Vocal Behavior In Songbirds Research Articles

The Role of the Basal Ganglia in the Development and Organization of Vocal Behavior in Songbirds

The Role of the Basal Ganglia in the Development and Organization of Vocal Behavior in Songbirds

Sex differences in seasonal brain plasticity and the neuroendocrine regulation of vocal behavior in songbirds

Birdsong is controlled in part by a discrete network of interconnected brain nuclei regulated in turn by steroid hormones and environmental stimuli. This complex interaction results in neural changes that occur seasonally as the environment varies (e.g., photoperiod, food/water availability, etc.). Variation in environment, vocal behavior, and neuroendocrine control has been primarily studied in male songbirds in both laboratory studies of captive birds and field studies of wild caught birds. The bias toward studying seasonality in the neuroendocrine regulation of song in male birds comes from a historic focus on sexually selected male behaviors. In fact, given that male song is often loud and accompanied by somewhat extravagant courtship behaviors, female song has long been overlooked. To compound this bias, the primary model songbird species for studies in the lab, zebra finches (Taeniopygia guttata) and canaries (Serinus canaria), exhibit little or no female song. Therefore, understanding the degree of variation and neuroendocrine control of seasonality in female songbirds is a major gap in our knowledge. In this review, we discuss the importance of studying sex differences in seasonal plasticity and the song control system. Specifically, we discuss sex differences in 1) the neuroanatomy of the song control system, 2) the distribution of receptors for androgens and estrogens and 3) the seasonal neuroplasticity of the hypothalamo-pituitary-gonadal axis as well as in the neural and cellular mechanisms mediating song system changes. We also discuss how these neuroendocrine mechanisms drive sex differences in seasonal behavior. Finally, we highlight specific gaps in our knowledge and suggest experiments critical for filling these gaps.

Local field potentials in a pre-motor region predict learned vocal sequences.

Neuronal activity within the premotor region HVC is tightly synchronized to, and crucial for, the articulate production of learned song in birds. Characterizations of this neural activity detail patterns of sequential bursting in small, carefully identified subsets of neurons in the HVC population. The dynamics of HVC are well described by these characterizations, but have not been verified beyond this scale of measurement. There is a rich history of using local field potentials (LFP) to extract information about behavior that extends beyond the contribution of individual cells. These signals have the advantage of being stable over longer periods of time, and they have been used to study and decode human speech and other complex motor behaviors. Here we characterize LFP signals presumptively from the HVC of freely behaving male zebra finches during song production to determine if population activity may yield similar insights into the mechanisms underlying complex motor-vocal behavior. Following an initial observation that structured changes in the LFP were distinct to all vocalizations during song, we show that it is possible to extract time-varying features from multiple frequency bands to decode the identity of specific vocalization elements (syllables) and to predict their temporal onsets within the motif. This demonstrates the utility of LFP for studying vocal behavior in songbirds. Surprisingly, the time frequency structure of HVC LFP is qualitatively similar to well-established oscillations found in both human and non-human mammalian motor areas. This physiological similarity, despite distinct anatomical structures, may give insight into common computational principles for learning and/or generating complex motor-vocal behaviors.

The Effects of Pitch Shifts on Delay-Induced Changes in Vocal Sequencing in a Songbird.

Like human speech, vocal behavior in songbirds depends critically on auditory feedback. In both humans and songbirds, vocal skills are acquired by a process of imitation whereby current vocal production is compared to an acoustic target. Similarly, performance in adulthood relies strongly on auditory feedback, and online manipulations of auditory signals can dramatically alter acoustic production even after vocalizations have been well learned. Artificially delaying auditory feedback can disrupt both speech and birdsong, and internal delays in auditory feedback have been hypothesized as a cause of vocal dysfluency in persons who stutter. Furthermore, in both song and speech, online shifts of the pitch (fundamental frequency) of auditory feedback lead to compensatory changes in vocal pitch for small perturbations, but larger pitch shifts produce smaller changes in vocal output. Intriguingly, large pitch shifts can partially restore normal speech in some dysfluent speakers, suggesting that the effects of auditory feedback delays might be ameliorated by online pitch manipulations. Although birdsong provides a promising model system for understanding speech production, the interactions between sensory feedback delays and pitch shifts have not yet been assessed in songbirds. To investigate this, we asked whether the addition of a pitch shift modulates delay-induced changes in Bengalese finch song, hypothesizing that pitch shifts would reduce the effects of feedback delays. Compared with the effects of delays alone, combined delays and pitch shifts resulted in a significant reduction in behavioral changes in one type of sequencing (branch points) but not another (distribution of repeated syllables).

