Effects of learning on song preferences and Zenk expression in female songbirds

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.     

鸣禽发声控制核团内的神经递质及其在发声学习中的作用

神经递质在鸣禽脑中不仅是神经元间信号传递中介物质,还有资料表明它们通过在习鸣敏感期影响发声控制团间的突触联系的形成和突触可塑性,从而对鸣转类型的确定和巩固起重要作用,本文着重介绍了鸣禽发声控制核团内神经递质的分布及变化情况,并就神经递质在发声学习中的作用进行了探讨。     

鸣禽前端脑通路与鸣唱可塑性

前端脑通路即鸣禽的基底神经节——前脑通路,为鸣唱学习和可塑性所必需。本文综述了前端脑通路的起源、发育、作用及其鸣唱可塑性方面的最新进展。     

Memory in the making: localized brain activation related to song learning in young songbirds

Songbird males learn to sing their songs from an adult ‘tutor’ early in life, much like human infants learn to speak. Similar to humans, in the songbird brain there are separate neural substrates for vocal production and for auditory memory. In adult songbirds, the caudal pallium, the avian equivalent of the auditory association cortex, has been proposed to contain the neural substrate of tutor song memory, while the song system is involved in song production as well as sensorimotor learning. If this hypothesis is correct, there should be neuronal activation in the caudal pallium, and not in the song system, while the young bird is hearing the tutor song. We found increased song-induced molecular neuronal activation, measured as the expression of an immediate early gene, in the caudal pallium of juvenile zebra finch males that were in the process of learning to sing their songs. No such activation was found in the song system. Molecular neuronal activation was significantly greater in response to tutor song than to novel song or silence in the medial part of the caudomedial nidopallium (NCM). In the caudomedial mesopallium, there was significantly greater molecular neuronal activation in response to tutor song than to silence. In addition, in the NCM there was a significant positive correlation between spontaneous molecular neuronal activation and the strength of song learning during sleep. These results suggest that the caudal pallium contains the neural substrate for tutor song memory, which is activated during sleep when the young bird is in the process of learning its song. The findings provide insight into the formation of auditory memories that guide vocal production learning, a process fundamental for human speech acquisition.     

Managing breeding forest songbirds with conspecific song playbacks

Recent studies confirm that several territorial songbird species use conspecific cues, including song, when selecting habitat. We conducted a controlled experiment with a population of black-throated blue warblers Dendroica caerulescens , a species of concern in boreal hardwood transition forests, to determine whether song playbacks influence settlement patterns. We tested whether conspecific song broadcast during spring arrival attracts black-throated blue warblers during territory establishment, and whether song playbacks shift territories from the previous year's breeding distributions. The results of our experiment demonstrate that song playbacks significantly increased territorial occupancy and shifted territories closer to the speakers. Loss of breeding habitat is implicated in population declines of many songbirds, and our results suggest that song playbacks should be further investigated as a tool for mitigating the effects of disruptive management actions. Additional work should consider the spatial arrangement of playback speakers to avoid attracting birds from safe areas. The demographic consequences of conspecific attraction must also be explored before this technique is widely implemented.     

Role of gene regulation in song circuit development and song learning

The songbird has emerged as an important model for study of brain-behavior relationships by virtue of its rich natural advantages and from the pioneering efforts of explorers using anatomical and behavioral approaches. Now, molecular biology is providing a new and complementary paradigm for discerning songbird brain organization and function. Here, I review the work over the last 10 years that has laid the foundation for approaching songbird biology from the molecular perspective. As a result of this work, specific hypotheses can now be framed and tested regarding the mechanisms behind song circuit formation, behavioral plasticity, and the boundaries of adaptability. Age-related changes in more than 15 molecules have been observed in the song system of juvenile zebra finches, and these changes seem to define specific phases in circuit development. In adult songbirds, ordinary song-related activities such as singing and listening cause dramatic increases in gene expression in brain areas specific to each activity. The sensitivity of gene activation is modulated as a result of experience in adulthood and also changes during juvenile song learning. These studies have provided unexpected insights into the functional organization of the song circuit and the potential role of extrinsic modulatory systems in directing and limiting plastic change in the brain. With this rich base of knowledge, and techniques of gene manipulation on the horizon, answers to old questions seem within our reach: What sets the boundaries of neural plasticity? What limits learning? © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 549–571, 1997     

Open-ended song learning in a hummingbird

Vocal learning in birds is typically restricted to a sensitive period early in life, with the few exceptions reported in songbirds and parrots. Here, we present evidence of open-ended vocal learning in a hummingbird, the third avian group with vocal learning. We studied vocalizations at four leks of the long-billed hermit Phaethornis longirostris during a four-year period. Individuals produce a single song repertoire, although several song-types can coexist at a single lek. We found that nine of 49 birds recorded on multiple days (18%) changed their song-type between consecutive recordings. Three of these birds replaced song-types twice. Moreover, the earliest estimated age when song replacement occurred ranged from 186 to 547 days (mean = 307 days) and all nine birds who replaced song-types produced a crystallized song before replacement. The findings indicate that song-type replacement is distinct from an initial early learning sensitive period. As half of lekking males do not survive past the first year of life in this species, song learning may well extend throughout the lifespan. This behaviour would be convergent to vocal learning programmes found in parrots and songbirds.     

