., 1998. The selectivity of sexual responses to song displays: effects of partial chemical lesion of the HVC in female canaries. Behav. Brain Res. 96 (1–2), 151–159. Draganoiu, T.I., Nagle, L., Kreutzer, M., 2002. Directional female preference for an exaggerated male trait in canary (Serinus canaria) song. Proc. R. Soc. Lond. Ser. B: Biol. Sci. 269 (1509), 2525–2531. Eda-Fujiwara, H., Satoh, R., Bolhuis, J.J., Kimura, T., 2003. Neuronal activation in female budgerigars is localized and related to male song complexity. Eur. J. Neurosci. 17 (1), 149–154. Eens, M., Pinxten, R., Verheyen, R.F., 1991. Male song as a cue for mate choice in the European Starling. Behaviour 116, 210–238. Falls, J.B., Brooks, R.J., 1975. Individual recognition by song in white-throated sparrows, II. Effects of location. Canad. J. Zool. 53, 412–420. Fortune, E.S., Margoliash, D., 1995. Parallel pathways and convergence onto HVC and adjacent neostriatum of adult zebra finches (Taeniopygia-Guttata). J. Compar. Neurol. 360 (3), 413–441. Gentner, T.Q., Hulse, S.H., 2000. Female European starling preference and choice for variation in conspecific male song. Anim. Behav. 59, 443–458. Gentner, T.Q., Hulse, S.H., Duffy, D., Ball, G.F., 2001. Response biases in auditory forebrain regions of female songbirds following exposure to sexually relevant variation in male song. J. Neurobiol. 46 (1), 48–58. Godard, R., Wiley, R.H., 1995. Individual recognition of song repertoires in 2 wood warblers. Behav. Ecol. Sociobiol. 37 (2), 119–123. Gobes, S.M.H., Bolhuis, J.J., 2007. Birdsong memory: A neural dissociation between song recognition and production. Current Biology 17 (9), 789–793. Hernandez, A.M., 2007. Development of Song Preferences and the Neural Responses to Local Geographic Song in Songbirds. University of Western Ontario, London, Canada. Hernandez, A.M., MacDougall-Shackleton, S.A., 2004. Effects of early song experience on song preferences and song control and auditory brain regions in female house finches (Carpodacus mexicanus). J. Neurobiol. 59 (2), 247–258. Jin, H., Clayton, D.F., 1997. Localized changes in immediate-early gene regulation during sensory and motor learning in zebra finches. Neuron 19 (5), 1049–1059. Konishi, M., 1965. The role of auditory feedback on the control of vocalizations in white-crowned sparrows. Zietschrift far Tierpsychologie 22, 770–783. Konishi, M., 1985. Birdsong – from behavior to neuron. Annu. Rev. Neurosci. 8, 125–170. Kuhl, P.K., 2003. Human speech and birdsong: Communication and the social brain. Proc. Natl. Acad. Sci. U.S.A. 100 (17), 9645–9646. Lauay, C., Gerlach, N.M., Adkins-Regan, E., DeVoogd, T.J., 2004. Female zebra finches require early song exposure to prefer high-quality song as adults. Anim. Behav. 68, 1249–1255. Lauay, C., Komorowski, R.W., Beadin, A.E., DeVoogd, T.J., 2005. Adult female and male zebra finches show distinct patterns of spine deficits in an auditory area and in the song system when reared without exposure to normal adult song. J. Compar. Neurol. 487, 119–126. Leitner, S., Voigt, C., Metzdorf, R., Catchpole, C.K., 2005. Immediate early gene (ZENK, Arc) expression in the auditory forebrain of female canaries varies in response to male song quality. J. Neurobiol. 64, 275–284.
284
A.M. Hernandez et al. / Behavioural Processes 77 (2008) 278–284
MacDougall-Shackleton, S.A., Hulse, S.H., Ball, G.F., 1998. Neural bases of song preferences in female zebra finches (Taeniopygia guttata). Neuroreport 9 (13), 3047–3052. MacDougall-Shackleton, S.A., MacDougall-Shackleton, E.A., Hahn, T.P., 2001. Physiological and behavioural responses of female mountain white-crowned sparrows to natal- and foreign-dialect songs. Canad. J. Zool.-Revue Canadienne De Zoologie 79 (2), 325–333. Maney, D.L., MacDougall-Shackleton, E.A., MacDougall-Shackleton, S.A., Ball, G.F., Hahn, T.P., 2003. Immediate early gene response to hearing song correlates with receptive behavior and depends on dialect in a female songbird. J. Compar. Physiol. A 189 (9), 667–674. Maney, D.L., Cho, E., Goode, C.T., 2006. Estrogen-dependent selectivity of genomic responses to bird song. Eur. J. Neurosci. 23 (6), 153–159. Marler, P., 1970. A comparative approach to vocal learning: song development in white-crowned sparrows. J. Compar. Physiol. Psychol. 71, 1–25. Mello, C., Nottebohm, F., Clayton, D., 1995. Repeated exposure to one song leads to a rapid and persistent decline in an immediate-early genes response to that song in zebra finch telencephalon. J. Neurosci. 15 (10), 6919–6925. Mello, C.V., Vicario, D.S., Clayton, D.F., 1992. Song presentation induces geneexpression in the songbird forebrain. Proc. Natl. Acad. Sci. U.S.A. 89 (15), 6818–6822. Miller, D.B., 1979a. The acoustic basis of mate recognition by female zebra finches (Taeniopygia guttata). Anim. Behav. 27, 376–380. Miller, D.B., 1979b. Long-term recognition of father’s song by female zebra finches. Nature 280, 389–391. Nagle, L., Kreutzer, M.L., 1997a. Adult female domesticated canaries can modify their song preferences. Canad. J. Zool.