Auditory discrimination learning and acoustic cue weighing in female zebra finches with localized FoxP1 knockdowns.

Rare disruptions of the transcription factor FOXP1 are implicated in a human neurodevelopmental disorder characterized by autism and/or intellectual disability with prominent problems in speech and language abilities. Avian orthologues of this transcription factor are evolutionarily conserved and highly expressed in specific regions of songbird brains, including areas associated with vocal production learning and auditory perception. Here, we investigated possible contributions of FoxP1 to song discrimination and auditory perception in juvenile and adult female zebra finches. They received lentiviral knockdowns of FoxP1 in one of two brain areas involved in auditory stimulus processing, HVC (proper name) or CMM (caudomedial mesopallium). Ninety-six females, distributed over different experimental and control groups were trained to discriminate between two stimulus songs in an operant Go/Nogo paradigm and subsequently tested with an array of stimuli. This made it possible to assess how well they recognized and categorized altered versions of training stimuli and whether localized FoxP1 knockdowns affected the role of different features during discrimination and categorization of song. Although FoxP1 expression was significantly reduced by the knockdowns, neither discrimination of the stimulus songs nor categorization of songs modified in pitch, sequential order of syllables or by reversed playback were affected. Subsequently, we analyzed the full dataset to assess the impact of the different stimulus manipulations for cue weighing in song discrimination. Our findings show that zebra finches rely on multiple parameters for song discrimination, but with relatively more prominent roles for spectral parameters and syllable sequencing as cues for song discrimination.NEW & NOTEWORTHY In humans, mutations of the transcription factor FoxP1 are implicated in speech and language problems. In songbirds, FoxP1 has been linked to male song learning and female preference strength. We found that FoxP1 knockdowns in female HVC and caudomedial mesopallium (CMM) did not alter song discrimination or categorization based on spectral and temporal information. However, this large dataset allowed to validate different cue weights for spectral over temporal information for song recognition.

Zebra finches (Taeniopygia guttata) demonstrate cognitive flexibility in using phonology and sequence of syllables in auditory discrimination.

Zebra finches rely mainly on syllable phonology rather than on syllable sequence when they discriminate between two songs. However, they can also learn to discriminate two strings containing the same set of syllables by their sequence. How learning about the phonological characteristics of syllables and their sequence relate to each other and to the composition of the stimuli is still an open question. We compared whether and how the zebra finches' relative sensitivity for syllable phonology and syllable sequence depends on the differences between syllable strings. Two groups of zebra finches were trained in a Go-Left/Go-Right task to discriminate either between two strings in which each string contained a unique set of song syllables ('Different-syllables group') or two strings in which both strings contained the same set of syllables, but in a different sequential order ('Same-syllables group'). We assessed to what extent the birds in the two experimental groups attend to the spectral characteristics and the sequence of the syllables by measuring the responses to test strings consisting of spectral modifications or sequence changes. Our results showed no difference in the number of trials needed to discriminate strings consisting of either different or identical sets of syllables. Both experimental groups attended to changes in spectral features in a similar way, but the group for which both training strings consisted of the same set of syllables responded more strongly to changes in sequence than the group for which the training strings consisted of different sets of syllables. This outcome suggests the presence of an additional learning process to learn about syllable sequence when learning about syllable phonology is not sufficient to discriminate two strings. Our study thus demonstrates that the relative importance of syllable phonology and sequence depends on how these features vary among stimuli. This indicates cognitive flexibility in the acoustic features that songbirds might use in their song recognition.

Effects of Cortical FoxP1 Knockdowns on Learned Song Preference in Female Zebra Finches.

