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

Download asset Open asset

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

Download asset Open asset

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.

1. 1. Becker Y

   (2020) Open Science Framework

   OSF Storage.

   https://doi.org/10.17605/OSF.IO/DPXS5

1. 1. Amiez C
   2. Petrides M

   (2009) Anatomical organization of the eye fields in the human and non-human primate frontal cortex

   Progress in Neurobiology 89:220–230.

   https://doi.org/10.1016/j.pneurobio.2009.07.010

   • PubMed
   • Google Scholar
2. 1. Amunts K
   2. Jäncke L
   3. Mohlberg H
   4. Steinmetz H
   5. Zilles K

   (2000) Interhemispheric asymmetry of the human motor cortex related to handedness and gender

   Neuropsychologia 38:304–312.

   https://doi.org/10.1016/s0028-3932(99)00075-5

   • PubMed
   • Google Scholar
3. 1. Arbib MA
   2. Liebal K
   3. Pika S

   (2008) Primate vocalization, gesture, and the evolution of human language

   Current Anthropology 49:1053–1063.

   https://doi.org/10.1086/593015

   • PubMed
   • Google Scholar
4. 1. Balezeau F
   2. Wilson B
   3. Gallardo G
   4. Dick F
   5. Hopkins W
   6. Anwander A
   7. Friederici AD
   8. Griffiths TD
   9. Petkov CI

   (2020) Primate auditory prototype in the evolution of the arcuate fasciculus

   Nature Neuroscience 23:611–614.

   https://doi.org/10.1038/s41593-020-0623-9

   • PubMed
   • Google Scholar
5. 1. Becker Y
   2. Phelipon R
   3. Sein J
   4. Velly L
   5. Renaud L
   6. Meguerditchian A

   (2021a) Planum temporale grey matter volume asymmetries in newborn monkeys (Papio anubis)

   Brain Structure & Function 227:463.

   https://doi.org/10.1007/s00429-021-02278-9

   • PubMed
   • Google Scholar
6. 1. Becker Y
   2. Sein J
   3. Velly L
   4. Giacomino L
   5. Renaud L
   6. Lacoste R
   7. Anton JL
   8. Nazarian B
   9. Berne C
   10. Meguerditchian A

   (2021b) Early Left-Planum Temporale Asymmetry in newborn monkeys (Papio anubis): A longitudinal structural MRI study at two stages of development

   NeuroImage 227:117575.

   https://doi.org/10.1016/j.neuroimage.2020.117575

   • PubMed
   • Google Scholar
7. 1. Becker Y
   2. Loh KK
   3. Coulon O
   4. Meguerditchian A

   (2022) The Arcuate Fasciculus and language origins: Disentangling existing conceptions that influence evolutionary accounts

   Neuroscience & Biobehavioral Reviews 134:104490.

   https://doi.org/10.1016/j.neubiorev.2021.12.013

   • Google Scholar
8. 1. Belmalih A
   2. Borra E
   3. Contini M
   4. Gerbella M
   5. Rozzi S
   6. Luppino G

   (2009) Multimodal architectonic subdivision of the rostral part (area F5) of the macaque ventral premotor cortex

   The Journal of Comparative Neurology 512:183–217.

   https://doi.org/10.1002/cne.21892

   • PubMed
   • Google Scholar
9. 1. Blake J
   2. O’Rourke P
   3. Borzellino G

   (1994) Form and function in the development of pointing and reaching gestures

   Infant Behavior and Development 17:195–203.

   https://doi.org/10.1016/0163-6383(94)90055-8

   • Google Scholar
10. 1. Boë LJ
    2. Berthommier F
    3. Legou T
    4. Captier G
    5. Kemp C
    6. Sawallis TR
    7. Becker Y
    8. Rey A
    9. Fagot J

    (2017) Evidence of a vocalic proto-system in the baboon (Papio papio) suggests pre-hominin speech precursors

    PLOS ONE 12:e0169321.

    https://doi.org/10.1371/journal.pone.0169321

    • Google Scholar
11. 1. Bonvillian JD
    2. Richards HC
    3. Dooley TT

    (1997) Early sign language acquisition and the development of hand preference in young children

    Brain and Language 58:1–22.

    https://doi.org/10.1006/brln.1997.1754

    • PubMed
    • Google Scholar
12. 1. Cantalupo C
    2. Hopkins WD

    (2001) Asymmetric Broca’s area in great apes

    Nature 414:505.