-Revue Canadienne De Zoologie 75 (8), 1346–1350. Nagle, L., Kreutzer, M.L., 1997b. Song tutoring influences female song preferences in domesticated canaries. Behaviour 134, 89–104. Nelson, D.A., Marler, P., Soha, J.A., Fullerton, A.L., 1997. The timing of song memorization differs in males and females: a new assay for avian vocal learning. Anim. Behav. 54, 587–597. Njegovan, M., Weisman, R., 1997. Pitch discrimination in field- and isolationreared black-capped chickadees (Parus atricapillus). J. Compar. Psychol. 111 (3), 294–301. Nottebohm, F., Arnold, A.P., 1976. Sexual dimorphism in vocal control areas of the songbird brain. Science 194, 211–213. Nottebohm, F., 2005. The neural basis of birdsong. PLoS Biol. 3, e164. O’Loghlen, A.L., Beecher, M.D., 1999. Mate, neighbor and stranger songs: a female song sparrow perspective. Anim. Behav. 58, 13–20. O’Loghlen, A.L., Rothstein, S.I., 1995. Culturally correct song dialects are correlated with male age and female song preferences in wild populations of brown-headed cowbirds. Behav. Ecol. Sociobiol. 36 (4), 251–259. Phillmore, L.S., Bloomfield, L.L., Weisman, R.G., 2003a. Effects of songs and calls on ZENK expression in the auditory telencephalon of fieldand isolate-reared black capped chickadees. Behav. Brain Res. 147 (1–2), 125–134. Phillmore, L.S., Sturdy, C.B., Weisman, R.G., 2003b. Does reduced social contact affect discrimination of distance cues and individual vocalizations? Anim. Behav. 65, 911–922. Riebel, K., 2000. Early experience leads to repeatable preferences for male song in female zebra finches. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 267, 2553–2558.
Riebel, K., 2003. The “mute” sex revisited: Vocal production and perception learning in female songbirds. Adv. Study Behav. 33, 49–86. Riebel, K., Hall, M.L., Langmore, N.E., 2005. Female songbirds still struggling to be heard. Trends Ecol. Evolut. 20 (8), 419–420. Riebel, K., Slater, P.J.B., 1998. Testing female chaffinch song preferences by operant conditioning. Anim. Behav. 56, 1443–1453. Riebel, K., Smallegange, I.M., Terpstra, N.J., Bolhuis, J.J., 2002. Sexual equality in zebra finch song preference: evidence for a dissociation between song recognition and production learning. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 269 (1492), 729–733. Rowe, C., Skelhorn, J., 2004. Avian psychology and communication. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 271 (1547), 1435–1442. Searcy, W.A., Marler, P., 1981. A test for responsiveness to song structure and programming in female sparrows. Science 213 (4510), 926–928. Searcy, W.A., Nowicki, S., Hughes, M., Peters, S., 2002. Geographic song discrimination in relation to dispersal distances in song sparrows. Am. Natural. 159 (3), 221–230. Sockman, K.W., Gentner, T.Q., Ball, G.F., 2002. Recent experience modulates forebrain gene-expression in response to mate-choice cues in European starlings. Proc. R. Soc. Lond. Ser. B-Biol. Sci. 269 (1508), 2479–2485. Sturdy, C.B., Phillmore, L.S., Weisman, R.G., 2000. Call-note discriminations in black-capped chickadees (Poecile atricapillus). J. Compar. Psychol. 114, 357–364. Sturdy, C.B., Phillmore, L.S., Sartor, J.J., Weisman, R.G., 2001. Reduced social contact causes auditory perceptual deficits in zebra finches, Taeniopygia guttata. Anim. Behav. 62, 1207–1218. Terpstra, N.J., Bolhuis, J.J., Riebel, K., van der Burg, J.M.M., den Boer-Visser, A., 2006. Localized brain activation specific to auditory memory in a female songbird. J. Comp. Neurol. 494 (5), 784–791. Tischmeyer, W., Grimm, R., 1999. Activation of immediate early genes and memory formation. Cell. Molec. Life Sci. 55, 564–574. Thorpe, W.H., 1958. The learning of song patterns by birds with special reference to the song of the chaffinch Fringilla coelebs. IBIS 100, 535–570. Tomaszycki, M.L., Sluzas, E.M., Sundberg, K.A., Newman, S.W., DeVoogd, T.J., 2006. Immediate early gene (ZENK) responses to song in juvenile female and male zebra finches: Effects of rearing environment. J Neurobiol. 66 (11), 1175–1182. Vallet, E., Beme, I., Kreutzer, M., 1998. Two-note syllables in canary songs elicit high levels of sexual display. Anim. Behav. 55, 291–297. Vignal, C., Andru, J., Mathevon, N., 2005. Social context modulates behavioural and brain immediate early gene responses to sound in male songbird. Eur. J. Neurosci. 2, 949–955. Wasserman, F.E., Cigliano, J.A., 1991. Song output and stimulation of the female in white-throated sparrows. Behav. Ecol. Sociobiol. 29 (1), 55–59. Weary, D.M., Guilford, T.C., Weisman, R.G., 1993. A product of discriminative learning may lead to female preferences for elaborate males. Evolution 47 (1), 333–336. Weisman, R., Shackleton, S., Ratcliffe, L., Weary, D., Boag, P., 1994. Sexual preferences of female zebra finches – Imprinting on Beak Color. Behaviour 128, 15–24. Yamaguchi, A., 1999. Auditory experience does not shape sexual preferences for songs in female northern cardinals. Behaviour 136, 309–329. Ziegler, H.P., Marler, P., 2004. Behavioural neurobiology of birdsong. Annal. NY Acad. Sci. 1016.