The Onset of Song Learning and Song Tutor Selection in Fledgling Zebra Finches

We investigated song development in the pre‐independent zebra finch (aged 15–35 d), a period when neural pathways for song learning and production are forming and social influences outside the family are limited. Expt 1 investigated the onset and the minimum duration of tutoring needed for song learning in fledglings. We found most begin to learn song from 25 d of age and need about 10 d contact with the father tutor to make accurate copies. This onset corresponds with major developments in the formation of the neural circuitry implicated in song acquisition. Subsong also begins on day 25 suggesting that the sensory and motor phases of song learning fully overlap in the zebra finch. Our findings support the hypothesis that the song circuitry is fully functional by 35 d of age and the sensitive phase for zebra finches extends therefore from about days 25–65. However, only the first 10 d of this period are necessary to learn a tutor's song with fair accuracy. Expt 2 investigated the role of the paternal bond, spatial proximity and mating status in a fledgling's choice of song tutor where the father was the sole parent. Young chose the father over single unrelated males (expt 2a) or unrelated males in company with their female partners (expt 2b). Given the close spatial proximity of both potential tutors to the fledglings it is probably the filial bond, established via paternal care that is the cause of this preference. Zebra finches sing the same song phrase in two contrasting contexts: female‐directed song during pre‐copulatory courtship and undirected song where no female or display is involved. In expt 3 we tested the song learning preference of pre‐independent young for two categories of non‐paternal tutors: those singing predominantly female‐directed song and those singing exclusively undirected song. There was a small, but significant, preference for fledgling zebra finches to copy songs from males that sang female‐directed song. This preference is consistent with the hypothesis that young males not only learn the acoustic features of their tutor's song but also the visual and dynamic movements that constitute the courtship display.     

Birdsong memory: a neural dissociation between song recognition and production

Songbirds learn their song from an adult conspecific tutor when they are young, much like the acquisition of speech in human infants. When an adult zebra finch is re-exposed to its tutor's song, there is increased neuronal activation in the caudomedial nidopallium (NCM), the songbird equivalent of the auditory association cortex. This neuronal activation is related to the fidelity of song imitation, suggesting that the NCM may contain the neural representation of song memory. We found that bilateral neurotoxic lesions to the NCM of adult male zebra finches impaired tutor-song recognition but did not affect the males' song production or their ability to discriminate calls. These findings demonstrate that the NCM performs an essential role in the representation of tutor-song memory. In addition, our results show that tutor-song memory and a motor program for the bird's own song have separate neural representations in the songbird brain. Thus, in both humans and songbirds, the cognitive systems of vocal production and auditory recognition memory are subserved by distinct brain regions.     

Neural song preference during vocal learning in the zebra finch depends on age and state

The zebra finch acquires its song by first memorizing a model song from a tutor and then matching its own vocalizations to the memory trace of the tutor song, called a template. Neural mechanisms underlying this process require a link between the neural memory trace and the premotor song circuitry, which drives singing. We now report that a premotor song nucleus responds more to the tutor song model than to every other stimulus examined, including the bird's own song (BOS). Neural tuning to the song model occurred only during waking and peaked during the template-matching period of development, when the vocal motor output is sculpted to match the tutor song. During the same developmental phase, the BOS was the most effective excitatory stimulus during sleep. The preference for BOS compared to tutor song inverted with sleep/wake state. Thus, song preference shifts with development and state.     

The hippocampus and caudomedial neostriatum show selective responsiveness to conspecific song in the female zebra finch

The perception of song is vital to the reproductive success of both male and female songbirds. Several neural structures underlying this perception have been identified by examining expression of immediate early genes (IEGs) following the presentation of conspecific or heterospecific song. In the few avian species investigated, areas outside of the circuit for song production contain neurons that are active following song presentation, specifically the caudal hyperstriatum ventrale (cHV) and caudomedial neostriatum (NCM). While studied in detail in the male zebra finch, IEG responses in these neural substrates involved in song perception have not been quantified in females. Therefore, adult female zebra finches were presented with zebra finch song, nonzebra finch song, randomly generated tones, or silence for 30 min. One hour later they were sacrificed, and their brains removed, sectioned, and immunocytochemically processed for FOS expression. Animals exposed to zebra finch song had a significantly higher density of FOS-immunoreactive cells in the NCM than those presented with other songs, tones, or silence. Neuronal activation in the cHV was equivalent in birds that heard zebra finch and non-zebra finch song, expression that was higher than that observed in the groups that heard no song. Interestingly, the hippocampus (HP) and adjacent parahippocampal area (AHP) were activated in a manner comparable to the NCM. These results suggest a general role for the cHV in song perception and a more specific role for the NCM and HP/AHP in facilitating recognition of and responsiveness to species-specific song in female zebra finches.     