The search for molecular underpinnings of human vocal communication has focused on genes encoding forkhead-box transcription factors, as rare disruptions of FOXP1, FOXP2, and FOXP4 have been linked to disorders involving speech and language deficits. In male songbirds, an animal model for vocal learning, experimentally altered expression levels of these transcription factors impair song production learning. The relative contributions of auditory processing, motor function or auditory-motor integration to the deficits observed after different FoxP manipulations in songbirds are unknown. To examine the potential effects on auditory learning and development, we focused on female zebra finches (Taeniopygia guttata) that do not sing but develop song memories, which can be assayed in operant preference tests. We tested whether the relatively high levels of FoxP1 expression in forebrain areas implicated in female song preference learning are crucial for the development and/or maintenance of this behavior. Juvenile and adult female zebra finches received FoxP1 knockdowns targeted to HVC (proper name) or to the caudomedial mesopallium (CMM). Irrespective of target site and whether the knockdown took place before (juveniles) or after (adults) the sensitive phase for song memorization, all groups preferred their tutor's song. However, adult females with FoxP1 knockdowns targeted at HVC showed weaker motivation to hear song and weaker song preferences than sham-treated controls, while no such differences were observed after knockdowns in CMM or in juveniles. In summary, FoxP1 knockdowns in the cortical song nucleus HVC were not associated with impaired tutor song memory but reduced motivation to actively request tutor songs.

The multi-dimensional nature of vocal learning.

How learning affects vocalizations is a key question in the study of animal communication and human language. Parallel efforts in birds and humans have taught us much about how vocal learning works on a behavioural and neurobiological level. Subsequent efforts have revealed a variety of cases among mammals in which experience also has a major influence on vocal repertoires. Janik and Slater (Anim. Behav.60, 1-11. (doi:10.1006/anbe.2000.1410)) introduced the distinction between vocal usage and production learning, providing a general framework to categorize how different types of learning influence vocalizations. This idea was built on by Petkov and Jarvis (Front. Evol. Neurosci.4, 12. (doi:10.3389/fnevo.2012.00012)) to emphasize a more continuous distribution between limited and more complex vocal production learners. Yet, with more studies providing empirical data, the limits of the initial frameworks become apparent. We build on these frameworks to refine the categorization of vocal learning in light of advances made since their publication and widespread agreement that vocal learning is not a binary trait. We propose a novel classification system, based on the definitions by Janik and Slater, that deconstructs vocal learning into key dimensions to aid in understanding the mechanisms involved in this complex behaviour. We consider how vocalizations can change without learning, and a usage learning framework that considers context specificity and timing. We identify dimensions of vocal production learning, including the copying of auditory models (convergence/divergence on model sounds, accuracy of copying), the degree of change (type and breadth of learning) and timing (when learning takes place, the length of time it takes and how long it is retained). We consider grey areas of classification and current mechanistic understanding of these behaviours. Our framework identifies research needs and will help to inform neurobiological and evolutionary studies endeavouring to uncover the multi-dimensional nature of vocal learning. This article is part of the theme issue 'Vocal learning in animals and humans'.

Re-evaluating vocal production learning in non-oscine birds.

The study of vocal production learning in birds is heavily biased towards oscine songbirds, making the songbird model the reference for comparative studies. However, as vocal learning was probably ancestral in songbirds, interspecific variations might all be variations on a single theme and need not be representative of the nature and characteristics of vocal learning in other bird groups. To assess the possible mechanisms of vocal learning and its evolution therefore requires knowledge about independently evolved incidences of vocal learning. This review examines the presence and nature of vocal production learning in non-songbirds. Using a broad definition of vocal learning and a comparative phylogenetic framework, I evaluate the evidence for vocal learning and its characteristics in non-oscine birds, including well-known vocal learners such as parrots and hummingbirds but also (putative) cases from other taxa. Despite the sometimes limited evidence, it is clear that vocal learning occurs in a range of different, non-related, taxa and can be caused by a variety of mechanisms. It is more widespread than often realized, calling for more systematic studies. Examining this variation may provide a window onto the evolution of vocal learning and increase the value of comparative research for understanding vocal learning in humans. This article is part of the theme issue 'Vocal learning in animals and humans'.

Vocal imitations and production learning by Australian musk ducks (Biziura lobata).

