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

  1. Yannick Becker
  2. Nicolas Claidière
  3. Konstantina Margiotoudi
  4. Damien Marie
  5. Muriel Roth
  6. Bruno Nazarian
  7. Jean-Luc Anton
  8. Olivier Coulon
  9. Adrien Meguerditchian  Is a corresponding author
  1. Laboratoire de Psychologie Cognitive, CNRS, Aix-Marseille University, France
  2. Centre IRMf Institut de Neurosciences de la Timone CNRS, Aix-Marseille University, France
  3. Institut de Neurosciences de la Timone CNRS, Aix-Marseille University, France
  4. Station de Primatologie CNRS-CELPHEDIA, France

Abstract

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.

Editor's evaluation

This is an elegant, well-designed study, filling a gap regarding structural asymmetries in Broca's area for Old World monkeys. Using a good number of subjects (50 baboons), the authors build on earlier behavioral work pointing to handedness contrasts between communicative vs manipulative gestures, and tested whether the lateralisation effect associated specifically with communicative gestures manifested itself in the depth asymmetry of the ventral Inferior Arcuate [IA] sulcus [Broca's area homologue], but not in the central sulcus. The results of the experiments indeed show a dissociation between communicative vs manipulative gestures, with only the communicative gestures being associated with an IA sulcus depth asymmetry tracking lateralized hand use. The authors point to a captivating phylogenetic continuity between language lateralization in humans and brain asymmetries related to gestures in nonhuman primates.

https://doi.org/10.7554/eLife.70521.sa0

Introduction

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.

Results

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).

Effect of left-/right-hand direction of two handedness types (communication vs action) on neuroanatomical sulcus depth asymmetries (IA sulcus vs Central sulcus).

Left panel: Pictures of the two types of handedness measures in baboons. ‘Communication Handedness’: a ‘Handslap’ communicative gesture in a juvenile male; ‘Action Handedness’: the non-communicative bimanual coordinated ‘tube task’ performed by an adult male. Top panel: 3-D brain representation from BrainVisa software of the baboon’s left hemisphere, including the IA sulcus; and the Central sulcus with the portion in purple where a significant effect was found in Margiotoudi et al., 2019. Graphs: Sulcus depth’s asymmetry (AQ) comparison between right-handed group versus left-handed group of baboons classified according to the type of manual tasks. Positive Mean Asymmetry Quotient values (AQ) indicate rightward hemispheric asymmetry, negative Mean Asymmetry Quotient values leftward hemispheric asymmetry. +/- SE indicated the Standard Error. (A) IA sulcus AQ between right-handed (N=28) versus left-handed (N=22) groups’ classification for communicative ‘Handslap’ gesture. Significant contralateral AQ difference (p < .01) between the two groups was found for a cluster including positions 65 to 95 (highlighted in purple in the graph and the 3D representation of the IA Sulcus). (B) Central Sulcus AQ between right-handed (N=28) versus left-handed (N=22) groups’ classification for non-communicative bimanual coordinated actions. (C) IA sulcus AQ between right-handed (N=28) versus left-handed (N=22) groups’ classification for non-communicative bimanual coordinated actions. (D) Initial graph (Adapted from Figure 2 from Margiotoudi et al., 2019) of the Central Sulcus AQ showing the significant contralateral AQ differences (p < .05) found between the left-handed (N=28) versus right-handed (N=35) groups group for the non-communicative bimanual coordinated actions (Action condition) for positions 56 to 61 (highlighted in purple in the graph and the 3D representation of the Central Sulcus).

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).

Correlation between handedness degree types and the Broca’s cluster’s asymmetry.

(A) Individual handedness degree (HI) for communicative gestures and AQ depth values of the Broca’s cluster (i.e. from positions 65–95) in dark blue dots. Light blue line: Significant negative correlation between HI and AQ. B. Individual handedness degree (HI) for non-communicative manipulative actions (HI) and AQ depth values of the Broca’s cluster (i.e. from positions 65–95) in dark green squares. Light green line (superposing on x axis): Non-significant correlation between HI and AQ.