    https://doi.org/10.1038/35107134

    • PubMed
    • Google Scholar
13. 1. Cochet H
    2. Vauclair J

    (2010) Pointing gestures produced by toddlers from 15 to 30 months: different functions, hand shapes and laterality patterns

    Infant Behavior & Development 33:431–441.

    https://doi.org/10.1016/j.infbeh.2010.04.009

    • PubMed
    • Google Scholar
14. 1. Cochet H
    2. Jover M
    3. Vauclair J

    (2011) Hand preference for pointing gestures and bimanual manipulation around the vocabulary spurt period

    Journal of Experimental Child Psychology 110:393–407.

    https://doi.org/10.1016/j.jecp.2011.04.009

    • PubMed
    • Google Scholar
15. 1. Corballis MC

    (2015) What’s left in language? Beyond the classical model

    Annals of the New York Academy of Sciences 1359:14–29.

    https://doi.org/10.1111/nyas.12761

    • PubMed
    • Google Scholar
16. 1. Cykowski MD
    2. Coulon O
    3. Kochunov PV
    4. Amunts K
    5. Lancaster JL
    6. Laird AR
    7. Glahn DC
    8. Fox PT

    (2008) The central sulcus: an observer-independent characterization of sulcal landmarks and depth asymmetry

    Cerebral Cortex 18:1999–2009.

    https://doi.org/10.1093/cercor/bhm224

    • PubMed
    • Google Scholar
17. 1. Dadda M
    2. Cantalupo C
    3. Hopkins WD

    (2006) Further evidence of an association between handedness and neuroanatomical asymmetries in the primary motor cortex of chimpanzees (Pan troglodytes)

    Neuropsychologia 44:2582–2586.

    https://doi.org/10.1016/j.neuropsychologia.2006.03.037

    • PubMed
    • Google Scholar
18. 1. Diedenhofen B
    2. Musch J

    (2015) cocor: a comprehensive solution for the statistical comparison of correlations

    PLOS ONE 10:e0121945.

    https://doi.org/10.1371/journal.pone.0121945

    • PubMed
    • Google Scholar
19. 1. Emmorey K
    2. Grabowski T
    3. McCullough S
    4. Damasio H
    5. Ponto L
    6. Hichwa R
    7. Bellugi U

    (2004) Motor-iconicity of sign language does not alter the neural systems underlying tool and action naming

    Brain and Language 89:27–37.

    https://doi.org/10.1016/S0093-934X(03)00309-2

    • PubMed
    • Google Scholar
20. 1. Fagard J

    (2013) The nature and nurture of human infant hand preference

    Annals of the New York Academy of Sciences 1288:114–123.

    https://doi.org/10.1111/nyas.12051

    • PubMed
    • Google Scholar
21. Book

    1. Friederici AD

    (2017) Language in Our Brain: The Origins of a Uniquely Human Capacity

    Cambridge, MA: MIT Press.

    https://doi.org/10.7551/mitpress/9780262036924.001.0001

    • Google Scholar
22. 1. Gannon PJ
    2. Holloway RL
    3. Broadfield DC
    4. Braun AR

    (1998) Asymmetry of chimpanzee planum temporale: humanlike pattern of Wernicke’s brain language area homolog

    Science 279:220–222.

    https://doi.org/10.1126/science.279.5348.220

    • PubMed
    • Google Scholar
23. 1. Gavrilov N
    2. Nieder A

    (2021) Distinct neural networks for the volitional control of vocal and manual actions in the monkey homologue of Broca’s area

    eLife 10:e62797.

    https://doi.org/10.7554/eLife.62797

    • PubMed
    • Google Scholar
24. 1. Gentilucci M
    2. Dalla Volta R

    (2008) Spoken language and arm gestures are controlled by the same motor control system

    Quarterly Journal of Experimental Psychology 61:944–957.

    https://doi.org/10.1080/17470210701625683

    • PubMed
    • Google Scholar
25. 1. Geschwind N
    2. Levitsky W

    (1968) Human brain: left-right asymmetries in temporal speech region

    Science 161:186–187.

    https://doi.org/10.1126/science.161.3837.186

    • PubMed
    • Google Scholar
26. 1. Graïc JM
    2. Peruffo A
    3. Corain L
    4. Centelleghe C
    5. Granato A
    6. Zanellato E
    7. Cozzi B

    (2020) Asymmetry in the Cytoarchitecture of the Area 44 Homolog of the Brain of the Chimpanzee Pan troglodytes

