Jon T. Sakata

Real-Time Contributions of Auditory Feedback to Avian Vocal Motor Control

Songbirds and humans both rely critically on hearing for learning and maintaining accurate vocalizations. Evidence strongly indicates that auditory feedback contributes in real time to human speech, but similar contributions of feedback to birdsong remain unclear. Here, we assessed real-time influences of auditory feedback on Bengalese finch song using a computerized system to detect targeted syllables as they were being sung and to disrupt feedback transiently at short and precisely controlled latencies. Altered feedback elicited changes within tens of milliseconds to both syllable sequencing and timing in ongoing song. These vocal disruptions were larger when feedback was altered at segments of song with variable sequence transitions than at stereotyped sequences. As in humans, these effects depended on the feedback delay relative to ongoing song, with the most disruptive delays approximating the average syllable duration. These results extend the parallels between speech and birdsong with respect to a moment-by-moment reliance on auditory feedback. Moreover, they demonstrate that song premotor circuitry is sensitive to auditory feedback during singing and suggest that feedback may contribute in real time to the control and calibration of song.

Online contributions of auditory feedback to neural activity in avian song control circuitry

Birdsong, like human speech, relies critically on auditory feedback to provide information about the quality of vocalizations. Although the importance of auditory feedback to vocal learning is well established, whether and how feedback signals influence vocal premotor circuitry has remained obscure. Previous studies in singing birds have not detected changes to vocal premotor activity after perturbations of auditory feedback, leading to the hypothesis that contributions of feedback to vocal plasticity might rely on“offline” processing. Here, we recorded single and multiunit activity in the premotor nucleus HVC (proper name) of singing Bengalese finches in response to feedback perturbations that are known to drive plastic changes in song. We found that transient feedback perturbation caused reliable decreases in HVC activity at short latencies (20–80 ms). Similar changes to HVC activity occurred in awake, nonsinging finches when the birds own song was played back with auditory perturbations that simulated those experienced by singing birds. These data indicate that neurons in avian vocal premotor circuitry are rapidly influenced by perturbations of auditory feedback and support the possibility that feedback information in HVC contributes “online” to the production and plasticity of vocalizations.

Integrating perspectives on vocal performance and consistency

SUMMARY Recent experiments in divergent fields of birdsong have revealed that vocal performance is important for reproductive success and under active control by distinct neural circuits. Vocal consistency, the degree to which the spectral properties (e.g. dominant or fundamental frequency) of song elements are produced consistently from rendition to rendition, has been highlighted as a biologically important aspect of vocal performance. Here, we synthesize functional, developmental and mechanistic (neurophysiological) perspectives to generate an integrated understanding of this facet of vocal performance. Behavioral studies in the field and laboratory have found that vocal consistency is affected by social context, season and development, and, moreover, positively correlated with reproductive success. Mechanistic investigations have revealed a contribution of forebrain and basal ganglia circuits and sex steroid hormones to the control of vocal consistency. Across behavioral, developmental and mechanistic studies, a convergent theme regarding the importance of vocal practice in juvenile and adult songbirds emerges, providing a basis for linking these levels of analysis. By understanding vocal consistency at these levels, we gain an appreciation for the various dimensions of song control and plasticity and argue that genes regulating the function of basal ganglia circuits and sex steroid hormones could be sculpted by sexual selection.

An Avian Basal Ganglia-Forebrain Circuit Contributes Differentially to Syllable Versus Sequence Variability of Adult Bengalese Finch Song

Behavioral variability is important for motor skill learning but continues to be present and actively regulated even in well-learned behaviors. In adult songbirds, two types of song variability can persist and are modulated by social context: variability in syllable structure and variability in syllable sequencing. The degree to which the control of both types of adult variability is shared or distinct remains unknown. The output of a basal ganglia-forebrain circuit, LMAN (the lateral magnocellular nucleus of the anterior nidopallium), has been implicated in song variability. For example, in adult zebra finches, neurons in LMAN actively control the variability of syllable structure. It is unclear, however, whether LMAN contributes to variability in adult syllable sequencing because sequence variability in adult zebra finch song is minimal. In contrast, Bengalese finches retain variability in both syllable structure and syllable sequencing into adulthood. We analyzed the effects of LMAN lesions on the variability of syllable structure and sequencing and on the social modulation of these forms of variability in adult Bengalese finches. We found that lesions of LMAN significantly reduced the variability of syllable structure but not of syllable sequencing. We also found that LMAN lesions eliminated the social modulation of the variability of syllable structure but did not detect significant effects on the modulation of sequence variability. These results show that LMAN contributes differentially to syllable versus sequence variability of adult song and suggest that these forms of variability are regulated by distinct neural pathways.

