Functional reorganization of brain regions supporting artificial grammar learning across the first half year of life.

Pre-babbling infants can track nonadjacent dependencies (NADs) in the auditory domain. While this forms a crucial prerequisite for language acquisition, the neurodevelopmental origins of this ability remain unknown. We applied functional near-infrared spectroscopy in neonates and 6- to 7-month-old infants to investigate the neural substrate supporting NAD learning and detection using tone sequences in an artificial grammar learning paradigm. Detection of NADs was indicated by left prefrontal activation in neonates while by left supramarginal gyrus (SMG), superior temporal gyrus (STG), and inferior frontal gyrus activation in 6- to 7-month-olds. Functional connectivity analyses further indicated that the neonate activation pattern during the test phase benefited from a brain network consisting of prefrontal regions, left SMG and STG during the rest and learning phases. These findings suggest a left-hemispheric learning-related functional brain network may emerge at birth and serve as the foundation for the later engagement of these regions for NAD detection, thus, providing a neural basis for language acquisition.

The function and evolution of child-directed communication.

Humans communicate with small children in unusual and highly conspicuous ways (child-directed communication (CDC)), which enhance social bonding and facilitate language acquisition. CDC-like inputs are also reported for some vocally learning animals, suggesting similar functions in facilitating communicative competence. However, adult great apes, our closest living relatives, rarely signal to their infants, implicating communication surrounding the infant as the main input for infant great apes and early humans. Given cross-cultural variation in the amount and structure of CDC, we suggest that child-surrounding communication (CSC) provides essential compensatory input when CDC is less prevalent-a paramount topic for future studies.

Declarative referential gesturing in a wild chimpanzee (Pan troglodytes).

Humans are argued to be unique in their ability and motivation to share attention with others about external entities-sharing attention for sharing's sake. Indeed, in humans, using referential gestures declaratively to direct the attention of others toward external objects and events emerges in the first year of life. In contrast, wild great apes seldom use referential gestures, and when they do, it seems to be exclusively for imperative purposes. This apparent species difference has fueled the argument that the motivation and ability to share attention with others is a human-specific trait with important downstream consequences for the evolution of our complex cognition [M. Tomasello, Becoming Human (2019)]. Here, we report evidence of a wild ape showing a conspecific an item of interest. We provide video evidence of an adult female chimpanzee, Fiona, showing a leaf to her mother, Sutherland, in the context of leaf grooming in Kibale Forest, Uganda. We use a dataset of 84 similar leaf-grooming events to explore alternative explanations for the behavior, including food sharing and initiating dyadic grooming or playing. Our observations suggest that in highly specific social conditions, wild chimpanzees, like humans, may use referential showing gestures to direct others' attention to objects simply for the sake of sharing. The difference between humans and our closest living relatives in this regard may be quantitative rather than qualitative, with ramifications for our understanding of the evolution of human social cognition.

Seeds of language-like generativity in bird call combinations.

Language is unbounded in its generativity, enabling the flexible combination of words into novel sentences. Critically, these constructions are intelligible to others due to our ability to derive a sentence's compositional meaning from the semantic relationships among its components. Some animals also concatenate meaningful calls into compositional-like combinations to communicate more complex information. However, these combinations are structurally highly stereotyped, suggesting a bounded system of holistically perceived signals that impedes the processing of novel variants. Using long-term data and playback experiments on pied babblers, we demonstrate that, despite production stereotypy, they can nevertheless process structurally modified and novel combinations of their calls, demonstrating a capacity for deriving meaning compositionally. Furthermore, differential responses to artificial combinations by fledglings suggest that this compositional sensitivity is acquired ontogenetically. Our findings demonstrate animal combinatorial systems can be flexible at the perceptual level and that such perceptual flexibility may represent a precursor of language-like generativity.

Cross-population variation in usage of a call combination: evidence of signal usage flexibility in wild bonobos.

The arbitrary relationship between signifier and signified is one of the features responsible for language's extreme lability, adaptability, and expressiveness. Understanding this arbitrariness and its emergence is essential in any account of the evolution of language. To shed light on the phylogeny of the phenomenon, comparative data examining the relationship between signal form and function in the communication systems of non-humans is central. Here we report the results of a study on the production and usage the whistle-high hoot call combination (W + HH) from two distant populations of wild bonobos (Pan paniscus): Lui Kotale, DRC, and Kokolopori, DRC. We find that the context in which bonobos produce the W + HHs varies systematically between populations. Our results suggest that variation in W + HH production may represent an example of signal-adjustment optionality, a key component of arbitrariness.