Acquiring vocalizations by learning them from other individuals is only known from a limited number of animal groups. For birds, oscine and some suboscine songbirds, parrots and hummingbirds demonstrate this ability. Here, we provide evidence for vocal learning in a member of a basal clade of the avian phylogeny: the Australian musk duck (Biziura lobata). A hand-reared individual imitated a slamming door and a human voice, and a female-reared individual imitated Pacific black duck quacks. These sounds have been described before, but were never analysed in any detail and went so far unnoticed by researchers of vocal learning. The imitations were produced during the males' advertising display. The hand-reared male used at least three different vocalizations in the display context, with each one produced in the same stereotyped and repetitive structure as the normal display sounds. Sounds of different origins could be combined in one vocalization and at least some of the imitations were memorized at an early age, well before they were produced later in life. Together with earlier observations of vocal differences between populations and deviant vocalizations in captive-reared individuals, these observations demonstrate the presence of advanced vocal learning at a level comparable to that of songbirds and parrots. We discuss the rearing conditions that may have given rise to the imitations and suggest that the structure of the duck vocalizations indicates a quite sophisticated and flexible control over the vocal production mechanism. The observations support the hypothesis that vocal learning in birds evolved in several groups independently rather than evolving once with several losses. This article is part of the theme issue 'Vocal learning in animals and humans'.

Rhythmic abilities in humans and non-human animals: a review and recommendations from a methodological perspective.

Rhythmic behaviour is ubiquitous in both human and non-human animals, but it is unclear whether the cognitive mechanisms underlying the specific rhythmic behaviours observed in different species are related. Laboratory experiments combined with highly controlled stimuli and tasks can be very effective in probing the cognitive architecture underlying rhythmic abilities. Rhythmic abilities have been examined in the laboratory with explicit and implicit perception tasks, and with production tasks, such as sensorimotor synchronization, with stimuli ranging from isochronous sequences of artificial sounds to human music. Here, we provide an overview of experimental findings on rhythmic abilities in human and non-human animals, while critically considering the wide variety of paradigms used. We identify several gaps in what is known about rhythmic abilities. Many bird species have been tested on rhythm perception, but research on rhythm production abilities in the same birds is lacking. By contrast, research in mammals has primarily focused on rhythm production rather than perception. Many experiments also do not differentiate between possible components of rhythmic abilities, such as processing of single temporal intervals, rhythmic patterns, a regular beat or hierarchical metrical structures. For future research, we suggest a careful choice of paradigm to aid cross-species comparisons, and a critical consideration of the multifaceted abilities that underlie rhythmic behaviour. This article is part of the theme issue 'Synchrony and rhythm interaction: from the brain to behavioural ecology'.

Editors' Review and Introduction: Learning Grammatical Structures: Developmental, Cross-Species, and Computational Approaches.

Human languages all have a grammar, that is, rules that determine how symbols in a language can be combined to create complex meaningful expressions. Despite decades of research, the evolutionary, developmental, cognitive, and computational bases of grammatical abilities are still not fully understood. "Artificial Grammar Learning" (AGL) studies provide important insights into how rules and structured sequences are learned, the relevance of these processes to language in humans, and whether the cognitive systems involved are shared with other animals. AGL tasks can be used to study how human adults, infants, animals, or machines learn artificial grammars of various sorts, consisting of rules defined typically over syllables, sounds, or visual items. In this introduction, we distill some lessons from the nine other papers in this special issue, which review the advances made from this growing body of literature. We provide a critical synthesis, identify the questions that remain open, and recognize the challenges that lie ahead. A key observation across the disciplines is that the limits of human, animal, and machine capabilities have yet to be found. Thus, this interdisciplinary area of research firmly rooted in the cognitive sciences has unearthed exciting new questions and venues for research, along the way fostering impactful collaborations between traditionally disconnected disciplines that are breaking scientific ground.

Structured Sequence Learning: Animal Abilities, Cognitive Operations, and Language Evolution.

Human language is a salient example of a neurocognitive system that is specialized to process complex dependencies between sensory events distributed in time, yet how this system evolved and specialized remains unclear. Artificial Grammar Learning (AGL) studies have generated a wealth of insights into how human adults and infants process different types of sequencing dependencies of varying complexity. The AGL paradigm has also been adopted to examine the sequence processing abilities of nonhuman animals. We critically evaluate this growing literature in species ranging from mammals (primates and rats) to birds (pigeons, songbirds, and parrots) considering also cross-species comparisons. The findings are contrasted with seminal studies in human infants that motivated the work in nonhuman animals. This synopsis identifies advances in knowledge and where uncertainty remains regarding the various strategies that nonhuman animals can adopt for processing sequencing dependencies. The paucity of evidence in the few species studied to date and the need for follow-up experiments indicate that we do not yet understand the limits of animal sequence processing capacities and thereby the evolutionary pattern. This vibrant, yet still budding, field of research carries substantial promise for advancing knowledge on animal abilities, cognitive substrates, and language evolution.