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 (F1,46 = 4,1, p < .05).

Discussion

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.

Materials and methods

Subjects

Inter-hemispheric asymmetries of the IA sulcus’ depth were quantified from anatomical T1w MRI images in 80 baboons Papio anubis born in captivity and free from developmental or anatomical abnormalities or brain disorders (generation F1, 52 females, 28 males, age range = 7–32 years, mean age (years): M = 17.7, SE = 5.9). Out of this sample, were included only subjects which overlaps with both (1) the sample of subjects for which individual measures of handedness for communicative gestures were available (i.e. hand slapping gesture, Meguerditchian and Vauclair, 2006) and (2) the previous sample of 63 subjects (i.e. 35 right-handed and 28 left-handed) reported in Margiotoudi et al., 2019 for which both Central sulcus depth measures and individual measures of handedness for manipulative actions (i.e. the bimanual tube task, Vauclair et al., 2005) were reported. It resulted a total overlap of 50 baboons (29 females and 21 males, mean age (years): M = 12.3, SE = 5.8) who combined thus the both types of measures of handedness (communication versus manipulation) and the depth measures of the two sulci of interest (IA sulcus and Central sulcus) in the two hemispheres of the brain.

All baboons were housed in social groups at the Station de Primatologie CNRS (UPS 846, Rousset, France; Agreement number for conducting experiments on vertebrate animals: D13-087-7) and have free access to outdoor areas connected to indoor areas. Wooden and metallic, ethologically approved, structures enrich the enclosures. Feeding times are held four times a day with seeds, monkey pellets and fresh fruits and vegetables. Water is available ad libitum. The study was approved by the ‘C2EA-71 Ethical Committee of Neurosciences’ (INT Marseille) under the number APAFIS#13553–201802151547729. The experimental procedure complied with the current French laws and the European directive 86/609/CEE.

Sulcal parametrization

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The IA sulcus and the Central sulcus were extracted from T1w images using the pipeline of the free BrainVisa software (see Mangin et al., 2004 for details of the procedure). The sulcus parametrization tool within the BrainVisa toolbox provides therefore sulcus-based morphometry by subdividing the sulci of each hemisphere into 99 standardized positions from dorsal to ventral sulcus extremities in order to quantify the variation of sulcal depth all across the sulci’s 99 positions (Mangin et al., 2004). This automatic algorithm is free from observer’s judgment. To estimate asymmetries of the sulci’s depth between the two hemispheres an asymmetry quotient (AQ) for each of the 99 sulcal positions AQ = (R – L) / [(R + L × 0.5)] was computed (Margiotoudi et al., 2019). The AQ values vary between –2 and +2 with positive values indicating right-hemispheric lateralisation and negative values indicating left-hemispheric lateralisation.

Behaviour correlate

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For further investigating its potential behavioural correlates, we tested whether the right- versus left-handed groups classified for a given manual task (i.e. gestural communication versus manipulative actions) differed in term of neurostructural depth asymmetries (AQ) within the IA sulcus and the Central sulcus. The two types of handedness measures were previously collected (for communicative gesture: Meguerditchian and Vauclair, 2006; Meguerditchian et al., 2011 for manipulative actions: Vauclair et al., 2005; Molesti et al., 2016).