Mechanisms underlying the social enhancement of vocal learning in songbirds.

Significance Social interactions are fundamental to the acquisition of speech and language; therefore, it is critical to reveal mechanisms of social influences to understand general mechanisms of vocal learning. Like humans, songbirds learn their vocalizations during development. We demonstrate that social interactions rapidly enhance vocal learning, attention to song, and the activity of catecholamine-synthesizing neurons in juvenile zebra finches. We also reveal that adult finches alter the structure of their vocalizations when interacting with juveniles in ways that resemble how humans alter their speech when interacting with infants, and that could enhance learning. Our data suggest that social influences on attention, acoustic structure, and catecholaminergic activity represent evolutionarily important mechanisms mediating the social enhancement of vocal learning across humans and songbirds. Social processes profoundly influence speech and language acquisition. Despite the importance of social influences, little is known about how social interactions modulate vocal learning. Like humans, songbirds learn their vocalizations during development, and they provide an excellent opportunity to reveal mechanisms of social influences on vocal learning. Using yoked experimental designs, we demonstrate that social interactions with adult tutors for as little as 1 d significantly enhanced vocal learning. Social influences on attention to song seemed central to the social enhancement of learning because socially tutored birds were more attentive to the tutor’s songs than passively tutored birds, and because variation in attentiveness and in the social modulation of attention significantly predicted variation in vocal learning. Attention to song was influenced by both the nature and amount of tutor song: Pupils paid more attention to songs that tutors directed at them and to tutors that produced fewer songs. Tutors altered their song structure when directing songs at pupils in a manner that resembled how humans alter their vocalizations when speaking to infants, that was distinct from how tutors changed their songs when singing to females, and that could influence attention and learning. Furthermore, social interactions that rapidly enhanced learning increased the activity of noradrenergic and dopaminergic midbrain neurons. These data highlight striking parallels between humans and songbirds in the social modulation of vocal learning and suggest that social influences on attention and midbrain circuitry could represent shared mechanisms underlying the social modulation of vocal learning.

Catecholaminergic contributions to vocal communication signals

Social context affects behavioral displays across a variety of species. For example, social context acutely influences the acoustic and temporal structure of vocal communication signals such as speech and birdsong. Despite the prevalence and importance of such social influences, little is known about the neural mechanisms underlying the social modulation of communication. Catecholamines are implicated in the regulation of social behavior and motor control, but the degree to which catecholamines influence vocal communication signals remains largely unknown. Using a songbird, the Bengalese finch, we examined the extent to which the social context in which song is produced affected immediate early gene expression (EGR‐1) in catecholamine‐synthesising neurons in the midbrain. Further, we assessed the degree to which administration of amphetamine, which increases catecholamine concentrations in the brain, mimicked the effect of social context on vocal signals. We found that significantly more catecholaminergic neurons in the ventral tegmental area and substantia nigra (but not the central grey, locus coeruleus or subcoeruleus) expressed EGR‐1 in birds that were exposed to females and produced courtship song than in birds that produced non‐courtship song in isolation. Furthermore, we found that amphetamine administration mimicked the effects of social context and caused many aspects of non‐courtship song to resemble courtship song. Specifically, amphetamine increased the stereotypy of syllable structure and sequencing, the repetition of vocal elements and the degree of sequence completions. Taken together, these data highlight the conserved role of catecholamines in vocal communication across species, including songbirds and humans.

Forebrain circuits underlying the social modulation of vocal communication signals

Across vertebrate species, signalers alter the structure of their communication signals based on the social context. For example, male Bengalese finches produce faster and more stereotyped songs when directing song to females (female‐directed [FD] song) than when singing in isolation (undirected [UD] song), and such changes have been found to increase the attractiveness of a males song. Despite the importance of such social influences, little is known about the mechanisms underlying the social modulation of communication signals. To this end, we analyzed differences in immediate early gene (EGR‐1) expression when Bengalese finches produced FD or UD song. Relative to silent birds, EGR‐1 expression was elevated in birds producing either FD or UD song throughout vocal control circuitry, including the interface nucleus of the nidopallium (NIf), HVC, the robust nucleus of the arcopallium (RA), Area X, and the lateral magnocellular nucleus of the anterior nidopallium (LMAN). Moreover, EGR‐1 expression was higher in HVC, RA, Area X, and LMAN in males producing UD song than in males producing FD song, indicating that social context modulated EGR‐1 expression in these areas. However, EGR‐1 expression was not significantly different between males producing FD or UD song in NIf, the primary vocal motor input into HVC, suggesting that context‐dependent changes could arise de novo in HVC. The pattern of context‐dependent differences in EGR‐1 expression in the Bengalese finch was highly similar to that in the zebra finch and suggests that social context affects song structure by modulating activity throughout vocal control nuclei.