Source specific sound mapping: Spatial, temporal and spectral distribution of sound in the Dutch North Sea.

Effective measures for protecting and preserving the marine environment require an understanding of the potential impact of anthropogenic sound on marine life. A crucial component is a proper assessment of the anthropogenic soundscape: which sounds are present where, when and how strong? We provide an extensive case study modelling the spatial, temporal and spectral distribution of sound radiated by several anthropogenic sources (ships, seismic airguns, explosives) and a naturally occurring one (wind) in the Dutch North Sea. We present the results as a series of sound maps covering the whole of the Dutch North Sea, showing the spatial and temporal distribution of the energy from these sources. Averaged over a two year period, shipping is responsible for the largest amount of acoustic energy (∼1800 J), followed by seismic surveys (∼300 J), explosions (∼20 J) and wind (∼20 J) in the frequency band between 100 Hz and 100 kHz. Our study shows that anthropogenic sources are responsible for 100 times more acoustic energy (averaged over 2 years) in the Dutch North Sea than naturally occurring sound from wind. The potential impact of these sounds on aquatic animals depends not only on these temporally averaged and spatially integrated broadband energies, but also on the source-specific spatial, spectral and temporal variation. Shipping is dominant in the southern part and along the coast in the north, throughout the years and across the spectrum. Seismic surveys are relatively local and spatially and temporally dependent on exploration activities in any particular year, and spectrally shifted to low frequencies relative to the other sources. Explosions in the southern part contribute wide-extent high energy bursts across the spectrum. Relating modelled sound fields to the temporal and spatial distribution of animal species may provide a powerful tool for understanding the potential impact of anthropogenic sound on marine life.

Problem-solving males become more attractive to female budgerigars.

Darwin proposed that mate choice might contribute to the evolution of cognitive abilities. An open question is whether observing the cognitive skills of an individual makes it more attractive as a mate. In this study, we demonstrated that initially less-preferred budgerigar males became preferred after females observed that these males, but not the initially preferred ones, were able to solve extractive foraging problems. This preference shift did not occur in control experiments in which females observed males with free access to food or in which females observed female demonstrators solving these extractive foraging problems. Our results suggest that direct observation of problem-solving skills increases male attractiveness and that this could contribute to the evolution of the cognitive abilities underlying such skills.

Zebra finches (Taeniopygia guttata) can categorize vowel-like sounds on both the fundamental frequency ("pitch") and spectral envelope.

Humans can categorize vowels based on spectral quality (vowel identity) or pitch (speaker sex). Songbirds show similarities to humans with respect to speech sound discrimination and categorization, but it is unclear whether they can categorize harmonically structured vowel-like sounds on either spectrum or pitch, while ignoring the other parameter. We trained zebra finches in two experimental conditions to discriminate two sets of harmonic vowel-like sounds that could be distinguished either by spectrum or fundamental frequency (pitch). After the birds reached learning criterion, they were tested on new sounds that were either noise-vocoded versions of the trained sounds (sharing the spectral envelope with the trained sounds but lacking fine spectral detail from which pitch could be extracted) or sounds lacking the amplified harmonics (sharing only pitch with the trained sounds). Zebra finches showed no difference in the number of trials needed to learn each stimulus-response mapping. Birds trained on harmonic spectrum generalized their discrimination to vocoded sounds, and birds trained on pitch generalized their discrimination to harmonic sounds with a flat spectrum. These results demonstrate that, depending on the training requirements, birds can extract either fundamental frequency or spectral envelope of vowel-like sounds and use these parameters to categorize new sounds. (PsycINFO Database Record (c) 2019 APA, all rights reserved).

Mechanisms underlying speech sound discrimination and categorization in humans and zebra finches.

