Broca’s area and its left hemispheric specialisation has historically been considered as the centre of speech production. Even if such a modular conception of language's neural bases was questioned by models of plastic and large distributed networks (Friederici, 2017; Hickok and Poeppel, 2007), it is still well acknowledged that Broca’s area remains a key node for language specialisation within this neural distributed network. Complementary work thereby highlighted Broca’s area as an interface between speech and multimodal motor integration including gesture and mouth mouvements (Gentilucci and Dalla Volta, 2008). Broca’s area is also known for its involvement in motor planning, sequential, and hierarchical organization of behaviours, such as linguistic grammar or tool use and tool making (Gentilucci and Dalla Volta, 2008; Koechlin and Jubault, 2006; Stout et al., 2015; Corballis, 2015; Wakita, 2014). This body of work raises evolutionary questions about the role of the motor system and gestural communication in language origins and its brain specialisation. Therefore, a growing number of researchers proposed that language organisation took some of its phylogenetical roots into a gestural system across primate evolution (Gentilucci and Dalla Volta, 2008; Corballis, 2015; Tomasello, 2008). Consequently, whereas comparative language research has focused on the potential continuities across primate brain circuitry (e.g., Balezeau et al., 2020; Becker et al., 2022) or vocal and auditory systems (e.g. Boë et al., 2017; Jarvis, 2019; Wilson et al., 2017), the research on gestural communication in apes and monkeys has historically shown a significant interest within this evolutionary framework.

A large body of nonhuman primate studies has documented some continuities of the communicative gestural system with several key features of human language such as intentionality, referentiality, learning flexibility, and lateralisation (e.g. Tomasello, 2008; Meguerditchian and Vauclair, 2014; Molesti et al., 2020). About manual lateralisation specifically, studies in baboons and great apes have indeed shown that communicative manual gesturing elicited stronger right-hand use in comparison to non-communicative manipulative actions at a populational-level (reviewed in: Meguerditchian et al., 2013). In addition, at the individual level, a double dissociation concerning the type of handedness has been documented between gestural communication and object manipulation, showing that primates classified as right-handed for communicative gesture are not especially classified as right-handed for object manipulation and vice versa (Meguerditchian and Vauclair, 2006). Those behavioural findings in different primate species suggested a specific lateralised system for communicative gestures, which might be different from the one involves in handedness for object manipulation. This is consistent with human literature showing that typical object-manipulation handedness measures turned out to be a rather poor marker of language lateralisation (Fagard, 2013), as most left-handers (78%) also show left-hemisphere dominance for language (Knecht et al., 2000; Mazoyer et al., 2014), just like right-handed people. In both humans and nonhuman primates, direction of handedness for object manipulation was found associated to contralateral asymmetries of the motor hand area within the Central sulcus (e.g. humans: Amunts et al., 2000; Cykowski et al., 2008; chimpanzees: Hopkins and Cantalupo, 2004; Dadda et al., 2006; Baboons: Margiotoudi et al., 2019; Capuchin monkeys: Phillips and Sherwood, 2005; Squirrel monkeys: Nudo et al., 1992). In fact, it has recently been demonstrated that the neural substrates of typical handedness measures and language brain organisation might be not related but rather independent from each other (Groen et al., 2013; Ocklenburg et al., 2014; Häberling et al., 2016; Labache et al., 2020).

Whether gestural communication’s handedness in humans is a better predictor of language lateralisation and is thus different than typical handedness measures remain unclear. Nevertheless, several studies in humans are supporting this hypothesis. In early human development, the degree of right-handedness for preverbal gestures is more pronounced at a populational-level than handedness for manipulation (Blake et al., 1994; Bonvillian et al., 1997; see also Fagard, 2013; Cochet and Vauclair, 2010) and increases when the lexical spurt occurs in children contrary to manipulation handedness (Cochet et al., 2011). Moreover, further work showed Broca's activation in the left hemisphere also for sign language production including manual and oro-facial gestures (Emmorey et al., 2004; MacSweeney et al., 2008).

Given such potential lateralisation links between gesture and language in humans, it is thus not excluded that the specific lateralisation’s signature found for communicative gestures in nonhuman primates might reflect evolutionary continuities with frontal hemispheric specialisation for speech/gesture integration. This hypothesis might be relevant to investigate given brain studies in nonhuman primates have shown gross left-hemispheric asymmetries of homologous language areas at a populational level that are similar to the ones described in humans (e.g., Geschwind and Levitsky, 1968; Keller et al., 2009): In particular Broca’s homologue in great apes (Cantalupo and Hopkins, 2001; Graïc et al., 2020) as well as the Planum Temporale in great apes and even in baboons, an Old World monkey species, in both adult and newborns (Gannon et al., 1998; Marie et al., 2018; Becker et al., 2021a; Becker et al., 2021b).