Comparative approaches to avian song system function: insights into auditory and motor processing

Many fundamental advances in our understanding of basic neural function have been made using bird song learning and performance as a model system. These advances have included a greater understanding of higher-order neural processing, developmental and hormonal influences on behavior, and the realization that neurogenesis plays an important role in normal adult brain function. The great diversity of passerine birds and song-related behaviors they exhibit suggest that oscine songbirds are ideally suited for comparative studies. While the comparative approach has been used successfully in the past to study song-related phenomena at anatomical and behavioral levels, it has been underutilized in addressing questions at the neurophysiological level. Most neurophysiological studies of songbird auditory and motor processing have been performed in one species, the zebra finch (Taeniopygia guttata). We present and compare neurophysiological studies we have performed in zebra finches and song sparrows (Melospiza melodia), species that differ markedly in their singing behavior and song repertoire characteristics. Interspecific similarities, and striking differences, in song neural processing are apparent. While preliminary, these data suggest that comparative neurophysiological studies of species carefully chosen for their vocal repertoire and singing behavior will contribute significantly to our understanding of vertebrate sensory and motor neural processing.     

Song recognition memory in juvenile zebra finches: effects of varying the number of presentations of heterospecific and conspecific songs

Seven male and three female zebra finches were exposed to 14 zebra finch (CON) and 14 starling (HET) songs during their sensitive period for song learning and then tested for their recognition memory of both the CON and HET songs in two separate memory tests. Amount of song exposure was varied by presenting individual songs either 3, 9, 27, or 81 times per day for nine consecutive days. After song exposure the birds were trained to discriminate two of the exposed, familiar songs (FAM) from two novel songs (NOV) in a go/no-go operant discrimination procedure, with FAM songs as "go" stimuli. Following discrimination training, untrained FAM and NOV songs were presented as probe songs without reinforcement. Birds responded more to FAM than NOV songs at all levels of song exposure, indicating that the songs were recognized. There were no differences in recognition memory for CON and HET song at any level of song exposure. The results suggest that selective song learning does not result from selective memorization of conspecific song.     

Lesions of a telencephalic nucleus in male zebra finches: Influences on vocal behavior in juveniles and adults

Male zebra finches learn to sing during a restricted phase of juvenile development. Song learning is characterized by the progressive modification of unstable song vocalizations by juvenile birds during development, a process that leads to the production of stereotyped vocal patterns as birds reach adulthood. The medial magnocellular nucleus of the anterior neostriatum (mMAN) is a small cortical region that has been implicated in song behavior based on its neuronal projection to the High Vocal Center (HVC), a nucleus that is critical for adult vocal production and presumably also plays a role in song learning. To assess the function of mMAN in song, ibotenic acid lesions of this brain region were made in juvenile male zebra finches during the period of vocal learning (40-50 days of age) and in adult males that were producing stable song (>90 days of age). Birds lesioned as juveniles produced highly abnormal, poor quality song as adults. Although the overall song quality of birds lesioned as adults was not highly disrupted or abnormal, the postoperative song behavior of these birds was discernibly different due to slight increases in variability of vocal production, particularly at the onset of singing. These results demonstrate that mMAN plays some important role in vocal production during the sensitive period for song learning, and is also important for consistent initiation and stereotyped production of adult song behavior.     

Diet and birdsong: short‐term nutritional enrichment improves songs of adult Bengalese finch males

Song is a notable sexual signal of birds, and serves as an honest indicator of male quality. Condition dependence of birdsong has been well examined from the viewpoint of the developmental stress hypothesis, which posits that complex songs assure fitness because learned acoustic features of songs are especially susceptible to early‐life stress that young birds experience in song learning periods. The effect of early stress on song phenotypes should be crucial, especially in age‐limited song learners which sing stereotyped songs throughout life. However, little attention has been paid to non‐learned song features that can change plastically even in adulthood of age‐limited song‐learners. Although it has been shown that food availability affects song rate in wild songbirds, there is limited evidence of the link between favorable nutritional conditions and song phenotypes other than song rate. Under the prediction that singing behavior reflects an individual's recent life history, we kept adult Bengalese finch males under high‐nutrition or normal diet for a short term, and examined changes in body mass and songs. We found that birds on a high‐nutrition diet showed higher song output (e.g. song rate and length) compared with those of the control group, while changes in body mass were moderate. In addition, note repertoire became more consistent and temporal structures got faster in both nutrition and control groups, which indicates that songs were subject to other factors than nutrition. Considering that female estrildid finches, including Bengalese and zebra finches, show a preference toward complex songs as well as longer songs and higher song rate, it is plausible that different aspects of singing behavior signal different male qualities, and provide multifaceted clues to females that choose mates.     