Speech sound categorization in birds seems in many ways comparable to that by humans, but it is unclear what mechanisms underlie such categorization. To examine this, we trained zebra finches and humans to discriminate two pairs of edited speech sounds that varied either along one dimension (vowel or speaker sex) or along two dimensions (vowel and speaker sex). Sounds could be memorized individually or categorized based on one dimension or by integrating or combining both dimensions. Once training was completed, we tested generalization to new speech sounds that were either more extreme, more ambiguous (i.e., close to the category boundary), or within-category intermediate between the trained sounds. Both humans and zebra finches learned the one-dimensional stimulus-response mappings faster than the two-dimensional mappings. Humans performed higher on the trained, extreme and within-category intermediate test-sounds than on the ambiguous ones. Some individual birds also did so, but most performed higher on the trained exemplars than on the extreme, within-category intermediate and ambiguous test-sounds. These results suggest that humans rely on rule learning to form categories and show poor performance when they cannot apply a rule. Birds rely mostly on exemplar-based memory with weak evidence for rule learning.

Bridging the gap: Learning of acoustic nonadjacent dependencies by a songbird.

Many animal species can detect dependencies between adjacent visual or auditory items in a string. Compared with adjacent dependencies, detecting nonadjacent dependencies, as present in linguistic constructions, is more challenging as this requires detecting a relation between items irrespective of the number and nature of the intervening items. There is limited evidence that nonhuman animals can detect such dependencies. An animal group in which such abilities might be expected is songbirds, which have learned songs consisting of a series of vocal elements given in specific sequences. So far no songbird (or other bird species) has been tested for its ability to detect nonadjacent dependencies. We examined whether zebra finches can detect the dependencies between items at the edges of artificially arranged strings of song elements. Zebra finches were trained to discriminate 2 sets of dependent song elements that always appeared in the same order (A and B; C and D), from other element combinations (AD, AC, BD, CB, CA, DB). The element combinations were separated by intervening (I) elements. Subsequent tests revealed that the finches could generalize the learned dependencies over different numbers and types of intervening items. Our findings show that the ability for detecting nonadjacent dependencies is not limited to humans or primates, and lend support to theories that suggest that nonadjacent dependencies can be learned by a nonlinguistic associative learning process. (PsycINFO Database Record

Selective auditory grouping by zebra finches: testing the iambic-trochaic law.

Humans have a strong tendency to spontaneously group visual or auditory stimuli together in larger patterns. One of these perceptual grouping biases is formulated as the iambic/trochaic law, where humans group successive tones alternating in pitch and intensity as trochees (high-low and loud-soft) and alternating in duration as iambs (short-long). The grouping of alternations in pitch and intensity into trochees is a human universal and is also present in one non-human animal species, rats. The perceptual grouping of sounds alternating in duration seems to be affected by native language in humans and has so far not been found among animals. In the current study, we explore to which extent these perceptual biases are present in a songbird, the zebra finch. Zebra finches were trained to discriminate between short strings of pure tones organized as iambs and as trochees. One group received tones that alternated in pitch, a second group heard tones alternating in duration, and for a third group, tones alternated in intensity. Those zebra finches that showed sustained correct discrimination were next tested with longer, ambiguous strings of alternating sounds. The zebra finches in the pitch condition categorized ambiguous strings of alternating tones as trochees, similar to humans. However, most of the zebra finches in the duration and intensity condition did not learn to discriminate between training stimuli organized as iambs and trochees. This study shows that the perceptual bias to group tones alternating in pitch as trochees is not specific to humans and rats, but may be more widespread among animals.

Spontaneous generalization of abstract multimodal patterns in young domestic chicks.

From the early stages of life, learning the regularities associated with specific objects is crucial for making sense of experiences. Through filial imprinting, young precocial birds quickly learn the features of their social partners by mere exposure. It is not clear though to what extent chicks can extract abstract patterns of the visual and acoustic stimuli present in the imprinting object, and how they combine them. To investigate this issue, we exposed chicks (Gallus gallus) to three days of visual and acoustic imprinting, using either patterns with two identical items or patterns with two different items, presented visually, acoustically or in both modalities. Next, chicks were given a choice between the familiar and the unfamiliar pattern, present in either the multimodal, visual or acoustic modality. The responses to the novel stimuli were affected by their imprinting experience, and the effect was stronger for chicks imprinted with multimodal patterns than for the other groups. Interestingly, males and females adopted a different strategy, with males more attracted by unfamiliar patterns and females more attracted by familiar patterns. Our data show that chicks can generalize abstract patterns by mere exposure through filial imprinting and that multimodal stimulation is more effective than unimodal stimulation for pattern learning.