The acoustic effect of vocal tract adjustments in zebra finches

Vocal production in songbirds requires the control of the respiratory system, the syrinx as sound source and the vocal tract as acoustic filter. Vocal tract movements consist of beak, tongue and hyoid movements, which change the volume of the oropharyngeal-esophageal cavity (OEC), glottal movements and tracheal length changes. The respective contributions of each movement to filter properties are not completely understood, but the effects of this filtering are thought to be very important for acoustic communication in birds. One of the most striking movements of the upper vocal tract during vocal behavior in songbirds involves the OEC. This study measured the acoustic effect of OEC adjustments in zebra finches by comparing resonance acoustics between an utterance with OEC expansion (calls) and a similar utterance without OEC expansion (respiratory sounds induced by a bilateral syringeal denervation). X-ray cineradiography confirmed the presence of an OEC motor pattern during song and call production, and a custom-built Hall-effect collar system confirmed that OEC expansion movements were not present during respiratory sounds. The spectral emphasis during zebra finch call production ranging between 2.5 and 5 kHz was not present during respiratory sounds, indicating strongly that it can be attributed to the OEC expansion.

The Song Must Go On: Resilience of the Songbird Vocal Motor Pathway

Stereotyped sequences of neural activity underlie learned vocal behavior in songbirds; principle neurons in the cortical motor nucleus HVC fire in stereotyped sequences with millisecond precision across multiple renditions of a song. The geometry of neural connections underlying these sequences is not known in detail though feed-forward chains are commonly assumed in theoretical models of sequential neural activity. In songbirds, a well-defined cortical-thalamic motor circuit exists but little is known the fine-grain structure of connections within each song nucleus. To examine whether the structure of song is critically dependent on long-range connections within HVC, we bilaterally transected the nucleus along the anterior-posterior axis in normal-hearing and deafened birds. The disruption leads to a slowing of song as well as an increase in acoustic variability. These effects are reversed on a time-scale of days even in deafened birds or in birds that are prevented from singing post-transection. The stereotyped song of zebra finches includes acoustic details that span from milliseconds to seconds–one of the most precise learned behaviors in the animal kingdom. This detailed motor pattern is resilient to disruption of connections at the cortical level, and the details of song variability and duration are maintained by offline homeostasis of the song circuit.

A sensorimotor area (NIf) is required for the production of learned vocalizations

AbstractSensory feedback is essential for the acquisition of complex motor behaviors, including birdsong. In zebra finches, auditory feedback is relayed to the descending motor pathway primarily through the nucleus interfacialis nidopalii (NIf). NIf projects to HVC - a premotor region essential for song, which projects to RA, a motor cortex analogue brain area that drives muscle activity required for vocalizations. NIf is also essential for ‘sleep replay’, a recapitulation of song-related neural dynamics in the motor pathway during sleep. Despite being one of the major inputs to the song control pathway, there is no known role for NIf in the production of zebra finch song. To address this, we reversibly inactivated NIf using TTX or Muscimol in 13 birds. We compared songs before and during inactivation and found large effects of NIf inactivation on song structure. Vocalizations after NIf inactivation resembled subsong, highly variable utterances typical of the very early phases of song learning. Subsong is driven by LMAN, the output nucleus of an avian basal ganglia circuit that projects to RA. To verify that NIf inactivations indeed switched song control from HVC to LMAN, we inactivated LMAN in conjunction with NIf in four birds. As with LMAN inactivations after HVC lesions, this manipulation led to a complete cessation of singing. We also lesioned NIf using ibotenic acid and saw the song recover within a day, consistent with previous studies. Our results show that NIf input to HVC is acutely necessary for generating learned vocal behavior in songbirds, and that in its absence vocal production reverts to subsong driven by LMAN. Absent NIf input, the song circuit reorganizes and recovers its ability to produce pre-lesion song over the course of 1-2 days, suggesting a redundant role for NIf that can be assumed by other parts of the song circuit.