Individual vocal recognition and the effect of partial lesions to HVc on discrimination, learning, and categorization of conspecific song in adult songbirds

Among songbirds, the capacity to associate particular songs with particular singers (i.e., vocal recognition) forms the cognitive basis for more complex communication behaviors such as female choice and territoriality. In the present study, we combine operant conditioning techniques and excitotoxic lesions to the forebrain nucleus HVc to examine the role of this region in the discrimination, associative learning, and categorization of conspecific song. We trained adult male and female European starlings, Sturnus vulgaris, to recognize simultaneously the songs of several conspecific males. Then, using a series of transfer procedures, we demonstrate that correct recognition does not generalize to song bouts containing novel motifs from familiar singers. This suggests that starlings do not make use of individually invariant source or filter characteristics for vocal recognition. We then lesioned a portion of HVc bilaterally with ibotenic acid, and exposed the birds to a series of manipulations testing the discrimination, associative learning, and categorization of conspecific song. The lesions attenuated song production among males, but retention of the basic recognition task (i.e., maintenance of the discrimination) was unaffected. However, when the response contingencies were reversed-as a test of associative learning independent of discrimination-the initial performance and subsequent learning rate were negatively correlated with the size of the HVc lesions. This suggests that HVc plays a role in the formation of associations between a song and some referent. The results of this study are discussed in light of earlier claims regarding the role of HVc in the perceptual processing of conspecific song.     

鸣禽鸣叫学习的神经生物学机制

鸣禽鸣叫具有复杂的神经生理和生化基础,表现为一种复杂的学习过程。鸣啭控制系统是研究神经系统与学习、行为和发育关系的重要模型。而鸣禽鸣叫学习行为与鸣啭控制系统内长时程增强效应、神经元超微结构的改变和神经核团内的电活动、激素水平高低及其周期性变化、神经元再生或改变、即早基因的表达等方面密切相关。对鸣禽鸣叫的神经生物学机制进行了综述。     

Quality of song learning affects female response to male bird song

Bird song is unusual as a sexually selected trait because its expression depends on learning as well as genetic and other environmental factors. Prior work has demonstrated that males who are deprived of the opportunity to learn produce songs that function little if at all in male-female interactions. We asked whether more subtle variation in male song-learning abilities influences female response to song. Using a copulation solicitation assay, we measured the response of female song sparrows (Melospiza melodia) to songs of laboratory-reared males that differed in the amount of learned versus invented material that they included and in the degree to which learned material accurately matched the model from which it was copied. Females responded significantly more to songs that had been learned better, by either measure. Females did not discriminate between the best-learned songs of laboratory-reared males and songs of wild males used as models during learning. These results provide, to our knowledge, a first experimental demonstration that variation in learning abilities among males plays a functionally important part in the expression of a sexually selected trait, and further provide support for the hypothesis that song functions as an indicator of male quality because it reflects variation in response to early developmental stress.     

Stimulatory effects on the reproductive axis in female songbirds by conspecific and heterospecific male song

Courtship vocalizations of male songbirds can profoundly enhance the reproductive physiology and behavior of conspecific females. However, no study has fully investigated the selectivity of conspecific song effects on reproductive development in birds. We studied the effects of conspecific and heterospecific song on reproductive development in domesticated (canaries) and wild songbirds (song sparrows). As expected, conspecific song enhanced follicular development. Unexpectedly, however, birds exposed to heterospecific song also underwent enhanced follicular development (compared to birds exposed to no song); conspecific and heterospecific songs were equally effective in enhancing ovarian development. In canaries exposed to 18L:6D, conspecific song induced oviposition earlier and at a greater frequency than in heterospecific and no song groups, with the fewest eggs being laid in the no song group. These results indicate that conspecific and heterospecific male song can enhance reproductive activity in female songbirds. Whether or not activation of the reproductive axis in female songbirds by heterospecific song occurs in the wild remains unclear. It is also unclear as to whether the ability of the reproductive axis to respond to heterospecific song performs a specific function, or whether it is simply a consequence of greater selection pressure acting upon behavioral responses to song.     

Circuits,hormones, and learning: Vocal behavior in songbirds

Species-typical vocal patterns subserve species identification and communication for individual organisms. Only a few groups of organisms learn the sounds used for vocal communication, including songbirds, humans, and cetaceans. Vocal learning in songbirds has come to serve as a model system for the study of brain-behavior relationships and neural mechanisms of learning and memory. Songbirds learn specific vocal patterns during a sensitive period of development via a complex assortment of neurobehavioral mechanisms. In many species of songbirds, the production of vocal behavior by adult males is used to defend territories and attract females, and both males and females must perceive vocal patterns and respond to them. In both juveniles and adults, specific types of auditory experience are necessary for initial song learning as well as the maintenance of stable song patterns. External sources of experience such as acoustic cues must be integrated with internal regulatory factors such as hormones, neurotransmitters, and cytokines for vocal patterns to be learned and produced. Thus, vocal behavior in songbirds is a culturally acquired trait that is regulated by multiple intrinsic as well as extrinsic factors. Here, we focus on functional relationships between circuitry and behavior in male songbirds. In that context, we consider in particular the influence of sex hormones on vocal behavior and its underlying circuitry, as well as the regulatory and functional mechanisms suggested by morphologic changes in the neural substrate for song control. We describe new data on the architecture of the song system that suggests strong similarities between the songbird vocal control system and neural circuits for memory, cognition, and use-dependent plasticity in the mammalian brain. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 602–618, 1997     

