Genetic determinants of individual variation in the superior temporal sulcus of chimpanzees (Pan troglodytes).

The superior temporal sulcus (STS) is a conserved fold that divides the middle and superior temporal gyri. In humans, there is considerable variation in the shape, folding pattern, lateralization, and depth of the STS that have been reported to be associated with social cognition and linguistic functions. We examined the role that genetic factors play on individual variation in STS morphology in chimpanzees. The surface area and depth of the STS were quantified in sample of 292 captive chimpanzees comprised of two genetically isolated population of individuals. The chimpanzees had been previously genotyped for AVPR1A and KIAA0319, two genes that play a role in social cognition and communication in humans. Single nucleotide polymorphisms in the KIAA0319 and AVPR1A genes were associated with average depth as well as asymmetries in the STS. By contrast, we found no significant effects of these KIA0319 and AVPR1A polymorphism on surface area and depth measures for the central sulcus. The overall findings indicate that genetic factors account for a small to moderate amount of variation in STS morphology in chimpanzees. These findings are discussed in the context of the role of the STS in social cognition and language in humans and their potential evolutionary origins.

Humans (Homo sapiens) but not baboons (Papio papio) demonstrate crossmodal pitch-luminance correspondence.

Humans spontaneously and consistently map information coming from different sensory modalities. Surprisingly, the phylogenetic origin of such cross-modal correspondences has been under-investigated. A notable exception is the study of Ludwig et al. (Visuoauditory mappings between high luminance and high pitch are shared by chimpanzees [Pan troglodytes] and humans. Proceedings of the National Academy of Sciences, 108(51), 20661-20665) which reports that both humans and chimpanzees spontaneously map high-pitched sounds with bright objects and low-pitched sounds with dark objects. Our pre-registered study aimed to directly replicate this research on both humans and baboons (Papio papio), an old world monkey which is more phylogenetically distant from humans than chimpanzees. Following Ludwig et al. participants were presented with a visual classification task where they had to sort black and white square (low and high luminance), while background sounds (low or high-pitched tones) were playing. Whereas we replicated the finding that humans' performance on the visual task was affected by congruency between sound and luminance of the target, we did not find any of those effects on baboons' performance. These results question the presence of a shared cross-modal pitch-luminance mapping in other nonhuman primates.

Maternal cradling bias in baboons: The first environmental factor affecting early infant handedness development?

The most emblematic behavioral manifestation of human brain asymmetries is handedness. While the precise mechanisms behind the development of handedness are still widely debated, empirical evidences highlight that besides genetic factors, environmental factors may play a crucial role. As one of these factors, maternal cradling behavior may play a key role in the emergence of early handedness in the offspring. In the present study we followed 41 Papio anubis infants living in social groups with their mother for which direction (e.g., left- or right-arm) and degree of maternal cradling-side bias were available from a previous published study. We assessed hand preferences for an unimanual grasping task at three developmental stages: (A) 0-4, (B) 4-6, and (C) 9-10 months of age. We found that individual hand preferences for grasping exist as soon as the first months of age, with a population-level left-handedness predominance, being stable until 6 months; to wit the period during which juveniles are mainly carried by their mothers. More importantly, this early postnatal handedness is positively correlated with maternal cradling lateralization. Interestingly, hand preferences assessed later in the development, once juveniles are no longer carried (i.e., from 9 to 10 months of age), are less dependent from the maternal cradling bias and less consistent with the earlier developmental stages, especially in infants initially cradled on the right maternal side. Our findings suggest that the ontogenetic dynamics of the infant's hand preference and its changes might ultimately rely on the degree of infant dependence from the mother across development.

Early Left-Planum Temporale Asymmetry in newborn monkeys (Papio anubis): A longitudinal structural MRI study at two stages of development.

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.

Beyond MRI: on the scientific value of combining non-human primate neuroimaging with metadata.

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.

Strengths and challenges of longitudinal non-human primate neuroimaging.

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.

Increased performance in juvenile baboons is consistent with ontogenetic changes in morphology.

