Recursive Self-feedback Improved Speech Fluency in Two Patients with Chronic Nonfluent Aphasia.

Background: Previous studies have demonstrated that people with nonfluent aphasia (PWNA) improve their language production after repeating personalized scripts, modeled by speech-language pathologists (SLPs). If PWNA could improve by using their own self-feedback, relying less on external feedback, barriers to aphasia treatment, such as a dearth of clinicians and mobility issues, can be overcome. Here we examine whether PWNA improve their language production through an automated procedure that exposes them to playbacks of their own speech, which are updated recursively, without any feedback from SLPs. Method: We tested if recursive self-feedback could improve speech fluency in two persons with chronic nonfluent aphasia. We compared two treatments: script production with recursive self-feedback (a new technique) and a non-self-feedback training. We administered the treatments remotely to the participants through their smartphones using two versions of a mobile app we developed. Each participant engaged in each treatment for about three weeks. We estimated clinical improvements of script production through a quantitative trend analysis and nonoverlap of all pairs. Results: Recursive self-feedback improved speaking rate and speech initiation latency of trained and untrained scripts in both participants. The control (non-self-feedback) training was also effective, but it induced a somewhat weaker improvement in speaking rate, and improved speech initiation latency in only one participant. Conclusion: Our findings provide preliminary evidence that PWNA can improve their speaking rate and speech initiation latency during production of scripts via fully automated recursive self-feedback. The beneficial effects of recursive self-feedback training suggest that speech unison and repeated exposures to written scripts may be optional ingredients of script-based treatments for aphasia.

Learning the sound inventory of a complex vocal skill via an intrinsic reward.

Reinforcement learning (RL) is thought to underlie the acquisition of vocal skills like birdsong and speech, where sounding like one's "tutor" is rewarding. However, what RL strategy generates the rich sound inventories for song or speech? We find that the standard actor-critic model of birdsong learning fails to explain juvenile zebra finches' efficient learning of multiple syllables. However, when we replace a single actor with multiple independent actors that jointly maximize a common intrinsic reward, then birds' empirical learning trajectories are accurately reproduced. The influence of each actor (syllable) on the magnitude of global reward is competitively determined by its acoustic similarity to target syllables. This leads to each actor matching the target it is closest to and, occasionally, to the competitive exclusion of an actor from the learning process (i.e., the learned song). We propose that a competitive-cooperative multi-actor RL (MARL) algorithm is key for the efficient learning of the action inventory of a complex skill.

Incentivizing free riders improves collective intelligence in social dilemmas.

Collective intelligence challenges are often entangled with collective action problems. For example, voting, rating, and social innovation are collective intelligence tasks that require costly individual contributions. As a result, members of a group often free ride on the information contributed by intrinsically motivated people. Are intrinsically motivated agents the best participants in collective decisions? We embedded a collective intelligence task in a large-scale, virtual world public good game and found that participants who joined the information system but were reluctant to contribute to the public good (free riders) provided more accurate evaluations, whereas participants who rated frequently underperformed. Testing the underlying mechanism revealed that a negative rating bias in free riders is associated with higher accuracy. Importantly, incentivizing evaluations amplifies the relative influence of participants who tend to free ride without altering the (higher) quality of their evaluations, thereby improving collective intelligence. These results suggest that many of the currently available information systems, which strongly select for intrinsically motivated participants, underperform and that collective intelligence can benefit from incentivizing free riding members to engage. More generally, enhancing the diversity of contributor motivations can improve collective intelligence in settings that are entangled with collective action problems.

Balanced imitation sustains song culture in zebra finches.

Songbirds acquire songs by imitation, as humans do speech. Although imitation should drive convergence within a group and divergence through drift between groups, zebra finch songs sustain high diversity within a colony, but mild variation across colonies. We investigated this phenomenon by analyzing vocal learning statistics in 160 tutor-pupil pairs from a large breeding colony. Song imitation is persistently accurate in some families, but poor in others. This is not attributed to genetic differences, as fostered pupils copied their tutors' songs as accurately or poorly as biological pupils. Rather, pupils of tutors with low song diversity make more improvisations compared to pupils of tutors with high song diversity. We suggest that a frequency dependent balanced imitation prevents extinction of rare song elements and overabundance of common ones, promoting repertoire diversity within groups, while constraining drift across groups, which together prevents the collapse of vocal culture into either complete uniformity or chaos.