Degraded and computer-generated speech processing in a bonobo.

The human auditory system is capable of processing human speech even in situations when it has been heavily degraded, such as during noise-vocoding, when frequency domain-based cues to phonetic content are strongly reduced. This has contributed to arguments that speech processing is highly specialized and likely a de novo evolved trait in humans. Previous comparative research has demonstrated that a language competent chimpanzee was also capable of recognizing degraded speech, and therefore that the mechanisms underlying speech processing may not be uniquely human. However, to form a robust reconstruction of the evolutionary origins of speech processing, additional data from other closely related ape species is needed. Specifically, such data can help disentangle whether these capabilities evolved independently in humans and chimpanzees, or if they were inherited from our last common ancestor. Here we provide evidence of processing of highly varied (degraded and computer-generated) speech in a language competent bonobo, Kanzi. We took advantage of Kanzi's existing proficiency with touchscreens and his ability to report his understanding of human speech through interacting with arbitrary symbols called lexigrams. Specifically, we asked Kanzi to recognise both human (natural) and computer-generated forms of 40 highly familiar words that had been degraded (noise-vocoded and sinusoidal forms) using a match-to-sample paradigm. Results suggest that-apart from noise-vocoded computer-generated speech-Kanzi recognised both natural and computer-generated voices that had been degraded, at rates significantly above chance. Kanzi performed better with all forms of natural voice speech compared to computer-generated speech. This work provides additional support for the hypothesis that the processing apparatus necessary to deal with highly variable speech, including for the first time in nonhuman animals, computer-generated speech, may be at least as old as the last common ancestor we share with bonobos and chimpanzees.

First observation of a chimpanzee with albinism in the wild: Social interactions and subsequent infanticide.

Albinism-the congenital absence of pigmentation-is a very rare phenomenon in animals due to the significant costs to fitness of this condition. Both humans and non-human individuals with albinism face a number of challenges, such as reduced vision, increased exposure to ultraviolet radiation, or compromised crypticity resulting in an elevated vulnerability to predation. However, while observations of social interactions involving individuals with albinism have been observed in wild non-primate animals, such interactions have not been described in detail in non-human primates (hereafter, primates). Here, we report, to our knowledge, the first sighting of an infant with albinism in wild chimpanzees (Pan troglodytes schweinfurthii), including social interactions between the infant, its mother, and group members. We also describe the subsequent killing of the infant by conspecifics as well as their behavior towards the corpse following the infanticide. Finally, we discuss our observations in relation to our understanding of chimpanzee behavior or attitudes towards individuals with very conspicuous appearances.

Chestnut-crowned babbler calls are composed of meaningless shared building blocks.

A core component of human language is its combinatorial sound system: meaningful signals are built from different combinations of meaningless sounds. Investigating whether nonhuman communication systems are also combinatorial is hampered by difficulties in identifying the extent to which vocalizations are constructed from shared, meaningless building blocks. Here we present an approach to circumvent this difficulty and show that a pair of functionally distinct chestnut-crowned babbler (Pomatostomus ruficeps) vocalizations can be decomposed into perceptibly distinct, meaningless entities that are shared across the 2 calls. Specifically, by focusing on the acoustic distinctiveness of sound elements using a habituation-discrimination paradigm on wild-caught babblers under standardized aviary conditions, we show that 2 multielement calls are composed of perceptibly distinct sounds that are reused in different arrangements across the 2 calls. Furthermore, and critically, we show that none of the 5 constituent elements elicits functionally relevant responses in receivers, indicating that the constituent sounds do not carry the meaning of the call and so are contextually meaningless. Our work, which allows combinatorial systems in animals to be more easily identified, suggests that animals can produce functionally distinct calls that are built in a way superficially reminiscent of the way that humans produce morphemes and words. The results reported lend credence to the recent idea that language's combinatorial system may have been preceded by a superficial stage where signalers neither needed to be cognitively aware of the combinatorial strategy in place, nor of its building blocks.