OBJECTIVES: In many primates, the greater proportion of climbing and suspensory behaviors in the juvenile repertoire likely necessitates good grasping capacities. Here, we tested whether very young individuals show near-maximal levels of grasping strength, and whether such an early onset of grasping performance could be explained by ontogenetic variability in the morphology of the limbs in baboons. MATERIAL AND METHODS: We quantified a performance trait, hand pull strength, at the juvenile and adult stages in a cross-sectional sample of 15 olive baboons (Papio anubis). We also quantified bone dimensions (i.e., lengths, widths, and heights) of the fore- (n = 25) and hind limb (n = 21) elements based on osteological collections covering the whole development of olive baboons. RESULTS: One-year old individuals demonstrated very high pull strengths (i.e., 200% of the adult performance, relative to body mass), that are consistent with relatively wider phalanges and digit joints in juveniles. The mature proportions and shape of the forelimb elements appeared only at full adulthood (i.e., ≥4.5 years), whereas the mature hind limb proportions and shape were observed much earlier during development. DISCUSSION: These changes in limb performance and morphology across ontogeny may be explained with regard to behavioral transitions that olive baboons experience during their development. Our findings highlight the effect of infant clinging to mother, an often-neglected feature when discussing the origins of grasping in primates. The differences in growth patterns, we found between the forelimb and the hind limb further illustrate their different functional roles, having likely evolved under different ecological pressures (manipulation and locomotion, respectively).

Gestural communication in olive baboons (Papio anubis): repertoire and intentionality.

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.

The baboon: A model for the study of language evolution.

Comparative research on the origins of human language often focuses on a limited number of language-related cognitive functions or anatomical structures that are compared across species. The underlying assumption of this approach is that a single or a limited number of factors may crucially explain how language appeared in the human lineage. Another potentially fruitful approach is to consider human language as the result of a (unique) assemblage of multiple cognitive and anatomical components, some of which are present in other species. This paper is a first step in that direction. It focuses on the baboon, a non-human primate that has been studied extensively for years, including several brain, anatomical, cognitive and cultural dimensions that are involved in human language. This paper presents recent data collected on baboons regarding (1) a selection of domain-general cognitive functions that are core functions for language, (2) vocal production, (3) gestural production and cerebral lateralization, and (4) cumulative culture. In all these domains, it shows that the baboons share with humans many cognitive or brain mechanisms which are central for language. Because of the multidimensionality of the knowledge accumulated on the baboon, that species is an excellent nonhuman primate model for the study of the evolutionary origins of language.

Manipulating social cues in baboon gesture learning: what does it tell us about the evolution of communication?

Reading the attentional state of an audience is crucial for effective intentional communication. This study investigates how individual learning experience affects subsequent ability to tailor gestural communication to audience visual attention. Olive baboons were atypically trained to request food with gestures by a human standing in profile, while not having access to her face. They were tested immediately after training, and then 1 year later in conditions that varied the human's cues to attention. In immediate testing, these baboons (profile group baboons) gestured towards untrained cues regardless of their relevance for visual communication. They were also less discriminant towards trained versus untrained cues than baboons trained by a human facing them (face group baboons, tested in Bourjade et al. Anim Behav 87:121-128; Bourjade et al., Anim Behav 87:121-128, 2014). In delayed testing, the number of gestures towards meaningful untrained cues increased and profile group baboons discriminated the orientation of the human body, a conspicuous proxy of visual attention. Our results provide support for the primary interplay between implicit learning and systematically reinforced associations made through explicit training in the scaffolding of intentional gesturing tuned to audience attention.

Left Brain Asymmetry of the Planum Temporale in a Nonhominid Primate: Redefining the Origin of Brain Specialization for Language.