Categorical Rhythms Are Shared between Songbirds and Humans.

Rhythm is a prominent feature of music. Of the infinite possible ways of organizing events in time, musical rhythms are almost always distributed categorically. Such categories can facilitate the transmission of culture-a feature that songbirds and humans share. We compared rhythms of live performances of music to rhythms of wild thrush nightingale and domestic zebra finch songs. In nightingales, but not in zebra finches, we found universal rhythm categories, with patterns that were surprisingly similar to those of music. Isochronous 1:1 rhythms were similarly common. Interestingly, a bias toward small ratios (around 1:2 to 1:3), which is highly abundant in music, was observed also in thrush nightingale songs. Within that range, however, there was no statistically significant bias toward exact integer ratios (1:2 or 1:3) in the birds. High-ratio rhythms were abundant in the nightingale song and are structurally similar to fusion rhythms (ornaments) in music. In both species, preferred rhythms remained invariant over extended ranges of tempos, indicating natural categories. The number of rhythm categories decreased at higher tempos, with a threshold above which rhythm became highly stereotyped. In thrush nightingales, this threshold occurred at a tempo twice faster than in humans, indicating weaker structural constraints and a remarkable motor proficiency. Together, the results suggest that categorical rhythms reflect similar constraints on learning motor skills across species. The saliency of categorical rhythms across humans and thrush nightingales suggests that they promote, or emerge from, the cultural transmission of learned vocalizations. VIDEO ABSTRACT.

A Modular Approach to Vocal Learning: Disentangling the Diversity of a Complex Behavioral Trait.

Vocal learning is a behavioral trait in which the social and acoustic environment shapes the vocal repertoire of individuals. Over the past century, the study of vocal learning has progressed at the intersection of ecology, physiology, neuroscience, molecular biology, genomics, and evolution. Yet, despite the complexity of this trait, vocal learning is frequently described as a binary trait, with species being classified as either vocal learners or vocal non-learners. As a result, studies have largely focused on a handful of species for which strong evidence for vocal learning exists. Recent studies, however, suggest a continuum in vocal learning capacity across taxa. Here, we further suggest that vocal learning is a multi-component behavioral phenotype comprised of distinct yet interconnected modules. Discretizing the vocal learning phenotype into its constituent modules would facilitate integration of findings across a wider diversity of species, taking advantage of the ways in which each excels in a particular module, or in a specific combination of features. Such comparative studies can improve understanding of the mechanisms and evolutionary origins of vocal learning. We propose an initial set of vocal learning modules supported by behavioral and neurobiological data and highlight the need for diversifying the field in order to disentangle the complexity of the vocal learning phenotype.

Crowd wisdom enhanced by costly signaling in a virtual rating system.

Costly signaling theory was developed in both economics and biology and has been used to explain a wide range of phenomena. However, the theory's prediction that signal cost can enforce information quality in the design of new communication systems has never been put to an empirical test. Here we show that imposing time costs on reporting extreme scores can improve crowd wisdom in a previously cost-free rating system. We developed an online game where individuals interacted repeatedly with simulated services and rated them for satisfaction. We associated ratings with differential time costs by endowing the graphical user interface that solicited ratings from the users with "physics," including an initial (default) slider position and friction. When ratings were not associated with differential cost (all scores from 0 to 100 could be given by an equally low-cost click on the screen), scores correlated only weakly with objective service quality. However, introducing differential time costs, proportional to the deviation from the mean score, improved correlations between subjective rating scores and objective service performance and lowered the sample size required for obtaining reliable, averaged crowd estimates. Boosting time costs for reporting extreme scores further facilitated the detection of top performances. Thus, human collective online behavior, which is typically cost-free, can be made more informative by applying costly signaling via the virtual physics of rating devices.

Regularities in zebra finch song beyond the repeated motif.