Communicative gesture was defined as a mouvement of the hand directed to a specific partner or audience in order to affect its behaviour (Molesti et al., 2020). Like in apes, some communicative manual gestures in baboons have been found to share human-like intentional control, referential properties, flexibility of acquisition and of use as well as similar specific pattern of manual lateralisation (reviewed in Tomasello, 2008; Meguerditchian and Vauclair, 2014; Meguerditchian et al., 2013). The present study focused specifically on the ‘Hand slapping’ gesture which was previously found optimal for measuring gestural communication’s lateralisation in this species (Meguerditchian and Vauclair, 2006; Meguerditchian et al., 2011). Indeed, the hand slapping behaviour – a probably innate gestures used by the baboon to threat or intimidate the recipient – is the most common and frequent visual gesture of the repertoire (Molesti et al., 2020) produced intentionally and unimanually in a lateralised manner across similar agonistic contexts and similar emitter’s postures (Meguerditchian et al., 2013). Hand use was recorded in a baboon when slapping or rubbing quickly and repetitively the hand on the ground in direction to a conspecific or a human observer at an out of reach distance. Recorded events were taken from different bouts and not repeated measures from the same bout. As Margiotoudi et al., 2019, in case a subject has been assessed in multiple sessions within 2004–2015, the final classification as right or left-handed was selected based on the session with the most observations, excluding subjects with less than five observations (Mean = 25.98, S.E. = 3.67).

Handedness for manipulative actions was assessed using the well-documented bimanual coordinated ‘Tube task’ (Hopkins, 1995). Hand use was recorded when extracting food with a finger out of a PVC tube hold by the other hand.

The individual handedness index (HI) for a given manual behaviour, or degree of individual manual asymmetry, was calculated based on the formula (#R-#L)/(#R+#L), with #R indicating right hand responses and #L for left hand responses. The HI values vary between –1 and +1 with positive values indicating right hand preference, negative values indicating left hand preference and 0 indicating no preference. The absolute HI score indicate the strength of manual preference.

Among the 50 baboons, for communicative gesture, 22 subjects were thus classified as left-handed, 28 as right-handed following the HI direction. A 51th subject, having a HI score of 0 (i.e. no manual bias), could not be classified in either categories and has been thus excluded from the study. For object-related manipulative actions (i.e. the bimanual tube task), 22 subjects were classified as left-handed, 28 as right-handed as already reported in Margiotoudi et al., 2019 for those 50 overlapping subjects. Among the 50 baboons, 18 subjects switched left-/right-handed categories of hand preference between communicative gesture and manipulative actions (i.e. 9 from left-handed group for gestural communication to right-handed group for manipulative actions, 9 from right-handed group for gestural communication to left-handed group for manipulative actions).

Statistical analysis

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Statistical analysis was conducted using R 3.6.1 by Cluster Mass Permutation tests (Maris and Oostenveld, 2007). First, an assembly of depth asymmetry measures was defined as a ‘cluster’ when continuous significant differences of the same sign across positions were found between groups (two-sided t-tests, Welch corrected for inequality of variance, p < .05). Second, the sum of t-values within each cluster was calculated (the ‘cluster mass’). Next, permutations were conducted for the between individual tests: For a given type of manual behaviour, Left-handed individuals’ AQ values versus Right-handed individuals’ AQ values were randomly redistributed between individuals and the maximum absolute cluster mass was calculated for each randomly permuted set. This procedure was repeated 5000 times and the 99% confidence interval (CI) of the maximum cluster mass was calculated. The clusters in the observed data were considered significant at 1% level if their absolute cluster mass was above the 99% CI of the distribution (i.e. p < .01).

We also performed a linear correlation between (1) the Handedness Index (HI) values for communicative gesture calculated from the 50 individuals and (2) the Asymmetric Quotient (AQ) values of those 50 baboons calculated from the respective left and right ventral IA sulcus’ depth sum of the continuous positions of the cluster for which a significant difference in AQ score is detected by t-test comparison between the right- and left-handed groups. The same procedure was followed for the HI values for non-communicative actions for those 50 individuals.

Data availability

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.

The following data sets were generated

References

    1. Rizzolatti G
    2. Fogassi L
    (2014) The mirror mechanism: recent findings and perspectives
    Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 369:20130420.
    https://doi.org/10.1098/rstb.2013.0420

Decision letter

  1. Timothy E Behrens
    Senior and Reviewing Editor; University of Oxford, United Kingdom
  2. Cedric Boeckx
    Reviewer; ICREA/Universitat de Barcelona, Spain

In the interests of transparency, eLife publishes the most substantive revision requests and the accompanying author responses.