At the interface of the auditory and vocal motor systems: NIf and its role in vocal processing,production and learning

Communication between auditory and vocal motor nuclei is essential for vocal learning. In songbirds, the nucleus interfacialis of the nidopallium (NIf) is part of a sensorimotor loop, along with auditory nucleus avalanche (Av) and song system nucleus HVC, that links the auditory and song systems. Most of the auditory information comes through this sensorimotor loop, with the projection from NIf to HVC representing the largest single source of auditory information to the song system. In addition to providing the majority of HVC’s auditory input, NIf is also the primary driver of spontaneous activity and premotor-like bursting during sleep in HVC. Like HVC and RA, two nuclei critical for song learning and production, NIf exhibits behavioral-state dependent auditory responses and strong motor bursts that precede song output. NIf also exhibits extended periods of fast gamma oscillations following vocal production. Based on the converging evidence from studies of physiology and functional connectivity it would be reasonable to expect NIf to play an important role in the learning, maintenance, and production of song. Surprisingly, however, lesions of NIf in adult zebra finches have no effect on song production or maintenance. Only the plastic song produced by juvenile zebra finches during the sensorimotor phase of song learning is affected by NIf lesions. In this review, we carefully examine what is known about NIf at the anatomical, physiological, and behavioral levels. We reexamine conclusions drawn from previous studies in the light of our current understanding of the song system, and establish what can be said with certainty about NIf’s involvement in song learning, maintenance, and production. Finally, we review recent theories of song learning integrating possible roles for NIf within these frameworks and suggest possible parallels between NIf and sensorimotor areas that form part of the neural circuitry for speech processing in humans.     

Androgen metabolism in the juvenile oscine forebrain: A cross‐species analysis at neural sites implicated in memory function

Juvenile songbirds are useful models for studying the neural bases of memory. Memory‐reliant behaviors demonstrated at this stage include song learning (most songbirds) and food caching (food‐storing songbirds). Sex steroids are implicated in the modulation of memory processes in several vertebrates. The songbird forebrain expresses aromatase, 5α‐reductase and 5β‐reductase, enzymes which convert testosterone to estradiol, 5α‐, and 5β‐dihydrotestosterone, respectively. To explore the role of local androgen metabolism on memory processes, we documented the activities of these enzymes in the anterior neostriatum (NAN), caudomedial neostriatum (NCM), and hippocampus (HP) of four species of juvenile songbird, two of which are food storers. Areas were dissected, homogenized, and provided with radiolabeled substrate; and formed estrogens, and 5α‐ and 5β‐reduced androgens were measured. In the NAN, 5β‐reductase was the predominant enzyme, suggesting that local inactivation of testosterone may preserve the sensitive period of song acquisition. In the NCM, estrogens were formed in abundance despite high 5β‐reductase, suggesting that locally high estrogen synthesis may play a role in processes of song perception. In the HP, both estrogens and 5α reduced androgens were formed, suggesting that HP function may be modulated by both estrogens and androgens. Finally, a derived measure of steroid‐differential reveals that food‐storing songbirds differ from nonstorers in the steroidal milleiu within the HP, but not in the NAN or NCM. Thus, distinct loci within the juvenile songbird forebrain are exposed to different patterns of androgen metabolites. This local conversion may play a role in the neuroendocrine modulation of memory in these birds. © 1999 John Wiley & Sons, Inc. J Neurobiol 40: 397–406, 1999     

Early life conditions that impact song learning in male zebra finches also impact neural and behavioral responses to song in females

Early life stressors can impair song in songbirds by negatively impacting brain development and subsequent learning. Even in species in which only males sing, early life stressors might also impact female behavior and its underlying neural mechanisms, but fewer studies have examined this possibility. We manipulated brood size in zebra finches to simultaneously examine the effects of developmental stress on male song learning and female behavioral and neural response to song. Although adult male HVC volume was unaffected, we found that males from larger broods imitated tutor song less accurately. In females, early condition did not affect the direction of song preference: all females preferred tutor song over unfamiliar song in an operant test. However, treatment did affect the magnitude of behavioral response to song: females from larger broods responded less during song preference trials. This difference in activity level did not reflect boldness per se, as a separate measure of this trait did not differ with brood size. Additionally, in females we found a treatment effect on expression of the immediate early gene ZENK in response to tutor song in brain regions involved in song perception (dNCM) and social motivation (LSc.vl, BSTm, TnA), but not in a region implicated in song memory (CMM). These results are consistent with the hypothesis that developmental stressors that impair song learning in male zebra finches also influence perceptual and/or motivational processes in females. However, our results suggest that the learning of tutor song by females is robust to disturbance by developmental stress. © 2018 Wiley Periodicals, Inc. Develop Neurobiol, 2018     

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.     

