Language is a distinguishing characteristic of our species, and the course of its evolution is one of the hardest problems in science. It has long been generally considered that human speech requires a low larynx, and that the high larynx of nonhuman primates should preclude their producing the vowel systems universally found in human language. Examining the vocalizations through acoustic analyses, tongue anatomy, and modeling of acoustic potential, we found that baboons (Papio papio) produce sounds sharing the F1/F2 formant structure of the human [ɨ æ ɑ ɔ u] vowels, and that similarly with humans those vocalic qualities are organized as a system on two acoustic-anatomic axes. This confirms that hominoids can produce contrasting vowel qualities despite a high larynx. It suggests that spoken languages evolved from ancient articulatory skills already present in our last common ancestor with Cercopithecoidea, about 25 MYA.

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Manual gestures and speech recruit a common neural network, involving Broca's area in the left hemisphere. Such speech-gesture integration gave rise to theories on the critical role of manual gesturing in the origin of language. Within this evolutionary framework, research on gestural communication in our closer primate relatives has received renewed attention for investigating its potential language-like features. Here, using in-vivo anatomical MRI in 50 baboons, we found that communicative gesturing is related to Broca homologue's marker in monkeys, namely the ventral portion of the Inferior Arcuate sulcus (IA sulcus). In fact, both direction and degree of gestural communication's handedness - but not handedness for object manipulation - are associated and correlated with contralateral depth asymmetry at this exact IA sulcus portion. In other words, baboons that prefer to communicate with their right hand have a deeper left-than-right IA sulcus, than those preferring to communicate with their left hand and vice versa. Interestingly, in contrast to handedness for object manipulation, gestural communication's lateralisation is not associated to the Central sulcus depth asymmetry, suggesting a double dissociation of handedness' types between manipulative action and gestural communication. It is thus not excluded that this specific gestural lateralisation signature within the baboons' frontal cortex might reflect a phylogenetical continuity with language-related Broca lateralisation in humans.

The Planum Temporale (PT) is one of the key hubs of the language network in the human brain. The gross asymmetry of this perisylvian region toward the left brain was considered as the most emblematic marker of hemispheric specialization of language processes in the brain. Interestingly, this neuroanatomical signature was documented also in newborn infants and preterms, suggesting the early brain's readiness for language acquisition. Nevertheless, this latter interpretation was questioned by a recent report in nonhuman primates of a potential similar signature in newborn baboons Papio anubis based on PT surface measures. Whether this "tip of the iceberg" PT asymmetry is actually reflecting asymmetry of its underlying grey matter volume remain unclear but critical to investigate potential continuities of cortical specialization with human infants. Here we report a population-level leftward asymmetry of the Planum Temporale grey matter volume in in vivo 34 newborn baboons Papio anubis, which showed intra-individual positive correlation with PT surface's asymmetry measures but also a more pronounced degree of leftward asymmetry at the population-level. This finding demonstrates that PT leftward structural asymmetry in this Old World monkey species is a robust phenomenon in early primate development, which clearly speaks for a continuity with early human brain specialization. Results also strengthen the hypothesis that early PT asymmetry might be not a human-specific marker for the pre-wired language-ready brain in infants.

The Arcuate Fasciculus (AF) is of considerable interdisciplinary interest, because of its major implication in language processing. Theories about language brain evolution are based on anatomical differences in the AF across primates. However, changing methodologies and nomenclatures have resulted in conflicting findings regarding interspecies AF differences: Historical knowledge about the AF originated from human blunt dissections and later from monkey tract-tracing studies. Contemporary tractography studies reinvestigate the fasciculus' morphology, but remain heavily bound to unclear anatomical priors and methodological limitations. First, we aim to disentangle the influences of these three epistemological steps on existing AF conceptions, and to propose a contemporary model to guide future work. Second, considering the influence of various AF conceptions, we discuss four key evolutionary changes that propagated current views about language evolution: 1) frontal terminations, 2) temporal terminations, 3) greater Dorsal-versus Ventral Pathway expansion, 4) lateralisation. We conclude that new data point towards a more shared AF anatomy across primates than previously described. Language evolution theories should incorporate this continuous AF evolution across primates.

Highlights Newborn baboons present a leftward Planum Temporale Asymmetry. The proportion is similar to human newborns and adults. As in human infants, the asymmetry strength increases across development. These findings question early Planum Temporale Asymmetry as a human-specific marker for the prewired language-ready brain.

Humans are the only species that can speak. Nonhuman primates, however, share some ‘domain-general’ cognitive properties that are essential to language processes. Whether these shared cognitive properties between humans and nonhuman primates are the results of a continuous evolution [homologies] or of a convergent evolution [analogies] remain difficult to demonstrate. However, comparing their respective underlying structure—the brain—to determinate their similarity or their divergence across species is critical to help increase the probability of either of the two hypotheses, respectively. Key areas associated with language processes are the Planum Temporale, Broca’s Area, the Arcuate Fasciculus, Cingulate Sulcus, The Insula, Superior Temporal Sulcus, the Inferior Parietal lobe, and the Central Sulcus. These structures share a fundamental feature: They are functionally and structurally specialised to one hemisphere. Interestingly, several nonhuman primate species, such as chimpanzees and baboons, show human-like structural brain asymmetries for areas homologous to key language regions. The question then arises: for what function did these asymmetries arise in non-linguistic primates, if not for language per se? In an attempt to provide some answers, we review the literature on the lateralisation of the gestural communication system, which may represent the missing behavioural link to brain asymmetries for language area’s homologues in our common ancestor.

Manual gestures and speech recruit a common neural network, involving Broca area in the left hemisphere. Evolutionary questions about this language organisation led to a renewed attention for comparative research on gestural communication in our closer primate relatives and its potential language-like features. Here, using in vivo anatomical MRI in 80 baboons, we found that communicative gesturing's lateralisation - but not handedness for manipulation - is related to Broca homologue's marker in monkeys, namely contralateral depth hemispheric asymmetry of the ventral portion of the inferior arcuate sulcus. This finding provides strong support for the gestural evolutionary continuities with language- related frontal specialisation, dating back not only to Homo sapiens evolution, but rather to a much older common ancestor shared with old-world monkeys, 25-35 million years ago.