For Old World monkeys specifically, no study regarding structural asymmetry for Broca’s homologue has been investigated. One reason is that determining this area in monkeys is particularly challenging in comparison to apes. In fact, the inferior precentral sulcus, the inferior frontal sulcus and the fronto-orbital sulcus, which are common borders of Broca’s homologue in apes (Cantalupo and Hopkins, 2001), are absent in monkeys and thus delimitation is not trivial. Nevertheless, all the detailed cytoarchitectonic studies addressing the Broca’s homologue within the frontal lobe in Old World monkeys (i.e. in mostly macaques but also in baboons) – and its two components Area 44 and 45 – pointed towards the same sulcus of interest as the epicentre of this region: the mid-ventral and ventral portion of the Inferior Arcuate sulcus (IA sulcus). The IA sulcus is considered homologue to the ascending branch of the inferior precentral sulcus (Amiez and Petrides, 2009) which delimits Broca’s area posteriorly in humans and great apes. In monkeys, Area 45 homologue sits in the anterior bank of the ventral IA sulcus (Petrides et al., 2005). In contrast, Area 44 homologue might be located in the fundus and the posterior bank of the ventral IA sulcus in monkeys (Petrides et al., 2005), which overlaps with F5 region related to the mirror neuron system (Belmalih et al., 2009; Rizzolatti and Fogassi, 2014). Electric stimulation in the fundus of the ventral IA sulcus elicited oro-facial and finger mouvements in macaques (Petrides et al., 2005). Concerning baboons specifically, a cytoarchitectonic study (Watanabe-Sawaguchi et al., 1991) showed similarities to the macaque frontal lobe organisation given Area 45 anteriorly to the IA sulcus, even if Area 44 was not described (Petrides et al., 2005; Belmalih et al., 2009; Rizzolatti and Fogassi, 2014; Watanabe-Sawaguchi et al., 1991). Therefore, in the absence of the usual Broca’s sulcal borders found in apes, the depth of the ventral part of the IA sulcus constitutes the only critical neuroanatomical marker for delimiting the border and the surface of Broca’s homologue in monkeys.

In sum, within the framework of the origin of hemispheric specialisation for language, most comparative works in nonhuman primates focused on population-level asymmetry for either brain or communicative behaviours. Those studies have reported similar population-level leftward brain asymmetry for key language homologue regions (Gannon et al., 1998; Cantalupo and Hopkins, 2001; Marie et al., 2018; Becker et al., 2021a; Becker et al., 2021b) or similar populational-level right-handedness for communicative gestures (reviewed in: Meguerditchian et al., 2013). Nevertheless, to test potential phylogenetic continuities, this approach suffered from lack of studies investigating the direct behavioural/brain correlates at the individual-levels.

In the present in-vivo MRI study conducted in 50 baboons (Papio anubis), we have (1) measured the inter-hemispheric asymmetries of the IA sulcus’ depth – from its dorsal to its most ventral portion among subjects for which the Central sulcus depth measure was available from a previous study (Margiotoudi et al., 2019) (2) as well as its potential links with direction and degree of communicative gesture’s handedness in comparison to handedness for manipulative actions as measured with a bimanual tube task (see Hopkins, 1995). In other words, we tested specifically whether the depth asymmetry of the most ventral Inferior Arcuate sulcus’ portion (ventral IA sulcus, i.e. the Broca’s homologue) – but not the Central sulcus – was exclusively associated with communicative gestures’ lateralisation.

Between baboons communicating preferentially with the right hand versus the ones with the left hand, we found significant contralateral differences of depth asymmetries in the ventral portion of the IA sulcus (i.e., from the mid-ventral IA position to the most ventral IA sulcus portion, namely from contiguous positions 65–95 out of the 99 segmented positions of the entire IA sulcus) according to a cluster-based permutation test (p < .01, t-value clustermass = 76.16, for p < .01 a clustermass of 65.28 was needed, see Maris and Oostenveld, 2007). In other words, the 28 baboons using preferentially their right hand for communicative gestures showed more leftward IA sulcus depth asymmetry at this cluster than the 22 ones using preferentially their left-hand. In contrast, for non-communicative manipulative actions, we found no significant difference of sulcus depth asymmetries between the left- (N = 22) versus right-handed (N = 28) groups concerning any portion of the IA sulcus, according to a cluster-based permutation test (p > .10) (Figure 1).

