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.

The relevance of the unique anatomy of the human prefrontal operculum to the emergence of speech.

Identifying the evolutionary origins of human speech remains a topic of intense scientific interest. Here we describe a unique feature of adult human neuroanatomy compared to chimpanzees and other primates that may provide an explanation of changes that occurred to enable the capacity for speech. That feature is the Prefrontal extent of the Frontal Operculum (PFOp) region, which is located in the ventrolateral prefrontal cortex, adjacent and ventromedial to the classical Broca's area. We also show that, in chimpanzees, individuals with the most human-like PFOp, particularly in the left hemisphere, have greater oro-facial and vocal motor control abilities. This critical discovery, when combined with recent paleontological evidence, suggests that the PFOp is a recently evolved feature of human cortical structure (perhaps limited to the genus Homo) that emerged in response to increasing selection for cognitive and motor functions evident in modern speech abilities.

A revised perspective on the evolution of the lateral frontal cortex in primates.

Detailed neuroscientific data from macaque monkeys have been essential in advancing understanding of human frontal cortex function, particularly for regions of frontal cortex without homologs in other model species. However, precise transfer of this knowledge for direct use in human applications requires an understanding of monkey to hominid homologies, particularly whether and how sulci and cytoarchitectonic regions in the frontal cortex of macaques relate to those in hominids. We combine sulcal pattern analysis with resting-state functional magnetic resonance imaging and cytoarchitectonic analysis to show that old-world monkey brains have the same principles of organization as hominid brains, with the notable exception of sulci in the frontopolar cortex. This essential comparative framework provides insights into primate brain evolution and a key tool to drive translation from invasive research in monkeys to human applications.

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.

Cerebral Activity in Female Baboons (Papio anubis) During the Perception of Conspecific and Heterospecific Agonistic Vocalizations: a Functional Near Infrared Spectroscopy Study.

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. Supplementary Information: The online version contains supplementary material available at 10.1007/s42761-022-00164-z.

Sequence organization and embodied mutual orientations: openings of social interactions between baboons.

Human interactions are organized in sequence, which is a key component of Levinson's 'interaction engine.' Referring back to the field where it originated, conversation analysis, we discuss its relevance within the interaction engine, before moving on to show how sequence organization is actually oriented to not only humans in social interaction, but also to non-human animals. On the basis of video-recorded encounters between baboons (Papio anubis), we study canonical sequences constituting openings and, within them, greetings. Openings are the locus where future interactants adjust to each other to coordinately enter in interaction, thus achieving a common definition of their context, activity, and relationships. The analysis shows that the ways individuals spatially approach each other provide systematic interactional affordances for how the first sequences of actions in the opening are formatted, initiated, and responded to. Adopting sequential multimodal analysis, we demonstrate how participants orient to central features of sequence organization-its sequential implicativeness and the expectations it produces-building on them their interpretations of others' actions, their responsivity, and their mutual understanding of the ongoing course of action as it unfolds. This paves the way for further reflections on the pervasiveness of the interactional engine in human and non-human primate communication. This article is part of the theme issue 'Revisiting the human 'interaction engine': comparative approaches to social action coordination'.

Broca's cerebral asymmetry reflects gestural communication's lateralisation in monkeys (Papio anubis).

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.

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.

Planum temporale grey matter volume asymmetries in newborn monkeys (Papio anubis).

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.

The Arcuate Fasciculus and language origins: Disentangling existing conceptions that influence evolutionary accounts.

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 more continuous AF evolution across primates.

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.

Corpus callosum morphology across the lifespan in baboons (Papio anubis): A cross-sectional study of relative mid-sagittal surface area and thickness.