Decision letter after peer review:

Thank you for submitting your article "Broca area homologue's asymmetry reflects gestural communication lateralisation in monkeys (Papio anubis)" for consideration by eLife. Your article has been reviewed by 2 peer reviewers, and the evaluation has been overseen by Ingrid Johnsrude as the Reviewing Editor and Timothy Behrens as the Senior Editor. The following individual involved in review of your submission has agreed to reveal their identity: Cedric Boeckx (Reviewer #1).

The reviewers have discussed their reviews with one another, and the Reviewing Editor has drafted this to help you prepare a revised submission.

Essential revisions:

1) A closer look at the raw depth data (which the authors have openly shared) suggests that variability at the endpoints of the sulcus, thus including the most ventral portion, is larger across subjects compared to the middle portion. Plotting the standard deviations is illustrative in this respect. The employed method does not exclude the possibility that this variability may result from difficulties in measuring the sulcus depth at the endpoints or due to alignments, for example when the sulci have different lengths. It is not clear how you ensured that the length of the sulcus in the left hemisphere overlaps with the one in the right hemisphere. Your method seems to assume that a certain portion of sulcus to the left (a bin) corresponds to the same portion of sulcus to the right. This assumption is fundamental to your analysis, right? In which case, is it possible that the significance observed in a portion of the sulcus is a "misalignment" artifact (the big standard deviations for this portion are concerning in that regard). Would it be possible to back up the work with VBM analysis (eg Backer et al. Brain Struct Funct 2021)? The VBM analysis might not be necessary if they are able to account for the concern in another way.

2) The correlations reported in Figure 2 might suffer from circularity problems, since the analysis is based on the AQ scores derived from the subset of bins which were already shown as significant in Figure 1. This needs to be addressed.

3) What is the evolutionary link between left lateralization for language in humans and gestural communication in the current study? The suggestion of phylogenetic continuity between language-related frontal lateralization and gestural communication seems premature in light of the contralateral effects the authors report. In this regard, while a functional shift from motor regions to the more inferior frontal regions for the gestural communication system may seem relevant, it remains to be elucidated how structural asymmetry-which has been shown to be in both the left and right hemispheres in baboons-can be turn into a fully left-lateralized language system in humans. Views arguing against the gesture-first hypothesis of language evolution should therefore also be considered (e.g., Kendon Psychon Bull Rev 2017).

4. On line 52 they state that research on gestural communication in primates has recently received increased attention. The word 'recently' is inappropriate, since a gestural origin for language has long been entertained. Rephrase this part to acknowledge this research tradition ('gestural protolanguage hypothesis').

5. On line 75-77, the authors list a couple of publications to support the idea that "the neural substrates of typical handedness measures and language brain organisation might be not related but rather independent from each other". There are more recent and comprehensive studies that should be cited in this context (the works of N.Tsourio-Mazoyer and C. Franks).

6. Pointers to the literature on sign language and handedness in the context of gestural communication and language lateralization (line 78 et seq.) would be a helpful addition.

7. The end of the Discussion section could be better articulated. Lines 352-354 should be expanded upon: "In an evolutionary perspective we propose therefore that the intentional communicative function of primate's communicative gesture might be a functional interface between actions and language prerequisites, nested inside the monkeys' Broca's homologue." Likewise, the notion of "embodied modality" on line 356 may not be fully transparent to readers.

8. references to complementary work seeking deep roots for 'language'-related brain circuitry (e.g.: PMID: 32313267) [lines 359-361] should be added.

