A neuroethological view of the multifaceted sensory influences on birdsong.

Learning and execution of complex motor skills are often modulated by sensory feedback and contextual cues arriving across multiple sensory modalities. Vocal motor behaviors, in particular, are primarily influenced by auditory inputs, both during learning and mature vocal production. The importance of auditory input in shaping vocal output has been investigated in several songbird species that acquire their adult song based on auditory exposure to a tutor during development. Recent studies have highlighted the influences of stimuli arriving through other sensory channels in juvenile song learning and in adult song production. Here, we review changes induced by diverse sensory stimuli during the song learning process and the production of adult song, considering the neuroethological significance of sensory channels in different species of songbirds. Additionally, we highlight advances, open questions, and possible future approaches for understanding the neural circuits that enable the multimodal shaping of singing behavior.

Wild nightingales flexibly match whistle pitch in real time.

Interactive vocal communication, similar to a human conversation, requires flexible and real-time changes to vocal output in relation to preceding auditory stimuli. These vocal adjustments are essential to ensuring both the suitable timing and content of the interaction. Precise timing of dyadic vocal exchanges has been investigated in a variety of species, including humans. In contrast, the ability of non-human animals to accurately adjust specific spectral features of vocalization extemporaneously in response to incoming auditory information is less well studied. One spectral feature of acoustic signals is the fundamental frequency, which we perceive as pitch. Many animal species can discriminate between sound frequencies, but real-time detection and reproduction of an arbitrary pitch have only been observed in humans. Here, we show that nightingales in the wild can match the pitch of whistle songs while singing in response to conspecifics or pitch-controlled whistle playbacks. Nightingales matched whistles across their entire pitch production range indicating that they can flexibly tune their vocal output along a wide continuum. Prompt whistle pitch matches were more precise than delayed ones, suggesting the direct mapping of auditory information onto a motor command to achieve online vocal replication of a heard pitch. Although nightingales' songs follow annual cycles of crystallization and deterioration depending on breeding status, the observed pitch-matching behavior is present year-round, suggesting a stable neural circuit independent of seasonal changes in physiology. Our findings represent the first case of non-human instantaneous vocal imitation of pitch, highlighting a promising model for understanding sensorimotor transformation within an interactive context. VIDEO ABSTRACT.

High-density electrode recordings reveal strong and specific connections between retinal ganglion cells and midbrain neurons.

The superior colliculus is a midbrain structure that plays important roles in visually guided behaviors in mammals. Neurons in the superior colliculus receive inputs from retinal ganglion cells but how these inputs are integrated in vivo is unknown. Here, we discovered that high-density electrodes simultaneously capture the activity of retinal axons and their postsynaptic target neurons in the superior colliculus, in vivo. We show that retinal ganglion cell axons in the mouse provide a single cell precise representation of the retina as input to superior colliculus. This isomorphic mapping builds the scaffold for precise retinotopic wiring and functionally specific connection strength. Our methods are broadly applicable, which we demonstrate by recording retinal inputs in the optic tectum in zebra finches. We find common wiring rules in mice and zebra finches that provide a precise representation of the visual world encoded in retinal ganglion cells connections to neurons in retinorecipient areas.

A feedforward inhibitory premotor circuit for auditory-vocal interactions in zebra finches.

During vocal exchanges, hearing specific auditory signals can provoke vocal responses or suppress vocalizations to avoid interference. These abilities result in the widespread phenomenon of vocal turn taking, yet little is known about the neural circuitry that regulates the input-dependent timing of vocal replies. Previous work in vocally interacting zebra finches has highlighted the importance of premotor inhibition for precisely timed vocal output. By developing physiologically constrained mathematical models, we derived circuit mechanisms based on feedforward inhibition that enable both the temporal modulation of vocal premotor drive as well as auditory suppression of vocalization during listening. Extracellular recordings in HVC during the listening phase confirmed the presence of auditory-evoked response patterns in putative inhibitory interneurons, along with corresponding signatures of auditory-evoked activity suppression. Further, intracellular recordings of identified neurons projecting to HVC from the upstream sensorimotor nucleus, nucleus interfacialis (NIf), shed light on the timing of auditory inputs to this network. The analysis of incrementally time-lagged interactions between auditory and premotor activity in the model resulted in the prediction of a window of auditory suppression, which could be, in turn, verified in behavioral data. A phasic feedforward inhibition model consistently explained the experimental results. This mechanism highlights a parsimonious and generalizable principle for how different driving inputs (vocal and auditory related) can be integrated in a single sensorimotor circuit to regulate two opposing vocal behavioral outcomes: the controlled timing of vocal output or the suppression of overlapping vocalizations.