The proliferation of birdsong research into the neural mechanisms of vocal learning is indebted to the remarkable stereotypy of the zebra finch's song motif. Motifs are composed of several syllables, which birds learn to produce in a fixed order. But at a higher level of organization-the bout-zebra finch song is no longer stereotyped. Song bouts include several repetitions of the motif, which are often linked by a variable number of short "connector" vocalizations. In this conceptual methods paper, we show that combinatorial analysis alone yields an incomplete description of this bout-level structure. In contrast, studying birdsong as a time-varying analog signal can reveal patterns of flexibility in the rhythmic organization of song bouts. Visualizing large song-samples in sorted raster plots shows that motifs are strung together via two distinct categories of connections: tight or loose. Loose connections allow considerable timing variation across renditions. Even among co-tutored birds that acquired similar motifs, we observe strong individual variability in rhythms and temporal plasticity of song bouts. These findings suggest that vocal flexibility could potentially allow individuals to express a variety of behavioral states through their songs, even in species that sing only a single stereotyped motif.

miR-9 regulates basal ganglia-dependent developmental vocal learning and adult vocal performance in songbirds.

miR-9 is an evolutionarily conserved miRNA that is abundantly expressed in Area X, a basal ganglia nucleus required for vocal learning in songbirds. Here, we report that overexpression of miR-9 in Area X of juvenile zebra finches impairs developmental vocal learning, resulting in a song with syllable omission, reduced similarity to the tutor song, and altered acoustic features. miR-9 overexpression in juveniles also leads to more variable song performance in adulthood, and abolishes social context-dependent modulation of song variability. We further show that these behavioral deficits are accompanied by downregulation of FoxP1 and FoxP2, genes that are known to be associated with language impairments, as well as by disruption of dopamine signaling and widespread changes in the expression of genes that are important in circuit development and functions. These findings demonstrate a vital role for miR-9 in basal ganglia function and vocal communication, suggesting that dysregulation of miR-9 in humans may contribute to language impairments and related neurodevelopmental disorders.

Animal Communication: Origins of Sequential Structure in Birdsong.

Culturally transmitted behaviors have an innate foundation, but the detailed sequential structure of such complex, acquired behaviors is often an outcome of historical accidents. New research has identified innate predispositions for structuring vocal sequences in culturally acquired birdsong.

Songbirds work around computational complexity by learning song vocabulary independently of sequence.

While acquiring motor skills, animals transform their plastic motor sequences to match desired targets. However, because both the structure and temporal position of individual gestures are adjustable, the number of possible motor transformations increases exponentially with sequence length. Identifying the optimal transformation towards a given target is therefore a computationally intractable problem. Here we show an evolutionary workaround for reducing the computational complexity of song learning in zebra finches. We prompt juveniles to modify syllable phonology and sequence in a learned song to match a newly introduced target song. Surprisingly, juveniles match each syllable to the most spectrally similar sound in the target, regardless of its temporal position, resulting in unnecessary sequence errors, that they later try to correct. Thus, zebra finches prioritize efficient learning of syllable vocabulary, at the cost of inefficient syntax learning. This strategy provides a non-optimal but computationally manageable solution to the task of vocal sequence learning.

Sexual dimorphism in striatal dopaminergic responses promotes monogamy in social songbirds.

In many songbird species, males sing to attract females and repel rivals. How can gregarious, non-territorial songbirds such as zebra finches, where females have access to numerous males, sustain monogamy? We found that the dopaminergic reward circuitry of zebra finches can simultaneously promote social cohesion and breeding boundaries. Surprisingly, in unmated males but not in females, striatal dopamine neurotransmission was elevated after hearing songs. Behaviorally too, unmated males but not females persistently exchanged mild punishments in return for songs. Song reinforcement diminished when dopamine receptors were blocked. In females, we observed song reinforcement exclusively to the mate's song, although their striatal dopamine neurotransmission was only slightly elevated. These findings suggest that song-triggered dopaminergic activation serves a dual function in social songbirds: as low-threshold social reinforcement in males and as ultra-selective sexual reinforcement in females. Co-evolution of sexually dimorphic reinforcement systems can explain the coexistence of gregariousness and monogamy.

How social learning adds up to a culture: from birdsong to human public opinion.