9. Fix the ungrammatical sentence fragment page. 8 LL: 173-174

"Similarly, then apes, some communicative manual gestures…".

https://doi.org/10.7554/eLife.70521.sa1

Author response

Essential revisions:

1) A closer look at the raw depth data (which the authors have openly shared) suggests that variability at the endpoints of the sulcus, thus including the most ventral portion, is larger across subjects compared to the middle portion. Plotting the standard deviations is illustrative in this respect. The employed method does not exclude the possibility that this variability may result from difficulties in measuring the sulcus depth at the endpoints or due to alignments, for example when the sulci have different lengths. It is not clear how you ensured that the length of the sulcus in the left hemisphere overlaps with the one in the right hemisphere. Your method seems to assume that a certain portion of sulcus to the left (a bin) corresponds to the same portion of sulcus to the right. This assumption is fundamental to your analysis, right? In which case, is it possible that the significance observed in a portion of the sulcus is a "misalignment" artifact (the big standard deviations for this portion are concerning in that regard). Would it be possible to back up the work with VBM analysis (eg Backer et al. Brain Struct Funct 2021)? The VBM analysis might not be necessary if they are able to account for the concern in another way.

Thank you for this in-depth check of our data. In fact, "misalignment" artifact between left and right hemisphere are very unlikely to explain our effect for the 3 following reasons:

First, for each sulcus, the automated sulci parametrization algorithm in BrainVisa provides depth measurements for 99 equal cuts within the entire sulcus, normalizing thus the length of both the left and the right sulcus, which prevent thus any potential "misalignment" artifact. In other word, it means that the position 33 in the right sulcus and the position 33 in the left sulcus are corresponding exactly to the same 1/3 portion of each sulcus across all subjects, regardless of their respective length. So the significant normalized bin found at the last third section of the sulcus (i.e., from 65 to 95) is corresponding to the exact relative sulcus portion in the two L/R sulci and in the 50 subjects.

Second, the specific effect occurs for, not only in the extremity, but in large portion (about the last third portion) of the sulcus (i.e. from positions 65 to 95).

Finally, the effect occurs exclusively for handedness for communicative gesture but not for handedness for non-communicative manipulation. There is no reason why any "misalignment" artifact would have impacted only asymmetry sulcal effect for gestural communication and not similarly for handedness for manipulation. Actually, the AQ variability that the reviewer noticed at the most ventral portion, is the main focused of the study for which we provided solid evidence that such a AQ variability is related to variation of handedness direction across subjects for gestural communication exclusively.

A VBM study would be very interesting for replicating our results. Therefore, we added this VBM perspective in the discussion:

“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.”

Although interesting, we don’t see the need or relevance for conducting, in the present paper, an entire new VBM study – as a simple “back up” – which, by the way, has its own limitations (Mechelli et al., 2005), especially for brain asymmetry studies regarding interhemispheric misalignment issue. Sulci depth approach on brain asymmetry has been acknowledged as solid and mature enough for comparative research (e.g., Coulon et al., IEEE EMBS 2011; Cykowski et al., Cerebral Cortex 2008; Hopkins et al., J. of Neuroscience 2010; Leroy et al., PNAS 2015). We demonstrated our findings are robust and stand on its own, the work being carefully controlled by both behavioral (non-communicative task) and sulcus (central sulcus) controls.

2) The correlations reported in Figure 2 might suffer from circularity problems, since the analysis is based on the AQ scores derived from the subset of bins which were already shown as significant in Figure 1. This needs to be addressed.

It is true that the variables “HI scores” (degree of hand preference) used in the correlation analysis were used also to define the category of handedness (i.e., left- or right- direction of handedness) used in the first categorial analysis. But, the respective finding provided by categorial analysis versus by correlational analysis are both valuable since different and complementary, given direction and degree effects might be independent and inconsistent. In other words, finding an effect of the direction of handedness (left versus right-hand) on the AQ scores in the categorial analysis doesn’t not mean that the degree of manual asymmetry is correlated to the degree of brain asymmetry. So additional correlational analyses are needed to test it (see Margiotoudi et al., 2019 Cortex). And vice et versa: the finding – that the stronger the degree of hand preference (HI), the stronger the degree of brain asymmetry (AQ) – is a valuable additional information that does not imply that the left-right direction of handedness has an influence on the AQ values. In fact, we found both, reinforcing the asymmetric link we found between gestural communication behaviour and the ventral third part of the inferior arcuate sulcus at both a qualitative and quantitative levels. We added in the discussion that this correlation analyses are built upon the first categorial findings:

“Building upon these first results, we also found a significant negative correlation between the Handedness Index (HI) values for gestures and the Asymmetric Quotient (AQ) depth values of the IA sulcus “Broca 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.”