Figure 1

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In addition, after calculating the AQ score per subject representing the sulcus depth asymmetry of the whole ‘Broca’s cluster’ (i.e. from the sum of the IA sulcus depths from positions 65–95 in the left hemisphere and the sum of IA sulcus depths from position 65–95 in the right hemisphere), we found a significant negative correlation between individual AQ depth values of the Broca’s cluster (i.e. from positions 65–95) and individual handedness degree for communication (HI): r(48) = –.337; p < .05 (i.e. The stronger the hand preference is for one hand, the deeper is the IA sulcus asymmetry from positions 65 to 95 in the contralateral hemisphere) (Figure 2A). In contrast, AQ depth values of the Broca’s cluster did not show significant correlation with HI for non-communicative actions (r(48) = –.037; p ≈ 1) (Figure 2B). Using the cocor package in R (Diedenhofen and Musch, 2015), a comparison between these two overlapping correlations based on dependent groups showed a significant difference between the two correlations (p < .05).

Figure 2

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When comparing with the control sulcus of interest, the Central sulcus related to the primary motor cortex, an opposite effect was found between handedness for manipulative actions and hand preferences for communicative gesture. We found no significant difference of sulcus depth asymmetries regarding communicative gestures. In contrast, Margiotoudi et al., 2019 reported that the CS presented a contralateral asymmetry at continuous positions 56–60 (labelled as the ‘Motor-hand area’s cluster’) for non-communicative manipulative actions, after permutation tests for correction (Figure 1).

Finally, we conducted a mixed-model analysis of variance with AQs depth values for the IA sulcus ‘Broca’s cluster’ and for the Central sulcus ‘Motor hand area’s cluster’ (AQ derived from continuous positions 56–60, see Margiotoudi et al., 2019) serving as the repeated measure while communication handedness (left- versus right-handed) and action handedness (left- versus right-handed) were between-group factors. The mixed-model analysis of variance demonstrated a significant main effect on the AQ scores for communication handedness (F1_,46 = 14.08, p < .01) and for action handedness (F_1,46 = 4,1, p < .05).

The results of the study are straightforward. We showed that the IA sulcus left- or rightward depth asymmetry at its mid-ventral and ventral portion (labelled as the ‘Broca cluster’) is associated exclusively with contralateral direction (left-/right-hand) of communicative manual gestures’ lateralisation in baboons but not handedness for non-communicative actions. Building upon these first results, we also found a significant negative correlation between the Handedness Index (HI) values for communicative gestures and the Asymmetric Quotient (AQ) depth values of the IA sulcus ‘Broca's cluster’, suggesting that the contralateral links between handedness for gestural communication and depth asymmetries at the most ventral portion of the IA sulcus is evident not only at a qualitative level but also at a quantitative level as well. In other words, individuals with a stronger degree of manual lateralisation for communicative gesture have greater IA sulcus depth asymmetries at this ventral cluster in the hemisphere contralateral to their preferred hand for communication. The ventral positions of such sulcal depth asymmetries are clearly at a crossroad of Broca-related frontal regions including the fundus of the sulcus, Area 44 (Petrides et al., 2005), the anterior bank, Area 45 (Petrides et al., 2005), the posterior bank and ventral F5 or granual frontal area (GrF) (Belmalih et al., 2009; Rizzolatti and Fogassi, 2014). Since the sulcus' depth might reflect a gyral surface and its underlying grey matter volume, future work of delineating and quantifying grey matter of the ventral IA sulcus would help determining which of those sub-regions of the Broca homologue is driving the asymmetry specifically, for instance by VBM methods.

Whereas handedness for manipulative actions in baboons was previously found related to the motor cortex asymmetry within the Central sulcus (Margiotoudi et al., 2019), our present findings report the first evidence in monkeys that the neurostructural lateralisation’s landmark of communicative gesture is located in a frontal region, related to Broca's homologue. Such a contrast of results between manipulation and communication found at the cortical level is consistent with what was found at the behavioural level in studies showing that communicative gesture in baboons and chimpanzees elicited specific and independent patterns of manual lateralisation in comparison to non-communicative manipulative actions (Meguerditchian and Vauclair, 2009; Meguerditchian et al., 2010). Therefore, it provides additional support to the hypothesis suggesting that gestural communication’s lateralisation in nonhuman primates might be, just as language brain organisation in human (see Häberling et al., 2016), related to a different lateralised neural system than handedness for pure manipulative action. Its specific correlates with Broca's homologue’s lateralisation is also consistent with what was found in our closest relatives, the chimpanzee (Taglialatela et al., 2006; Meguerditchian et al., 2012).