Compositionality in animals and humans.

A key step in understanding the evolution of human language involves unravelling the origins of language's syntactic structure. One approach seeks to reduce the core of syntax in humans to a single principle of recursive combination, merge, for which there is no evidence in other species. We argue for an alternative approach. We review evidence that beneath the staggering complexity of human syntax, there is an extensive layer of nonproductive, nonhierarchical syntax that can be fruitfully compared to animal call combinations. This is the essential groundwork that must be explored and integrated before we can elucidate, with sufficient precision, what exactly made it possible for human language to explode its syntactic capacity, transitioning from simple nonproductive combinations to the unrivalled complexity that we now have.

Dwarf mongoose alarm calls: investigating a complex non-human animal call.

Communication plays a vital role in the social lives of many species and varies greatly in complexity. One possible way to increase communicative complexity is by combining signals into longer sequences, which has been proposed as a mechanism allowing species with a limited repertoire to increase their communicative output. In mammals, most studies on combinatoriality have focused on vocal communication in non-human primates. Here, we investigated a potential combination of alarm calls in the dwarf mongoose (Helogale parvula), a non-primate mammal. Acoustic analyses and playback experiments with a wild population suggest: (i) that dwarf mongooses produce a complex call type (T3) which, at least at the surface level, seems to comprise units that are not functionally different to two meaningful alarm calls (aerial and terrestrial); and (ii) that this T3 call functions as a general alarm, produced in response to a wide range of threats. Using a novel approach, we further explored multiple interpretations of the T3 call based on the information content of the apparent comprising calls and how they are combined. We also considered an alternative, non-combinatorial interpretation that frames T3 as the origin, rather than the product, of the individual alarm calls. This study complements previous knowledge of vocal combinatoriality in non-primate mammals and introduces an approach that could facilitate comparisons between different animal and human communication systems.

An exploration of Menzerath's law in wild mountain gorilla vocal sequences.

Menzerath's law, traditionally framed as a negative relationship between the size of a structure and its constituent parts (e.g. sentences with more clauses have shorter clauses), is widespread across information-coding systems ranging from human language and the vocal and gestural sequences of primates and birds, to the building blocks of DNA, genes and proteins. Here, we analysed an extensive dataset of 'close-call' sequences produced by wild mountain gorillas (Gorilla beringei beringei, no. individuals = 10, no. sequences = 2189) to determine whether, in accordance with Menzerath's law, a negative relationship existed between the number of vocal units in a sequence and the duration of its constituent units. We initially found positive evidence for this but, on closer inspection, the negative relationship was driven entirely by the difference between single- and multi-unit (two to six unit) sequences. Once single-unit sequences were excluded from the analysis, we identified a relationship in the opposite direction, with longer sequences generally composed of longer units. The close-call sequences of mountain gorillas therefore represent an intriguing example of a non-human vocal system that only partially conforms to the predictions of Menzerath's law.

Meaningful call combinations and compositional processing in the southern pied babbler.

Language's expressive power is largely attributable to its compositionality: meaningful words are combined into larger/higher-order structures with derived meaning. Despite its importance, little is known regarding the evolutionary origins and emergence of this syntactic ability. Although previous research has shown a rudimentary capability to combine meaningful calls in primates, because of a scarcity of comparative data, it is unclear to what extent analog forms might also exist outside of primates. Here, we address this ambiguity and provide evidence for rudimentary compositionality in the discrete vocal system of a social passerine, the pied babbler (Turdoides bicolor). Natural observations and predator presentations revealed that babblers produce acoustically distinct alert calls in response to close, low-urgency threats and recruitment calls when recruiting group members during locomotion. On encountering terrestrial predators, both vocalizations are combined into a "mobbing sequence," potentially to recruit group members in a dangerous situation. To investigate whether babblers process the sequence in a compositional way, we conducted systematic experiments, playing back the individual calls in isolation as well as naturally occurring and artificial sequences. Babblers reacted most strongly to mobbing sequence playbacks, showing a greater attentiveness and a quicker approach to the loudspeaker, compared with individual calls or control sequences. We conclude that the sequence constitutes a compositional structure, communicating information on both the context and the requested action. Our work supports previous research suggesting combinatoriality as a viable mechanism to increase communicative output and indicates that the ability to combine and process meaningful vocal structures, a basic syntax, may be more widespread than previously thought.