The planum temporale (PT) is a critical region of the language functional network in the human brain showing a striking size asymmetry toward the left hemisphere. Historically considered as a structural landmark of the left-brain specialization for language, a similar anatomical bias has been described in great apes but never in monkeys-indicating that this brain landmark might be unique to Hominidae evolution. In the present in vivo magnetic resonance imaging study, we show clearly for the first time in a nonhominid primate species, an Old World monkey, a left size predominance of the PT among 96 olive baboons (Papio anubis), using manual delineation of this region in each individual hemisphere. This asymmetric distribution was quasi-identical to that found originally in humans. Such a finding questions the relationship between PT asymmetry and the emergence of language, indicating that the origin of this cerebral specialization could be much older than previously thought, dating back, not to the Hominidae, but rather to the Catarrhini evolution at the common ancestor of humans, great apes and Old World monkeys, 30-40 million years ago.

Genetic Factors and Orofacial Motor Learning Selectively Influence Variability in Central Sulcus Morphology in Chimpanzees (Pan troglodytes).

Captive chimpanzees (Pan troglodytes) have been shown to learn the use of novel attention-getting (AG) sounds to capture the attention of humans as a means of requesting or drawing their attention to a desired object or food. There are significant individual differences in the use of AG sounds by chimpanzees and, here, we examined whether changes in cortical organization of the central sulcus (CS) were associated with AG sound production. MRI scans were collected from 240 chimpanzees, including 122 that reliably produced AG sounds and 118 that did not. For each subject, the depth of CS was quantified along the superior-inferior plane with specific interest in the inferior portion corresponding to the region of the motor cortex where the mouth and orofacial movements are controlled. Results indicated that CS depth in the inferior, but not superior, portion was significantly greater in chimpanzees that reliably produced AG sounds compared with those who did not. Quantitative genetic analyses indicated that overall CS surface area and depth were significantly heritable, particularly in the superior regions, but less so in the inferior and central portions. Further, heritability in CS depth was altered as a function of acquisition of AG sounds. The collective results suggest that learning to produce AG sounds resulted in region-specific cortical reorganization within the inferior portion of the CS, a finding previously undocumented in chimpanzees or any nonhuman primate.SIGNIFICANCE STATEMENT Recent studies in chimpanzees (Pan troglodytes) have shown that some can learn to produce novel sounds by configuring different orofacial movement patterns and these sounds are used in communicatively relevant contexts. Here, we examined the neuromorphological correlates in the production of these sounds in chimpanzees. We show that chimpanzees that have learned to produce these sounds show significant differences in central sulcus (CS) morphology, particularly in the inferior region. We further show that overall CS morphology and regions within the superior portion are significantly heritable, whereas central and inferior portions of the CS are not. The collective findings suggest chimpanzees exhibit cortical plasticity in regions of the brain that were central to the emergence of speech functions in humans.

The average baboon brain: MRI templates and tissue probability maps from 89 individuals.

The baboon (Papio) brain is a remarkable model for investigating the brain. The current work aimed at creating a population-average baboon (Papio anubis) brain template and its left/right hemisphere symmetric version from a large sample of T1-weighted magnetic resonance images collected from 89 individuals. Averaging the prior probability maps output during the segmentation of each individual also produced the first baboon brain tissue probability maps for gray matter, white matter and cerebrospinal fluid. The templates and the tissue probability maps were created using state-of-the-art, freely available software tools and are being made freely and publicly available: http://www.nitrc.org/projects/haiko89/ or http://lpc.univ-amu.fr/spip.php?article589. It is hoped that these images will aid neuroimaging research of the baboon by, for example, providing a modern, high quality normalization target and accompanying standardized coordinate system as well as probabilistic priors that can be used during tissue segmentation.

Gaze following in baboons (Papio anubis): juveniles adjust their gaze and body position to human's head redirections.

Gaze following, the ability to follow the gaze of other individuals, has been widely studied in non-human primate species, mostly in adult individuals. Yet, the literature on gaze following revealed a quite variability across the different findings, some of it might reflect true inter-species differences, while others might be related to methodological differences, or to an underestimation of the factors involved in the expression of gaze following. In the current study, we tested 54 captive olive baboons (Papio anubis), housed in social groups, to assess how juvenile and adult baboons would spontaneously react to a sudden change in the direction of a human experimenter's head. First, our results showed that juveniles, more than adult baboons, co-oriented their gaze with the experimenter's gaze. We also observed a strong habituation effect in adult baboons but not in juveniles, as the adults' response vanished at the second exposure to a change of direction of the experimenter's head. Second, our results showed that juveniles subsequently adopted an original strategy when the experimenter's head indicated some new directions: they reliably adjusted their spatial body position to keep a gaze contact with the experimenter's line of sight. We discussed how the age class and the individual expertise of the baboons could lead to some modulations in terms of attentiveness, motivation, or cognitive abilities, and thus likely influence gaze following.