Regarding Broca’s area in humans, very recently, a functional segregation was proposed with Broca’s anterior part implicated in language syntax and its posterior part exclusively implicated in motor actions (Zaccarella et al., 2021). The authors argued that action and language meet at this interface. In an evolutionary perspective we propose therefore that the intentionality of primate’s communicative gesture might account for this hypothesised functional interface of actions and language prerequisites, nested inside the monkeys’ Broca’s homologue (see also: Rizzolatti and Craighero, 2004Arbib et al., 2008; Rizzolatti and Fogassi, 2014; Corballis, 2015). In addition, in macaques Broca’s homologue, neuronal recordings showed populations of specific neurons activated for both volitional vocal and manual actions (Gavrilov and Nieder, 2021).

The articulation of our results with this recent literature suggests that gestural communication may be a compelling modality for one of the multimodal evolutionary roots of the typical multimodal language system in humans and its hemispheric specialisation. It is thus not excluded that language-related frontal lateralisation might be much older than previously thought and inherited from a gestural communicative system dating back, not to Hominid origins, but rather to the common ancestor of humans, great apes and Old World monkeys, 25–35 million years ago.

The behavioural, neuro-anatomical and statistic code data that support the findings of this study are available in "OSF Storage" with the identifier https://doi.org/10.17605/OSF.IO/DPXS5 and the URL https://osf.io/dpxs5/?viewonly=f406ad972edd43e485e5e4076bae0f78.

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Author details

1. Yannick Becker

   1. Laboratoire de Psychologie Cognitive, CNRS, Aix-Marseille University, Marseille, France
   2. Centre IRMf Institut de Neurosciences de la Timone CNRS, Aix-Marseille University, Marseille, France

   Contribution

   Data curation, Formal analysis, Writing - original draft

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-9728-8316

2. Nicolas Claidière

   Laboratoire de Psychologie Cognitive, CNRS, Aix-Marseille University, Marseille, France

   Contribution

   Data curation, Formal analysis

   Competing interests

   No competing interests declared

3. Konstantina Margiotoudi

   Laboratoire de Psychologie Cognitive, CNRS, Aix-Marseille University, Marseille, France

   Contribution

   Formal analysis

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-9505-3978

4. Damien Marie

   Laboratoire de Psychologie Cognitive, CNRS, Aix-Marseille University, Marseille, France

   Contribution

   Data curation, Formal analysis

   Competing interests

   No competing interests declared

5. Muriel Roth

   Centre IRMf Institut de Neurosciences de la Timone CNRS, Aix-Marseille University, Marseille, France

   Contribution

   Resources, designed MRI sequences

   Competing interests

   No competing interests declared

6. Bruno Nazarian

   Centre IRMf Institut de Neurosciences de la Timone CNRS, Aix-Marseille University, Marseille, France

   Contribution

   Resources, designed the baboons' monitoring programs

   Competing interests

   No competing interests declared

7. Jean-Luc Anton

   Centre IRMf Institut de Neurosciences de la Timone CNRS, Aix-Marseille University, Marseille, France

   Contribution

   Resources, coordinated the MRI sessions

   Competing interests

   No competing interests declared

8. Olivier Coulon

   Institut de Neurosciences de la Timone CNRS, Aix-Marseille University, Marseille, France

   Contribution

   Methodology, Resources, Software, Writing - review and editing, designed the sulcus parametrization tool

   Competing interests

   No competing interests declared

9. Adrien Meguerditchian

   1. Laboratoire de Psychologie Cognitive, CNRS, Aix-Marseille University, Marseille, France
   2. Station de Primatologie CNRS-CELPHEDIA, Marseille, France

   Contribution

   Conceptualization, Funding acquisition, Investigation, Methodology, Project administration, Supervision, Writing - original draft, Writing - review and editing, supervised the MRI acquisitions

   For correspondence

   adrien.meguerditchian@univ-amu.fr

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-3754-6747

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