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Gesturing is a widespread phenomenon in the animal kingdom, as well as an important facet of human language. As such, studying the communicative gestures of our close phylogenetic relatives is essential to better understand its evolution. While recent studies have shown that ape gestural communication shares some properties with human language, very little is known about the properties of gestural communication in monkeys. The aims of this study were to establish the first quantitative repertoire of gestural communication in a species of old-world monkeys, the olive baboon Papio anubis, and to determine its properties in terms of variability, flexibility, and intentionality. Gestural communication was continuously recorded on 47 captive olive baboons over 1 year. Their gestural repertoire was composed of 67 visual, tactile, and audible gestures, which were used flexibly across different contexts, indicating means–ends dissociation. We found that the use of gestures was variable across individuals and ages, notably with repertoire size decreasing with age. Baboons used their gestures intentionally; gesturers looked at the recipient, waited for a response, and took into account the attentional state of their recipient. Particularly, they actively adjusted the modality of their gesture to the recipient’s visual attention, using more visual gestures when the recipient was attending and more tactile gestures when the recipient was not. Thus, the gestural communicative system of olive baboons possesses properties which are similar to the ones of apes and to human language. These intentional features of gestural communication, that may constitute a prerequisite of language evolution, may have been present in the common ancestor of baboons and humans, around 30–40 million years ago.

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 non-human 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 remains unclear but critical to investigate potential continuities of cortical specialization with human infants. Here we report a population-level leftward asymmetry of the PT grey matter volume in in vivo 34 newborn baboons P. 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.

About 66–72% of human mothers cradle their infants on their left side. Given that left-cradling exposes the baby’s face to the mother’s left visual field (i.e., mainly projected to her right hemisphere) and is altered by emotional states such as stress, maternal left-cradling was interpreted as reflecting right-hemispheric dominance for emotional processing. Whether this phenomenon is unique to human evolution is still in debate. In the present study we followed 44 olive baboon ( Papio anubis ) mothers and their infants in different social groups. We found that a maternal cradling bias exists and is predominantly towards the left in a similar proportion as in humans, but shifts toward a right bias in mothers living in high density groups. The sensitivity of left-cradling to social pressure highlights its potential links with the mother’s stress as reported in humans. Our finding clearly illustrates the phylogenetic continuity between humans and Old-World monkeys concerning this lateralization and its potential links with hemispheric specialization for emotions, inherited from a common ancestor 25–35 million years ago.

•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. The “language-ready” brain theory suggests that the infant brain is pre-wired for language acquisition prior to language exposure. As a potential brain marker of such a language readiness, a leftward structural brain asymmetry was found in human infants for the Planum Temporale (PT), which overlaps with Wernicke's area. In the present longitudinal in vivo MRI study conducted in 35 newborn monkeys (Papio anubis), we found a similar leftward PT surface asymmetry. Follow-up rescanning sessions on 29 juvenile baboons at 7-10 months showed that such an asymmetry increases across the two ages classes. These original findings in non-linguistic primate infants strongly question the idea that the early PT asymmetry constitutes a human infant-specific marker for language development. Such a shared early perisylvian organization provides additional support that PT asymmetry might be related to a lateralized system inherited from our last common ancestor with Old-World monkeys at least 25–35 million years ago.

The planum temporale ( PT ), a key language area, is specialized in the left hemisphere in prelinguistic infants and considered as a marker of the pre-wired language-ready brain. However, studies have reported a similar structural PT left-asymmetry not only in various adult non-human primates, but also in newborn baboons. Its shared functional links with language are not fully understood. Here we demonstrate using previously obtained MRI data that early detection of PT left-asymmetry among 27 newborn baboons ( Papio anubis , age range of 4 days to 2 months) predicts the future development of right-hand preference for communicative gestures but not for non-communicative actions. Specifically, only newborns with a larger left-than-right PT were more likely to develop a right-handed communication once juvenile, a contralateral brain-gesture link which is maintained in a group of 70 mature baboons. This finding suggests that early PT asymmetry may be a common inherited prewiring of the primate brain for the ontogeny of ancient lateralised properties shared between monkey gesture and human language. The planum temporale is a key structure in the human language network. Here the authors show that planum temporale asymmetry at birth in baboons predicts the development of communicative right-hand use, which suggests some common features in the wiring of communicative properties between species.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.An amendment to this paper has been published and can be accessed via a link at the top of the paper.

•Strengths and challenges of longitudinal non-human primate MRI are described.•Statistical power calculation of longitudinal and cross-sectional designs are provided.•The impact of template choice on grey matter estimation is demonstrated.•Recommendations for designing and analysing such studies are provided. Longitudinal non-human primate neuroimaging has the potential to greatly enhance our understanding of primate brain structure and function. Here we describe its specific strengths, compared to both cross-sectional non-human primate neuroimaging and longitudinal human neuroimaging, but also its associated challenges. We elaborate on factors guiding the use of different analytical tools, subject-specific versus age-specific templates for analyses, and issues related to statistical power.

•Data sharing of primate neuroimaging offers new opportunities.•The potential of metadata to enrich primate neuroimaging is described.•Illustration of how meta-data can be shared in the BIDS format is provided. Sharing and pooling large amounts of non-human primate neuroimaging data offer new exciting opportunities to understand the primate brain. The potential of big data in non-human primate neuroimaging could however be tremendously enhanced by combining such neuroimaging data with other types of information. Here we describe metadata that have been identified as particularly valuable by the non-human primate neuroimaging community, including behavioural, genetic, physiological and phylogenetic data.

The “voice areas” in the superior temporal cortex have been identified in both humans and non-human primates as selective to conspecific vocalizations only (i.e., expressed by members of our own species), suggesting its old evolutionary roots across the primate lineage. With respect to non-human primate species, it remains unclear whether the listening of vocal emotions from conspecifics leads to similar or different cerebral activations when compared to heterospecific calls (i.e., expressed by another primate species) triggered by the same emotion. Using a neuroimaging technique rarely employed in monkeys so far, functional Near Infrared Spectroscopy, the present study investigated in three lightly anesthetized female baboons ( Papio anubis ), temporal cortex activities during exposure to agonistic vocalizations from conspecifics and from other primates (chimpanzees— Pan troglodytes ), and energy matched white noises in order to control for this low-level acoustic feature. Permutation test analyses on the extracted OxyHemoglobin signal revealed great inter-individual differences on how conspecific and heterospecific vocal stimuli were processed in baboon brains with a cortical response recorded either in the right or the left temporal cortex. No difference was found between emotional vocalizations and their energy-matched white noises. Despite the phylogenetic gap between Homo sapiens and African monkeys, modern humans and baboons both showed a highly heterogeneous brain process for the perception of vocal and emotional stimuli. The results of this study do not exclude that old evolutionary mechanisms for vocal emotional processing may be shared and inherited from our common ancestor.