Training experience in gestures affects the display of social gaze in baboons' communication with a human.

Gaze behaviour, notably the alternation of gaze between distal objects and social partners that accompanies primates' gestural communication is considered a standard indicator of intentionality. However, the developmental precursors of gaze behaviour in primates' communication are not well understood. Here, we capitalized on the training in gestures dispensed to olive baboons (Papio anubis) as a way of manipulating individual communicative experience with humans. We aimed to delineate the effects of such a training experience on gaze behaviour displayed by the monkeys in relation with gestural requests. Using a food-requesting paradigm, we compared subjects trained in requesting gestures (i.e. trained subjects) to naïve subjects (i.e. control subjects) for their occurrences of (1) gaze behaviour, (2) requesting gestures and (3) temporal combination of gaze alternation with gestures. We found that training did not affect the frequencies of looking at the human's face, looking at food or alternating gaze. Hence, social gaze behaviour occurs independently from the amount of communicative experience with humans. However, trained baboons-gesturing more than control subjects-exhibited most gaze alternation combined with gestures, whereas control baboons did not. By reinforcing the display of gaze alternation along with gestures, we suggest that training may have served to enhance the communicative function of hand gestures. Finally, this study brings the first quantitative report of monkeys producing requesting gestures without explicit training by humans (controls). These results may open a window on the developmental mechanisms (i.e. incidental learning vs. training) underpinning gestural intentional communication in primates.

Baboons (Papio papio), but not humans, break cognitive set in a visuomotor task.

Cognitive set can be both helpful and harmful in problem solving. A large set of similar problems may be solved mechanically by applying a single-solution method. However, efficiency might be sacrificed if a better solution exists and is overlooked. Despite half a century of research on cognitive set, there have been no attempts to investigate whether it occurs in nonhuman species. The current study utilized a nonverbal, computer task to compare cognitive set between 104 humans and 15 baboons (Papio papio). A substantial difference was found between humans' and baboons' abilities to break cognitive set. Consistent with previous studies, the majority of humans were highly impaired by set, yet baboons were almost completely unaffected. Analysis of the human data revealed that children (aged 7-10) were significantly better able to break set than adolescents (11-18) and adults (19-68). Both the evolutionary and developmental implications of these findings are discussed.

Evolution of the central sulcus morphology in primates.

The central sulcus (CS) divides the pre- and postcentral gyri along the dorsal-ventral plane of which all motor and sensory functions are topographically organized. The motor-hand area of the precentral gyrus or KNOB has been described as the anatomical substrate of the hand in humans. Given the importance of the hand in primate evolution, here we examine the evolution of the motor-hand area by comparing the relative size and pattern of cortical folding of the CS surface area from magnetic resonance images in 131 primates, including Old World monkeys, apes and humans. We found that humans and great apes have a well-formed motor-hand area that can be seen in the variation in depth of the CS along the dorsal-ventral plane. We further found that great apes have relatively large CS surface areas compared to Old World monkeys. However, relative to great apes, humans have a small motor-hand area in terms of both adjusted and absolute surface areas.

Why vocal production of atypical sounds in apes and its cerebral correlates have a lot to say about the origin of language.

Ackermann et al. mention the "acquisition of species-atypical sounds" in apes without any discussion. In our commentary, we demonstrate that these atypical sounds in chimpanzees not only include laryngeal sounds, but also have a major significance regarding the origins of language, if we consider looking at their context of use, their social properties, their relations with gestures, their lateralization, and their neurofunctional correlates as well.

Planum temporale asymmetry in newborn monkeys predicts the future development of gestural communication's handedness.

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.