Motor‐induced transcription but sensory‐regulated translation of ZENK in socially interactive songbirds

The ZENK gene, depending upon singing activity, is transcribed within all the telencephalic nuclei controlling vocal behavior in songbirds. We show here that singing by deafened or completely isolated adult zebra finches induced high levels of ZENK transcription. This mRNA however, was not translated into high levels of ZENK protein. Instead, high levels of singing-driven ZENK protein translation were found in socially interactive birds. This dissociation between ZENK mRNA and ZENK protein was regionally specific to the robust nucleus of the arcopallium (RA), a region that is well known for its control of vocal-motor behavior in birds. Our results suggest cooperation between motor and sensory processes for regulating mRNA induction and subsequent protein synthesis in socially active songbirds.

Presynaptic Depression of Glutamatergic Synaptic Transmission by D1-Like Dopamine Receptor Activation in the Avian Basal Ganglia

Vocal behavior in songbirds exemplifies a rich integration of motor, cognitive, and social functions that are shared among vertebrates. As a part of the underlying neural substrate, the song system, the anterior forebrain pathway (AFP) is required for song learning and maintenance. The AFP resembles the mammalian basal ganglia-thalamocortical loop in its macroscopic organization, neuronal intrinsic properties, and microcircuitry. Area X, the first station in the AFP, is a part of the basal ganglia essential for vocal learning. It receives glutamatergic inputs from pallial structures and sends GABAergic outputs to thalamic structures. It also receives dense dopaminergic innervation from the midbrain. The role of this innervation is essentially unknown. Here we provide evidence that dopamine (DA) can modulate the glutamatergic inputs to spiny neurons in area X. In whole-cell voltage-clamp recordings from neurons in brain slices of adult zebra finches, we found that activation of D1-like DA receptors depresses ionotropic glutamatergic synaptic current in area X spiny neurons. This effect is mediated by a presynaptic site of action, mimicked by activation of adenylyl cyclase, and blocked by protein kinase A inhibitor and an adenosine A1 receptor antagonist. These results suggest that, in addition to altering the input-output function of spiny neurons by modulating their excitability, as we have shown previously, DA can directly influence the excitatory inputs to these neurons as well. Thus, DA can exert fine control over information processing through spiny neurons in area X, the dynamics of the AFP output, and ultimately song learning and maintenance.

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.

Axonal connections of the medial magnocellular nucleus of the anterior neostriatum in zebra finches.

The medial magnocellular nucleus of the anterior neostriatum (mMAN) is a small cortical nucleus which was previously identified as a component of the neural circuitry controlling vocal behavior in songbirds based on its efferent connection to the High Vocal Center (HVC), a major song control nucleus (Nottebohm et al. [1982] J. Comp. Neurol. 207:344-357; Bottjer et al. [1989] J. Comp. Neurol. 279:312-326). We have conducted tract tracing experiments (using wheat-germ agglutinin-horseradish peroxidase (WGA-HRP), the carbocyanine dye DiI, and biocytin) to determine the complete pattern of afferent and efferent connections of mMAN in adult male zebra finches. We confirmed the existence of an efferent projection from mMAN to HVC and discovered a novel projection to the region medial to caudal HVC called paraHVC (pHVC). Injections of retrograde tracers into mMAN showed that afferent input to mMAN originates from the dorsomedial nucleus of the posterior thalamus (DMP). Injections of DiI into DMP produced anterograde label over mMAN, thus confirming the DMP-to-mMAN projection. Interestingly, this anterograde label extended beyond the region of mMAN defined by HVC-projecting neurons into the immediately surrounding cortex. This extended terminal field of DMP efferents indicates that mMAN encompasses a core population of projection neurons surrounded by a shell of non-HVC-projecting neurons, both of which receive input from the dorsal thalamus. Analysis of retrograde DiI label resulting from DMP injections revealed two major sources of afferent input to DMP originating in regions of the archistriatum and hypothalamus. Inputs to DMP were distributed throughout the dorsal archistriatum and included the area that receives a projection from the parvicellular shell region of the lateral magnocellular nucleus of the anterior neostriatum, a song control nucleus, as well as the dorsal portion of the robust nucleus of the archistriatum, the motor-cortical output of the song control system. The projections from song control regions of the archistriatum to DMP may feed information back into telencephalic song control circuitry via the DMP-->mMAN-->HVC/pHVC pathway. The other source of afferent input to DMP is located in the external cellular stratum of the lateral hypothalamus (SCE). This newly delineated SCE-->DMP-->mMAN-->HVC/pHVC pathway is the first report of a hypothalamic brain region neuroanatomically integrated with song control circuitry. Because hypothalamic brain regions are important for homeostasis and regulating behavior, the trans-synaptic circuitry of mMAN may help to integrate information about the bird's internal state, such as sexual maturation, with song learning and production.