Relationship between the Sequencing and Timing of Vocal Motor Elements in Birdsong.

Accurate coordination of the sequencing and timing of motor gestures is important for the performance of complex and evolutionarily relevant behaviors. However, the degree to which motor sequencing and timing are related remains largely unknown. Birdsong is a communicative behavior that consists of discrete vocal motor elements (‘syllables’) that are sequenced and timed in a precise manner. To reveal the relationship between syllable sequencing and timing, we analyzed how variation in the probability of syllable transitions at branch points, nodes in song with variable sequencing across renditions, correlated with variation in the duration of silent gaps between syllable transitions (‘gap durations’) for adult Bengalese finch song. We observed a significant negative relationship between transition probability and gap duration: more prevalent transitions were produced with shorter gap durations. We then assessed the degree to which long-term age-dependent changes and acute context-dependent changes to syllable sequencing and timing followed this inverse relationship. Age- but not context-dependent changes to syllable sequencing and timing were inversely related. On average, gap durations at branch points decreased with age, and the magnitude of this decrease was greater for transitions that increased in prevalence than for transitions that decreased in prevalence. In contrast, there was no systematic relationship between acute context-dependent changes to syllable sequencing and timing. Gap durations at branch points decreased when birds produced female-directed courtship song compared to when they produced undirected song, and the magnitude of this decrease was not related to the direction and magnitude of changes to transition probabilities. These analyses suggest that neural mechanisms that regulate syllable sequencing could similarly control syllable timing but also highlight mechanisms that can independently regulate syllable sequencing and timing.

Advantages of Comparative Studies in Songbirds to Understand the Neural Basis of Sensorimotor Integration.

Sensorimotor integration is the process through which the nervous system creates a link between motor commands and associated sensory feedback. This process allows for the acquisition and refinement of many behaviors, including learned communication behaviors such as speech and birdsong. Consequently, it is important to understand fundamental mechanisms of sensorimotor integration, and comparative analyses of this process can provide vital insight. Songbirds offer a powerful comparative model system to study how the nervous system links motor and sensory information for learning and control. This is because the acquisition, maintenance, and control of birdsong critically depend on sensory feedback. Furthermore, there is an incredible diversity of song organizations across songbird species, ranging from songs with simple, stereotyped sequences to songs with complex sequencing of vocal gestures, as well as a wide diversity of song repertoire sizes. Despite this diversity, the neural circuitry for song learning, control, and maintenance remains highly similar across species. Here, we highlight the utility of songbirds for the analysis of sensorimotor integration and the insights about mechanisms of sensorimotor integration gained by comparing different songbird species. Key conclusions from this comparative analysis are that variation in song sequence complexity seems to covary with the strength of feedback signals in sensorimotor circuits and that sensorimotor circuits contain distinct representations of elements in the vocal repertoire, possibly enabling evolutionary variation in repertoire sizes. We conclude our review by highlighting important areas of research that could benefit from increased comparative focus, with particular emphasis on the integration of new technologies.

Social Memory Formation Rapidly and Differentially Affects the Motivation and Performance of Vocal Communication Signals in the Bengalese Finch (Lonchura striata var. domestica).

Cognitive processes like the formation of social memories can shape the nature of social interactions between conspecifics. Male songbirds use vocal signals during courtship interactions with females, but the degree to which social memory and familiarity influences the likelihood and structure of male courtship song remains largely unknown. Using a habituation-dishabituation paradigm, we found that a single, brief (<30 s) exposure to a female led to the formation of a short-term memory for that female: adult male Bengalese finches were significantly less likely to produce courtship song to an individual female when re-exposed to her 5 min later (i.e., habituation). Familiarity also rapidly decreased the duration of courtship songs but did not affect other measures of song performance (e.g., song tempo and the stereotypy of syllable structure and sequencing). Consistent with a contribution of social memory to the decrease in courtship song with repeated exposures to the same female, the likelihood that male Bengalese finches produced courtship song increased when they were exposed to a different female (i.e., dishabituation). Three consecutive exposures to individual females also led to the formation of a longer-term memory that persisted over days. Specifically, when courtship song production was assessed 2 days after initial exposures to females, males produced fewer and shorter courtship songs to familiar females than to unfamiliar females. Measures of song performance, however, were not different between courtship songs produced to familiar and unfamiliar females. The formation of a longer-term memory for individual females seemed to require at least three exposures because males did not differentially produce courtship song to unfamiliar females and females that they had been exposed to only once or twice. Taken together, these data indicate that brief exposures to individual females led to the rapid formation and persistence of social memories and support the existence of distinct mechanisms underlying the motivation to produce and the performance of courtship song.