3) What is the evolutionary link between left lateralization for language in humans and gestural communication in the current study? The suggestion of phylogenetic continuity between language-related frontal lateralization and gestural communication seems premature in light of the contralateral effects the authors report. In this regard, while a functional shift from motor regions to the more inferior frontal regions for the gestural communication system may seem relevant, it remains to be elucidated how structural asymmetry-which has been shown to be in both the left and right hemispheres in baboons-can be turn into a fully left-lateralized language system in humans. Views arguing against the gesture-first hypothesis of language evolution should therefore also be considered (e.g., Kendon Psychon Bull Rev 2017).

Thank you for this point which indeed requires clarification in our manuscript. We added thus a paragraph at the end of the introduction to clarify the implications of our contribution in comparison to previous comparative population-level works on leftward brain lateralization for language.

“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; Catalupo and Hopkins, 2001; Marie et al., 2018; Becker et al., 2021 b,c) or similar populational-level right-handedness for communicative gestures (reviewed in: Meguerditchain 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.”

It must be noted that not all humans are functionally left lateralized for language neither and structural left lateralisation of key-language regions like the Planum Temporale occur in about 65% of the (human) population just like in nonhuman primates (e.g., Geschwind and Levitsky, Science 1968).

Difference in degree in the population-level leftward lateralization between baboons and humans does not mean that there is no continuity in the underlying behavioral/brain correlates at the individual level. It is probable that a population-level bias, which is present in the baboon, has increased in humans in the course of the evolution.

Regarding views arguing for multimodal language origins (like Kendon, 2017), we have added in our discussion:

“…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 left-hemispheric specialization.”

4. On line 52 they state that research on gestural communication in primates has recently received increased attention. The word 'recently' is inappropriate, since a gestural origin for language has long been entertained. Rephrase this part to acknowledge this research tradition ('gestural protolanguage hypothesis').

Ok, good point, we deleted the word “recently” and reformulate.

We have rephrased accordingly:

“the research on gestural communication in apes and monkeys has historically shown a significant interest within this evolutionary framework.”

5. On line 75-77, the authors list a couple of publications to support the idea that "the neural substrates of typical handedness measures and language brain organisation might be not related but rather independent from each other". There are more recent and comprehensive studies that should be cited in this context (the works of N.Tsourio-Mazoyer and C. Franks).

We have added line 73: Labache et al., eLife 2020 to the list of publications.

6. Pointers to the literature on sign language and handedness in the context of gestural communication and language lateralization (line 78 et seq.) would be a helpful addition.

We have added in line 80:

“Moreover, further work showed Broca activation in the left hemisphere also for sign language production including manual and oro-facial gestures (Emmorey et al., 2004; MacSweeney, and Waters, 2008).”

7. The end of the Discussion section could be better articulated. Lines 352-354 should be expanded upon: "In an evolutionary perspective we propose therefore that the intentional communicative function of primate's communicative gesture might be a functional interface between actions and language prerequisites, nested inside the monkeys' Broca's homologue." Likewise, the notion of "embodied modality" on line 356 may not be fully transparent to readers.

We have rephrased the last paragraph of our discussion accordingly:

“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 hypothesized functional interface of actions and language prerequisites, nested inside the monkeys’ Broca’s homologue (see also: Arbib 2006, Rizzolatti 2017, 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.”

8. References to complementary work seeking deep roots for 'language'-related brain circuitry (e.g.: PMID: 32313267) [lines 359-361] should be added.