Developmental plasticity in neural circuits for a learned behavior.

The neural substrate underlying learned vocal behavior in songbirds provides a textbook illustration of anatomical localization of function for a complex learned behavior in vertebrates. The song-control system has become an important model for studying neural systems related to learning, behavior, and development. The song system of zebra finches is characterized by a heightened capacity for both neural and behavioral change during development and has taught us valuable information regarding sensitive periods, rearrangement of synaptic connections, topographic specificity, cell death and neurogenesis, experience-dependent neural plasticity, and sexual differentiation. The song system differs in some interesting ways from some well-studied mammalian model systems and thus offers fresh perspectives on specific theoretical issues. In this highly selective review, we concentrate on two major questions: What are the developmental changes in the song system responsible for song learning and the restriction of learning to a sensitive period, and what factors explain the highly sexually dimorphic development of this system? We discuss the important role of sex steroid hormones and of neurotrophins in creating a male-typical neural song circuit (which can learn to produce complex vocalizations) instead of a reduced, female-typical song circuit that does not produce learned song.

Induced cell death in a thalamic nucleus during a restricted period of zebra finch vocal development

A discrete network of forebrain nuclei underlies vocal learning and production in male zebra finches. Three nuclei within this network form a neural pathway that is particularly important for vocal learning in juveniles: area X of the avian striatum projects to the medial dorsolateral nucleus of the anterior thalamus (DLM), which in turn projects to the lateral magnocellular nucleus of the anterior neostriatum (IMAN). Lesions of any of these nuclei in juvenile birds disrupt normal vocal development, whereas the same lesions in adult birds have no effect on already-learned song. Because numerous studies have shown that neuronal survival in the developing nervous system depends on access to efferent targets, we have investigated the possibility that the survival of DLM neurons is similarly regulated over the course of vocal learning. Thus, the efferent target of DLM (IMAN) was lesioned electrolytically in male birds at various stages of vocal development (20, 40, 60 d of age and adult) and birds were killed either 2, 4, or 6 d postlesion. Electrolytic lesions of IMAN removed the single identified efferent target of DLM projection neurons and axotomized the terminal arborizations of these neurons. Although DLM does not normally lose neurons during vocal development, IMAN lesions in 20-d-old birds yielded numerous pyknotic cells throughout DLM by 4 d postlesion and a two-thirds reduction in DLM neuron density by 6 d postlesion. In contrast, IMAN lesions in adult birds had little or no effect on neuronal survival in DLM. Analysis of 40-d-old birds revealed significant but less substantial cell loss than in 20-d-old birds, whereas 60-d-old birds were not different from adults. The age-related decline in the vulnerability of DLM cells to IMAN lesion-induced death suggests that factors that regulate DLM neuron survival may also be involved in the acquisition of learned vocal behavior in songbirds.

Interspecific comparisons of the size of neural song control regions and song complexity in duetting birds: evolutionary implications

Previous studies have demonstrated a correlation between song repertoire size and volume of song control regions (SCRs) in the brains of songbirds. In the present study we demonstrate that 2 congeneric species of tropical duetting wrens, the rufous-and-white wren (Thryothorus rufalbus) and the bay wren (T. nigricapillus), share the same relationship between SCR volume and vocal complexity. In each species, females sing in elaborate duets with males. Males of these species have similar song repertoire sizes; there is no significant difference between heterospecific males in the volumes of SCRs. Female rufous-and-white wrens have less than half as large a song repertoire as female bay wrens, and all of their SCRs measured are significantly smaller than those of bay wren females. This interspecific equivalence of the relationship between SCR volume and repertoire size suggests that the neural system regulating vocal behavior in songbirds is evolutionarily conservative in the manner in which it encodes song complexity.