Distributed social learning may occur at many temporal and spatial scales, but it rarely adds up to a stable culture. Cultures vary in stability and diversity (polymorphism), ranging from chaotic or drifting cultures, through cumulative polymorphic cultures, to stable monolithic cultures with high conformity levels. What features can sustain polymorphism, preventing cultures from collapsing into either chaotic or highly conforming states? We investigate this question by integrating studies across two quite separate disciplines: the emergence of song cultures in birds, and the spread of public opinion and social conventions in humans. In songbirds, the learning process has been studied in great detail, while in human studies the structure of social networks has been experimentally manipulated on large scales. In both cases, the manner in which communication signals are compressed and filtered - either during learning or while traveling through the social network - can affect culture polymorphism and stability. We suggest a simple mechanism of a shifting balance between converging and diverging social forces to explain these effects. Understanding social forces that shape cultural evolution might be useful for designing agile communication systems, which are stable and polymorphic enough to promote gradual changes in institutional behavior.

Studying the Mechanisms of Developmental Vocal Learning and Adult Vocal Performance in Zebra Finches through Lentiviral Injection.

Here we provide a detailed step-by-step protocol for using lentivirus to manipulate miRNA expression in Area X of juvenile zebra finches and for analyzing the consequences on song learning and song performance. This protocol has four parts: 1) making the lentiviral construct to overexpress miRNA miR-9; 2) packaging the lentiviral vector; 3) stereotaxic injection of the lentivirus into Area X of juvenile zebra finches; 4) analysis of song learning and song performance in juvenile and adult zebra finches. These methods complement the methods employed in recent works that showed changing FoxP2 gene expression in Area X with lentivirus or adeno-associated virus leads to impairments in song behavior.

Statistical learning in songbirds: from self-tutoring to song culture.

At the onset of vocal development, both songbirds and humans produce variable vocal babbling with broadly distributed acoustic features. Over development, these vocalizations differentiate into the well-defined, categorical signals that characterize adult vocal behaviour. A broadly distributed signal is ideal for vocal exploration, that is, for matching vocal production to the statistics of the sensory input. The developmental transition to categorical signals is a gradual process during which the vocal output becomes differentiated and stable. But does it require categorical input? We trained juvenile zebra finches with playbacks of their own developing song, produced just a few moments earlier, updated continuously over development. Although the vocalizations of these self-tutored (ST) birds were initially broadly distributed, birds quickly developed categorical signals, as fast as birds that were trained with a categorical, adult song template. By contrast, siblings of those birds that received no training (isolates) developed phonological categories much more slowly and never reached the same level of category differentiation as their ST brothers. Therefore, instead of simply mirroring the statistical properties of their sensory input, songbirds actively transform it into distinct categories. We suggest that the early self-generation of phonological categories facilitates the establishment of vocal culture by making the song easier to transmit at the micro level, while promoting stability of shared vocabulary at the group level over generations.This article is part of the themed issue 'New frontiers for statistical learning in the cognitive sciences'.

Temporal regularity increases with repertoire complexity in the Australian pied butcherbird's song.

Music maintains a characteristic balance between repetition and novelty. Here, we report a similar balance in singing performances of free-living Australian pied butcherbirds. Their songs include many phrase types. The more phrase types in a bird's repertoire, the more diverse the singing performance can be. However, without sufficient temporal organization, avian listeners may find diverse singing performances difficult to perceive and memorize. We tested for a correlation between the complexity of song repertoire and the temporal regularity of singing performance. We found that different phrase types often share motifs (notes or stereotyped groups of notes). These shared motifs reappeared in strikingly regular temporal intervals across different phrase types, over hundreds of phrases produced without interruption by each bird. We developed a statistical estimate to quantify the degree to which phrase transition structure is optimized for maximizing the regularity of shared motifs. We found that transition probabilities between phrase types tend to maximize regularity in the repetition of shared motifs, but only in birds of high repertoire complexity. Conversely, in birds of low repertoire complexity, shared motifs were produced with less regularity. The strong correlation between repertoire complexity and motif regularity suggests that birds possess a mechanism that regulates the temporal placement of shared motifs in a manner that takes repertoire complexity into account. We discuss alternative musical, mechanistic and ecological explanations to this effect.

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.