The corpus callosum enables integration and coordination of cognitive processing between the cerebral hemispheres. In the aging human brain, these functions are affected by progressive axon and myelin deteriorations, reflected as atrophy of the midsagittal corpus callosum in old age. In non-human primates, these degenerative processes are less pronounced as previous morphometric studies on capuchin monkey, rhesus monkeys, and chimpanzees do not find old-age callosal atrophy. In the present study, we extend these previous findings by studying callosal development of the olive baboon (Papio anubis) across the lifespan and compare it to chimpanzee and human data. For this purpose, total relative (to forebrain volume) midsagittal area, subsectional area, and regional thickness of the corpus callosum were assessed in 91 male and female baboons using non-invasive MRI-based morphometry. The studied age range was 2.5-26.6 years and lifespan trajectories were fitted using general additive modelling. Relative area of the total and anterior corpus callosum showed a positive linear trajectory. That is, both measures increased slowly but continuously from childhood into old age, and no decline was observed in old age. Thus, comparable with all other non-human primates studied to-date, baboons do not show callosal atrophy in old age. This observation lends supports to the notion that atrophy of the corpus callosum is a unique characteristic of human brain aging.

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).

Validating the use of functional Near-Infrared Spectroscopy in monkeys: The case of brain activation lateralization in Papio anubis.

Hemispheric asymmetries have long been seen as characterizing the human brain; yet, an increasing number of reports suggest the presence of such brain asymmetries in our closest primate relatives. However, most available data in non-human primates have so far been acquired as part of neurostructural approaches such as MRI, while comparative data in humans are often dynamically acquired as part of neurofunctional studies. In the present exploratory study in baboons (Papio anubis), we tested whether brain lateralization could be recorded non-invasively using a functional Near-Infrared Spectroscopy (fNIRS) device in two contexts: motor and auditory passive stimulations. Under light propofol anaesthesia monitoring, three adult female baboons were exposed to a series of (1) left- versus right-arm passive movement stimulations; and (2) left- versus right-ear versus stereo auditory stimulations while recording fNIRS signals in the related brain areas (i.e., motor central sulcus and superior temporal cortices respectively). For the sensorimotor condition our results show that left-arm versus right-arm stimulations induced typical contralateral difference in hemispheric activation asymmetries in the three subjects. For the auditory condition, we also revealed typical human-like patterns of hemispheric asymmetries in one subject, namely a leftward lateralization for right ear stimulations for all three channels. Overall, our findings support the use of fNIRS to investigate brain processing in non-human primates from a functional perspective, opening the way for the development of non-invasive procedures in non-human primate brain research.

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.

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.

Author Correction: Sulcal organization in the medial frontal cortex provides insights into primate brain evolution.

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

Human-like maternal left-cradling bias in monkeys is altered by social pressure.

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.

Optional-switch cognitive flexibility in primates: Chimpanzees' (Pan troglodytes) intermediate susceptibility to cognitive set.

Within human problem-solving, the propensity to use a familiar approach, rather than switch to a more efficient alternative is pervasive. This susceptibility to "cognitive set" prevents optimization by biasing response patterns toward known solutions. In a recent study, which used a nonverbal touch screen task, baboons exhibited a striking ability to deviate from their learned strategy to use a more efficient shortcut. Humans, on the other hand, displayed the opposite response pattern and almost exclusively used a less efficient, but familiar, response. In the current study, we sought to further explore variation in susceptibility to cognitive set within the primate lineage by conducting the Learned Strategy-Direct Strategy task with 10 chimpanzees (Pan troglodytes). Using multilevel multinomial modeling, we found that chimpanzees' shortcut use was intermediate to baboons' and humans'. However, unlike either baboons or humans, there was pronounced inter- and intraindividual variability in chimpanzees' shortcut use. Additionally, a subset of chimpanzees employed a unique solution, wherein they switched strategies midtrial. Further, we found that chimpanzees did not exhibit switch costs when switching between the learned strategy and the shortcut, but humans did. We propose that differences in abstract rule encoding may underlie differences in susceptibility to cognitive set on the Learned Strategy-Direct Strategy task within the primate lineage. (PsycINFO Database Record (c) 2020 APA, all rights reserved).