Preservation of musical memory in an amnesic professional cellist

Learning and memory of music involves a multitude of perceptual, motor, affective, and autobiographical memory processes [1]. Patient and imaging studies suggest that musical memory may involve distinct neural substrates [2,3]. However, the degree of independence of such a system from other memory domains is controversial [4]. We have investigated a 68-year-old professional cellist, patient PM, who developed severe amnesia following encephalitis. This case provided a unique opportunity to study musical memory in a patient with a precisely defined premorbid musical knowledge and well-demarcated focal lesions of the brain. Despite severe memory impairments, he performed like healthy musicians in various tests of recognition memory for music. These findings suggest that learning and retention of musical information depends on brain networks distinct from those involved in other types of episodic and semantic memory.     

Learning from inhibition: Functional roles of hippocampal CA1 inhibition in spatial learning and memory

Hippocampal inhibitory interneurons exert a powerful influence on learning and memory. Inhibitory interneurons are known to play a major role in many diseases that affect memory, and to strongly influence brain functions required for memory-related tasks. While previous studies involving genetic, optogenetic, and pharmacological manipulations have shown that hippocampal interneurons play essential roles in spatial and episodic learning and memory, exactly how interneurons affect local circuit computations during spatial navigation is not well understood. Given the significant anatomical, morphological, and functional heterogeneity in hippocampal interneurons, one may suspect cell-type specific roles in circuit computations. Here, we review emerging evidence of CA1 hippocampal interneurons’ role in local circuit computations that support spatial learning and memory and discuss open questions about CA1 interneurons in spatial learning.     

Increasing stereotypy in adult zebra finch song correlates with a declining rate of adult neurogenesis

Adult neurogenesis is often correlated with learning new tasks, suggesting that a function of incorporating new neurons is to permit new memory formation. However, in the zebra finch, neurons are added to the song motor pathway throughout life, long after the initial song motor pattern is acquired by about 3 months of age. To explore this paradox, we examined the relationship between adult song structure and neuron addition using sensitive measures of song acoustic structure. We report that between 4 and 15 months of age there was an increase in the stereotypy of fine-grained spectral and temporal features of syllable acoustic structure. These results indicate that the zebra finch continues to refine motor output, perhaps by practice, over a protracted period beyond the time when song is first learned. Over the same age range, there was a decrease in the addition of new neurons to HVC, a region necessary for song production, but not to Area X or the hippocampus, regions not essential for singing. We propose that age-related changes in the stereotypy of syllable acoustic structure and HVC neuron addition are functionally related.     

Social facilitation of male song by male and female conspecifics in the zebra finch, Taeniopygia guttata

Zebra finches are a ubiquitous model system for the study of vocal learning in animal communication. Their song has been well described, but its possible function(s) in social communication are only partly understood. The so-called ‘directed song’ is a high-intensity, high-performance song given during courtship in close proximity to the female, which is known to mediate mate choice and mating. However, this singing mode constitutes only a fraction of zebra finch males’ prolific song output. Potential communicative functions of their second, ‘undirected’ singing mode remain unresolved in the face of contradicting reports of both facilitating and inhibiting effects of social company on singing. We addressed this issue by experimentally manipulating social contexts in a within-subject design, comparing a solo versus male or female only company condition, each lasting for 24 h. Males’ total song output was significantly higher when a conspecific was in audible and visible distance than when they were alone. Male and female company had an equally facilitating effect on song output. Our findings thus indicate that singing motivation is facilitated rather than inhibited by social company, suggesting that singing in zebra finches might function both in inter- and intrasexual communication.     

The neurobiology of the human memory

Memory can be defined as the ability to acquire, process, store, and retrieve information. Memory is indispensable for learning, adaptation, and survival of every living organism. In humans, the remembering process has acquired great flexibility and complexity, reaching close links with other mental functions, such as thinking and emotions. Changes in synaptic connectivity and interactions among multiple neural networks provide the neurobiological substrates for memory encoding, retention, and consolidation. Memory may be categorized as short-term and long-term memory (according to the storage temporal duration), as implicit and explicit memory (with respect to the consciousness of remembering), as declarative (knowing that [fact]) and procedural (knowing how [skill]) memory, or as sensory (echoic, iconic and haptil), semantic, and episodic memory (according to the various remembering domains). Significant advances have been obtained in understanding memory neurobiology, but much remains to be learned in its cognitive, psychological, and phenomenological aspects.     

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     

The neurodynamic bases of imitating learning and episodic memory

In this review, three essentially important processes in the development of cognitive behavior are considered, viz., knowledge of a spatial environment by means of physical activity, coding, and the calling of the existential context of episodic memory and imitation learning based on the mirror neural mechanism. The data show that the parietal and frontal systems, which are involved in learning by imitation, allow a developing animal to obtain skills of management and motive synergies in perisomatic space, as well as to understand the intentions and the purposes of the observed actions of other individuals. At the same time the widely distributed parietal and frontal and entorhinal–hippocampal system mediates spatial knowledge and the solution of the navigation tasks that are important for the creation of the existential context of episodic memory.