Cultural niche construction of repertoire size and learning strategies in songbirds

Birdsong is a complex cultural and biological system, and the selective forces driving evolutionary changes in aspects of song learning vary considerably among species. The extent to which repertoire size, the number of syllables or song types sung by a bird, is subject to sexual selection is unknown, and studies to date have provided inconsistent evidence. Here, we propose that selection pressure on the size and complexity of birdsong repertoires may facilitate the construction of a niche in which learning, sexual selection, and song-based homophily may co-evolve. We show, using a review of the birdsong literature and mathematical modeling, that learning mode (open-ended or closed-ended learning) is correlated with the size of birdsong repertoires. Underpinning this correlation may be a form of cultural niche construction in which a costly biological trait (for example, open-ended learning) can spread in a population (or be lost) as a result of direct selection on an associated cultural trait (for example, song repertoire size).     

Immediate and long-term effects of testosterone on song plasticity and learning in juvenile song sparrows

Steroid sex hormones play critical roles in the development of brain regions used for vocal learning. It has been suggested that puberty-induced increases in circulating testosterone (T) levels crystallize a bird's repertoire and inhibit future song learning. Previous studies show that early administration of T crystallizes song repertoires but have not addressed whether new songs can be learned after this premature crystallization. We brought 8 juvenile song sparrows (Melospiza melodia) into the laboratory in the late summer and implanted half of them with subcutaneous T pellets for a two week period in October. Birds treated with T tripled their singing rates and crystallized normal songs in 2 weeks. After T removal, subjects were tutored by 4 new adults. Birds previously treated with T tended toward learning fewer new songs post T, consistent with the hypothesis that T helps to close the song learning phase. However, one T-treated bird proceeded to learn several new songs in the spring, despite singing perfectly crystallized songs in the fall. His small crystallized fall repertoire and initial lag behind other subjects in song development suggest that this individual may have had limited early song learning experience. We conclude that an exposure to testosterone sufficient for crystallization of a normal song repertoire does not necessarily prevent future song learning and suggest that early social experiences might override the effects of hormones in closing song learning.     

Response biases in auditory forebrain regions of female songbirds following exposure to sexually relevant variation in male song

In many species of songbirds, individual variation between the songs of competing males is correlated with female behavioral preferences. The neural mechanisms of song based female preference in songbirds are not known. Working with female European starlings (Sturnus vulgaris), we used immunocytochemistry for ZENK protein to localize forebrain regions that respond to sexually relevant variation in conspecific male song. The number of ZENK-ir cells in ventral caudo-medial neostriatum [NCMv] was significantly higher in females exposed to longer songs than in those exposed to shorter songs, whereas variation in the total duration of song exposure yielded no significant differences in ZENK expression. ZENK expression in caudo-medial ventral hyperstriatum [cmHV] was uniformly high in all subjects, and did not vary significantly among the three groups. These results suggest that subregions of NCM in female starlings are tuned to variation in male song length, or to song features correlated therewith. Female starlings exhibit robust behavioral preferences for longer over shorter male songs (Gentner and Hulse; Anim Behav 59:443-458, 2000). Therefore, the results of this study strongly implicate NCM in at least a portion of the perceptual processes underlying the complex natural behavior of female choice.     

Functional differences in forebrain auditory regions during learned vocal recognition in songbirds

Converging evidence implicates the auditory forebrain regions caudal medial mesopallium (formerly cmHV) and caudal medial nidopallium in the perceptual processing of conspecific vocalizations in songbirds. Little is known however, about more specific processing within these regions especially during song-based perceptual behaviors. One hallmark of the caudal medial mesopallium and caudal medial nidopallium, areas analogous to mammalian secondary auditory cortical structures, is their robust expression of the immediate-early-gene zenk in response to conspecific songs. Using European starlings operantly trained to recognize the songs of individual conspecifics, we show that the levels and patterns of zenk protein expression in the caudal medial nidopallium and caudal medial mesopallium differ when song recognition demands are placed on the system. In the caudal medial mesopallium, expression is significantly elevated above basal levels during the recognition of familiar songs, the acquisition of novel associations for familiar songs, and the acquisition of novel song discriminations. In the caudal medial nidopallium, however, expression is significantly elevated above basal levels only during the acquisition of novel song discriminations. The results directly implicate the caudal medial nidopallium and caudal medial mesopallium in at least a portion of the auditory processes underlying vocal recognition. Moreover, the observed differences between these regions imply the functional localization (or at least the concentration) of different auditory processing mechanisms within the caudal medial nidopallium and the caudal medial mesopallium.