Assessing the uniqueness of language: Animal grammatical abilities take center stage.

Questions related to the uniqueness of language can only be addressed properly by referring to sound knowledge of the relevant cognitive abilities of nonhuman animals. A key question concerns the nature and extent of animal rule-learning abilities. I discuss two approaches used to assess these abilities. One is comparing the structures of animal vocalizations to linguistic ones, and another is addressing the grammatical rule- and pattern-learning abilities of animals through experiments using artificial grammars. Neither of these approaches has so far provided unambiguous evidence of advanced animal abilities. However, when we consider how animal vocalizations are analyzed, the types of stimuli and tasks that are used in artificial grammar learning experiments, the limited number of species examined, and the groups to which these belong, I argue that the currently available evidence is insufficient to arrive at firm conclusions concerning the limitations of animal grammatical abilities. As a consequence, the gap between human linguistic rule-learning abilities and those of nonhuman animals may be smaller and less clear than is currently assumed. This means that it is still an open question whether a difference in the rule-learning and rule abstraction abilities between animals and humans played the key role in the evolution of language.

Zebra Finch Song Phonology and Syntactical Structure across Populations and Continents-A Computational Comparison.

Learned bird songs are often characterized by a high degree of variation between individuals and sometimes between populations, while at the same time maintaining species specificity. The evolution of such songs depends on the balance between plasticity and constraints. Captive populations provide an opportunity to examine signal variation and differentiation in detail, so we analyzed adult male zebra finch (Taeniopygia guttata) songs recorded from 13 populations across the world, including one sample of songs from wild-caught males in their native Australia. Cluster analysis suggested some, albeit limited, evidence that zebra finch song units belonged to universal, species-wide categories, linked to restrictions in vocal production and non-song parts of the vocal repertoire. Across populations, songs also showed some syntactical structure, although any song unit could be placed anywhere within the song. On the other hand, there was a statistically significant differentiation between populations, but the effect size was very small, and its communicative significance dubious. Our results suggest that variation in zebra finch songs within a population is largely determined by species-wide constraints rather than population-specific features. Although captive zebra finch populations have been sufficiently isolated to allow them to genetically diverge, there does not appear to have been any divergence in the genetically determined constraints that underlie song learning. Perhaps more surprising is the lack of locally diverged cultural traditions. Zebra finches serve as an example of a system where frequent learning errors may rapidly create within-population diversity, within broad phonological and syntactical constraints, and prevent the formation of long-term cultural traditions that allow populations to diverge.

Can Birds Perceive Rhythmic Patterns? A Review and Experiments on a Songbird and a Parrot Species.

While humans can easily entrain their behavior with the beat in music, this ability is rare among animals. Yet, comparative studies in non-human species are needed if we want to understand how and why this ability evolved. Entrainment requires two abilities: (1) recognizing the regularity in the auditory stimulus and (2) the ability to adjust the own motor output to the perceived pattern. It has been suggested that beat perception and entrainment are linked to the ability for vocal learning. The presence of some bird species showing beat induction, and also the existence of vocal learning as well as vocal non-learning bird taxa, make them relevant models for comparative research on rhythm perception and its link to vocal learning. Also, some bird vocalizations show strong regularity in rhythmic structure, suggesting that birds might perceive rhythmic structures. In this paper we review the available experimental evidence for the perception of regularity and rhythms by birds, like the ability to distinguish regular from irregular stimuli over tempo transformations and report data from new experiments. While some species show a limited ability to detect regularity, most evidence suggests that birds attend primarily to absolute and not relative timing of patterns and to local features of stimuli. We conclude that, apart from some large parrot species, there is limited evidence for beat and regularity perception among birds and that the link to vocal learning is unclear. We next report the new experiments in which zebra finches and budgerigars (both vocal learners) were first trained to distinguish a regular from an irregular pattern of beats and then tested on various tempo transformations of these stimuli. The results showed that both species reduced the discrimination after tempo transformations. This suggests that, as was found in earlier studies, they attended mainly to local temporal features of the stimuli, and not to their overall regularity. However, some individuals of both species showed an additional sensitivity to the more global pattern if some local features were left unchanged. Altogether our study indicates both between and within species variation, in which birds attend to a mixture of local and to global rhythmic features.