We have added this reference:

“(…) whereas comparative language research has focused on the potential continuities across primate brain circuitry (e.g., Balezeau et al., 2020; Becker et al., 2021a) or vocal and auditory systems (…)”

9. Fix the ungrammatical sentence fragment page. 8 LL: 173-174

"Similarly, then apes, some communicative manual gestures…".

Thanks, we have changed the sentence:

“Like in apes, some communicative manual gestures in baboons have been found to share human-like intentional control, referential properties, flexibility of acquisition and of use as well as similar specific pattern of manual lateralisation (reviewed in Tomasello, 2008; Meguerditchian and Vauclair, 2014; Meguerditchain et al., 2013).”

https://doi.org/10.7554/eLife.70521.sa2

Article and author information

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

Funding

H2020 European Research Council (716931 - GESTIMAGE - ERC-2016-STG)

  • Adrien Meguerditchian

Agence Nationale de la Recherche (ANR-12-PDOC-0014-01)

  • Adrien Meguerditchian

Agence Nationale de la Recherche (ANR-16-CONV-0002)

  • Adrien Meguerditchian

Initiative d’Excellence d’Aix-Marseille Université (A*Midex AMX-19-IET-004)

  • Yannick Becker

Agence Nationale de la Recherche (ANR-17-EURE-0029)

  • Yannick Becker

Agence Nationale de la Recherche (LangPrimate)

  • Adrien Meguerditchian

Agence Nationale de la Recherche (ILCB)

  • Adrien Meguerditchian

Initiative d’Excellence d’Aix-Marseille Université (NeuroMarseille)

  • Adrien Meguerditchian

Agence Nationale de la Recherche (NeuroSchool)

  • Yannick Becker

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Acknowledgements

We are very grateful to the Station de Primatologie CNRS, particularly the animal care staff and technicians, Jean-Noël Benoit, Jean-Christophe Marin, Valérie Moulin, Fidji and Richard Francioly, Laurence Boes, Célia Sarradin, Brigitte Rimbaud, Sebastien Guiol, Georges Di Grandi for their critical involvement in this project; Leonard Samain-Aupic for sulci labelling; Ivan Balansard, Sandrine Melot-Dusseau, Laura Desmis, Frederic Lombardo and Colette Pourpe for additional assistance.

Ethics

All baboons were housed in social groups at the Station de Primatologie CNRS (UPS 846, Rousset, France; Agreement number for conducting experiments on vertebrate animals: D13-087-7) and have free access to outdoor areas connected to indoor areas. Wooden and metallic, ethologically approved, structures enrich the enclosures. Feeding times are held four times a day with seeds, monkey pellets and fresh fruits and vegetables. Water is available ad libitum. The study was approved by the "C2EA-71 Ethical Committee of Neurosciences" (INT Marseille) under the number APAFIS#13553-201802151547729. The experimental procedure complied with the current French laws and the European directive 86/609/CEE.

Senior and Reviewing Editor

  1. Timothy E Behrens, University of Oxford, United Kingdom

Reviewer

  1. Cedric Boeckx, ICREA/Universitat de Barcelona, Spain

Publication history

  1. Preprint posted: February 9, 2021 (view preprint)
  2. Received: May 19, 2021
  3. Accepted: February 1, 2022
  4. Accepted Manuscript published: February 2, 2022 (version 1)
  5. Version of Record published: February 15, 2022 (version 2)

Copyright

© 2022, Becker et al.

This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

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  1. Yannick Becker
  2. Nicolas Claidière
  3. Konstantina Margiotoudi
  4. Damien Marie
  5. Muriel Roth
  6. Bruno Nazarian
  7. Jean-Luc Anton
  8. Olivier Coulon
  9. Adrien Meguerditchian
(2022)
Broca's cerebral asymmetry reflects gestural communication's lateralisation in monkeys (Papio anubis)
eLife 11:e70521.
https://doi.org/10.7554/eLife.70521

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