Inhibition within a premotor circuit controls the timing of vocal turn-taking in zebra finches.

Vocal turn-taking is a fundamental organizing principle of human conversation but the neural circuit mechanisms that structure coordinated vocal interactions are unknown. The ability to exchange vocalizations in an alternating fashion is also exhibited by other species, including zebra finches. With a combination of behavioral testing, electrophysiological recordings, and pharmacological manipulations we demonstrate that activity within a cortical premotor nucleus orchestrates the timing of calls in socially interacting zebra finches. Within this circuit, local inhibition precedes premotor neuron activation associated with calling. Blocking inhibition results in faster vocal responses as well as an impaired ability to flexibly avoid overlapping with a partner. These results support a working model in which premotor inhibition regulates context-dependent timing of vocalizations and enables the precise interleaving of vocal signals during turn-taking.

Finding the Beat: From Socially Coordinated Vocalizations in Songbirds to Rhythmic Entrainment in Humans.

Humans and oscine songbirds share the rare capacity for vocal learning. Songbirds have the ability to acquire songs and calls of various rhythms through imitation. In several species, birds can even coordinate the timing of their vocalizations with other individuals in duets that are synchronized with millisecond-accuracy. It is not known, however, if songbirds can perceive rhythms holistically nor if they are capable of spontaneous entrainment to complex rhythms, in a manner similar to humans. Here we review emerging evidence from studies of rhythm generation and vocal coordination across songbirds and humans. In particular, recently developed experimental methods have revealed neural mechanisms underlying the temporal structure of song and have allowed us to test birds' abilities to predict the timing of rhythmic social signals. Surprisingly, zebra finches can readily learn to anticipate the calls of a "vocal robot" partner and alter the timing of their answers to avoid jamming, even in reference to complex rhythmic patterns. This capacity resembles, to some extent, human predictive motor response to an external beat. In songbirds, this is driven, at least in part, by the forebrain song system, which controls song timing and is essential for vocal learning. Building upon previous evidence for spontaneous entrainment in human and non-human vocal learners, we propose a comparative framework for future studies aimed at identifying shared mechanism of rhythm production and perception across songbirds and humans.

The Forebrain Song System Mediates Predictive Call Timing in Female and Male Zebra Finches.

The dichotomy between vocal learners and non-learners is a fundamental distinction in the study of animal communication. Male zebra finches (Taeniopygia guttata) are vocal learners that acquire a song resembling their tutors', whereas females can only produce innate calls. The acoustic structure of short calls, produced by both males and females, is not learned. However, these calls can be precisely coordinated across individuals. To examine how birds learn to synchronize their calls, we developed a vocal robot that exchanges calls with a partner bird. Because birds answer the robot with stereotyped latencies, we could program it to disrupt each bird's responses by producing calls that are likely to coincide with the bird's. Within minutes, the birds learned to avoid this disruptive masking (jamming) by adjusting the timing of their responses. Notably, females exhibited greater adaptive timing plasticity than males. Further, when challenged with complex rhythms containing jamming elements, birds dynamically adjusted the timing of their calls in anticipation of jamming. Blocking the song system cortical output dramatically reduced the precision of birds' response timing and abolished their ability to avoid jamming. Surprisingly, we observed this effect in both males and females, indicating that the female song system is functional rather than vestigial. We suggest that descending forebrain projections, including the song-production pathway, function as a general-purpose sensorimotor communication system. In the case of calls, it enables plasticity in vocal timing to facilitate social interactions, whereas in the case of songs, plasticity extends to developmental changes in vocal structure.

The hidden effect of hearing acuity on speech recall, and compensatory effects of self-paced listening.

OBJECTIVE: The purpose of this research was to determine whether negative effects of hearing loss on recall accuracy for spoken narratives can be mitigated by allowing listeners to control the rate of speech input. DESIGN: Paragraph-length narratives were presented for recall under two listening conditions in a within-participants design: presentation without interruption (continuous) at an average speech-rate of 150 words per minute; and presentation interrupted at periodic intervals at which participants were allowed to pause before initiating the next segment (self-paced). STUDY SAMPLE: Participants were 24 adults ranging from 21 to 33 years of age. Half had age-normal hearing acuity and half had mild- to-moderate hearing loss. The two groups were comparable for age, years of formal education, and vocabulary. RESULTS: When narrative passages were presented continuously, without interruption, participants with hearing loss recalled significantly fewer story elements, both main ideas and narrative details, than those with age-normal hearing. The recall difference was eliminated when the two groups were allowed to self-pace the speech input. CONCLUSION: Results support the hypothesis that the listening effort associated with reduced hearing acuity can slow processing operations and increase demands on working memory, with consequent negative effects on accuracy of narrative recall.