Leadless Permanent Pacing: A Single Centre Australian Experience.

BACKGROUND: To describe the performance and clinical outcomes of consecutive patients having a leadless pacemaker (LP) implanted at a single institution. METHODS: Clinical data and device parameters were prospectively collected on all patients undergoing LP implantation from November 2015 to April 2018. RESULTS: A total of 79 patients (52 male), median age of 78 years, was included. Leadless pacemaker implantation was successful in 76 patients (96%). Implantation failed in two patients due to excessive venous tortuosity and due to inadequate sensing in another. Seventy-three (73) patients (96%) had chronic atrial fibrillation and all had a Class I or II indication for pacing. Procedure time was 29minutes (IQR 21-43) and fluoroscopy time was 8minutes (IQR 5-13). The median R wave at implant was 11.2mV (IQR 6.9-15.0). The median capture threshold at 0.24ms was 0.5V (IQR 0.4-0.9) and impedance was 754Ω (IQR 680-880). Intraprocedural acute dislodgement occurred in one patient following cutting of the tether but successful snaring and reimplantation was performed. During a median follow-up of 355days (range 9-905), overall electrical performance has been excellent. No patients have been readmitted for device revision or complications. Five (5) patients (7%) died during follow-up from unrelated causes. CONCLUSIONS: Leadless pacemakers can be implanted safely and effectively in the majority of patients. Device electrical performance was excellent over a median follow-up of 12 months.

Experimental Evidence for Phonemic Contrasts in a Nonhuman Vocal System.

The ability to generate new meaning by rearranging combinations of meaningless sounds is a fundamental component of language. Although animal vocalizations often comprise combinations of meaningless acoustic elements, evidence that rearranging such combinations generates functionally distinct meaning is lacking. Here, we provide evidence for this basic ability in calls of the chestnut-crowned babbler (Pomatostomus ruficeps), a highly cooperative bird of the Australian arid zone. Using acoustic analyses, natural observations, and a series of controlled playback experiments, we demonstrate that this species uses the same acoustic elements (A and B) in different arrangements (AB or BAB) to create two functionally distinct vocalizations. Specifically, the addition or omission of a contextually meaningless acoustic element at a single position generates a phoneme-like contrast that is sufficient to distinguish the meaning between the two calls. Our results indicate that the capacity to rearrange meaningless sounds in order to create new signals occurs outside of humans. We suggest that phonemic contrasts represent a rudimentary form of phoneme structure and a potential early step towards the generative phonemic system of human language.

Element repetition rates encode functionally distinct information in pied babbler 'clucks' and 'purrs'.

Human language is a recombinant system that achieves its productivity through the combination of a limited set of sounds. Research investigating the evolutionary origin of this generative capacity has generally focused on the capacity of non-human animals to combine different types of discrete sounds to encode new meaning, with less emphasis on meaning-differentiating mechanisms achieved through potentially simpler temporal modifications within a sequence of repeated sounds. Here we show that pied babblers (Turdoides bicolor) generate two functionally distinct vocalisations composed of the same sound type, which can only be distinguished by the number of repeated elements. Specifically, babblers produce extended 'purrs' composed of, on average, around 17 element repetitions when drawing young offspring to a food source and truncated 'clucks' composed of a fixed number of 2-3 elements when collectively mediating imminent changes in foraging site. We propose that meaning-differentiating temporal structuring might be a much more widespread combinatorial mechanism than currently recognised and is likely of particular value for species with limited vocal repertoires in order to increase their communicative output.

Language evolution: syntax before phonology?

Phonology and syntax represent two layers of sound combination central to language's expressive power. Comparative animal studies represent one approach to understand the origins of these combinatorial layers. Traditionally, phonology, where meaningless sounds form words, has been considered a simpler combination than syntax, and thus should be more common in animals. A linguistically informed review of animal call sequences demonstrates that phonology in animal vocal systems is rare, whereas syntax is more widespread. In the light of this and the absence of phonology in some languages, we hypothesize that syntax, present in all languages, evolved before phonology.

Call combination production is linked to the social environment in Western Australian magpies (Gymnorhina tibicen dorsalis).

It has recently become clear that some language-specific traits previously thought to be unique to humans (such as the capacity to combine sounds) are widespread in the animal kingdom. Despite the increase in studies documenting the presence of call combinations in non-human animals, factors promoting this vocal trait are unclear. One leading hypothesis proposes that communicative complexity co-evolved with social complexity owing to the need to transmit a diversity of information to a wider range of social partners. The Western Australian magpie (Gymnorhina tibicen dorsalis) provides a unique model to investigate this proposed link because it is a group-living, vocal learning species that is capable of multi-level combinatoriality (independently produced calls contain vocal segments and comprise combinations). Here, we compare variations in the production of call combinations across magpie groups ranging in size from 2 to 11 birds. We found that callers in larger groups give call combinations: (i) in greater diversity and (ii) more frequently than callers in smaller groups. Significantly, these observations support the hypothesis that combinatorial complexity may be related to social complexity in an open-ended vocal learner, providing an important step in understanding the role that sociality may have played in the development of vocal combinatorial complexity. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Beyond bigrams: call sequencing in the common marmoset (Callithrix jacchus) vocal system.

Over the last two decades, an emerging body of research has demonstrated that non-human animals exhibit the ability to combine context-specific calls into larger sequences. These structures have frequently been compared with language's syntax, whereby linguistic units are combined to form larger structures, and leveraged to argue that syntax might not be unique to language. Currently, however, the overwhelming majority of examples of call combinations are limited to simple sequences comprising just two calls which differ dramatically from the open-ended hierarchical structuring of the syntax found in language. We revisit this issue by taking a whole-repertoire approach to investigate combinatoriality in common marmosets (Callithrix jacchus). We use Markov chain models to quantify the vocal sequences produced by marmosets providing evidence for structures beyond the bigram, including three-call and even combinations of up to eight or nine calls. Our analyses of these longer vocal sequences are suggestive of potential further internal organization, including some amount of recombination, nestedness and non-adjacent dependencies. We argue that data-driven, whole-repertoire analyses are fundamental to uncovering the combinatorial complexity of non-human animals and will further facilitate meaningful comparisons with language's combinatoriality.

Syntax-like Structures in Maternal Contact Calls of Chestnut-Crowned Babblers (Pomatostomus ruficeps).

The combination of meaning-bearing units (e.g., words) into higher-order structures (e.g., compound words and phrases) is integral to human language. Despite this central role of syntax in language, little is known about its evolutionary progression. Comparative data using animal communication systems offer potential insights, but only a handful of species have been identified to combine meaningful calls together into larger signals. We investigated a candidate for syntax-like structure in the highly social chestnut-crowned babbler (Pomatostomus ruficeps). Using a combination of behavioral observations, acoustic analyses, and playback experiments, we test whether the form and function of maternal contact calls is modified by combining the core "piping" elements of such calls with at least one other call element or call. Results from the acoustic analyses (236 analysed calls from 10 individuals) suggested that piping call elements can be flexibly initiated with either "peow" elements from middle-distance contact calls or adult "begging" calls to form "peow-pipe" and "beg-pipe" calls. Behavioral responses to playbacks (20 trials to 7 groups) of natural peow-pipe and beg-pipe calls were comparable to those of artificially generated versions of each call using peow elements and begging calls from other contexts. Furthermore, responses to playbacks (34 trials to 7 groups) of the three forms of maternal contact calls (piping alone, peow-pipe, beg-pipe) differed. Together these data suggest that meaning encoded in piping calls is modified by combining such calls with begging calls or peow elements used in other contexts and so provide rare empirical evidence for syntactic-like structuring in a nonhuman animal.

Chimpanzee gestural exchanges share temporal structure with human language.

Humans regularly engage in efficient communicative conversations, which serve to socially align individuals1. In conversations, we take fast-paced turns using a human-universal structure of deploying and receiving signals which shows consistent timing across cultures2. We report here that chimpanzees also engage in rapid signal-to-signal turn-taking during face-to-face gestural exchanges with a similar average latency between turns to that of human conversation. This correspondence between human and chimpanzee face-to-face communication points to shared underlying rules in communication. These structures could be derived from shared ancestral mechanisms or convergent strategies that enhance coordinated interactions or manage competition for communicative 'space'.