    Frontiers in Neuroanatomy 14:e55.

    https://doi.org/10.3389/fnana.2020.00055

    • PubMed
    • Google Scholar
27. 1. Groen MA
    2. Whitehouse AJO
    3. Badcock NA
    4. Bishop DVM

    (2013) Associations between handedness and cerebral lateralisation for language: a comparison of three measures in children

    PLOS ONE 8:e64876.

    https://doi.org/10.1371/journal.pone.0064876

    • PubMed
    • Google Scholar
28. 1. Häberling IS
    2. Corballis PM
    3. Corballis MC

    (2016) Language, gesture, and handedness: Evidence for independent lateralized networks

    Cortex 82:72–85.

    https://doi.org/10.1016/j.cortex.2016.06.003

    • PubMed
    • Google Scholar
29. 1. Hickok G
    2. Poeppel D

    (2007) The cortical organization of speech processing

    Nature Reviews. Neuroscience 8:393–402.

    https://doi.org/10.1038/nrn2113

    • PubMed
    • Google Scholar
30. 1. Hopkins WD

    (1995) Hand preferences for a coordinated bimanual task in 110 chimpanzees (Pan troglodytes): cross-sectional analysis

    Journal of Comparative Psychology 109:291–297.

    https://doi.org/10.1037/0735-7036.109.3.291

    • PubMed
    • Google Scholar
31. 1. Hopkins WD
    2. Cantalupo C

    (2004) Handedness in chimpanzees (Pan troglodytes) is associated with asymmetries of the primary motor cortex but not with homologous language areas

    Behavioral Neuroscience 118:1176–1183.

    https://doi.org/10.1037/0735-7044.118.6.1176

    • PubMed
    • Google Scholar
32. 1. Jarvis ED

    (2019) Evolution of vocal learning and spoken language

    Science (New York, N.Y.) 366:50–54.

    https://doi.org/10.1126/science.aax0287

    • PubMed
    • Google Scholar
33. 1. Keller SS
    2. Crow T
    3. Foundas A
    4. Amunts K
    5. Roberts N

    (2009) Broca’s area: nomenclature, anatomy, typology and asymmetry

    Brain and Language 109:29–48.

    https://doi.org/10.1016/j.bandl.2008.11.005

    • PubMed
    • Google Scholar
34. 1. Knecht S
    2. Dräger B
    3. Deppe M
    4. Bobe L
    5. Lohmann H
    6. Flöel A
    7. Ringelstein EB
    8. Henningsen H

    (2000) Handedness and hemispheric language dominance in healthy humans

    Brain 123:2512–2518.

    https://doi.org/10.1093/brain/123.12.2512

    • PubMed
    • Google Scholar
35. 1. Koechlin E
    2. Jubault T

    (2006) Broca’s area and the hierarchical organization of human behavior

    Neuron 50:963–974.

    https://doi.org/10.1016/j.neuron.2006.05.017

    • PubMed
    • Google Scholar
36. 1. Labache L
    2. Mazoyer B
    3. Joliot M
    4. Crivello F
    5. Hesling I
    6. Tzourio-Mazoyer N

    (2020) Typical and atypical language brain organization based on intrinsic connectivity and multitask functional asymmetries

    eLife 9:e58722.

    https://doi.org/10.7554/eLife.58722

    • PubMed
    • Google Scholar
37. 1. MacSweeney M
    2. Capek CM
    3. Campbell R
    4. Woll B

    (2008) The signing brain: the neurobiology of sign language

    Trends in Cognitive Sciences 12:432–440.

    https://doi.org/10.1016/j.tics.2008.07.010

    • PubMed
    • Google Scholar
38. 1. Mangin JF
    2. Rivière D
    3. Cachia A
    4. Duchesnay E
    5. Cointepas Y
    6. Papadopoulos-Orfanos D
    7. Collins DL
    8. Evans AC
    9. Régis J

    (2004) Object-based morphometry of the cerebral cortex

    IEEE Transactions on Medical Imaging 23:968–982.

    https://doi.org/10.1109/TMI.2004.831204

    • PubMed
    • Google Scholar
39. 1. Margiotoudi K
    2. Marie D
    3. Claidière N
    4. Coulon O
    5. Roth M
    6. Nazarian B
    7. Lacoste R
    8. Hopkins WD
    9. Molesti S
    10. Fresnais P
    11. Anton JL
    12. Meguerditchian A

    (2019) Handedness in monkeys reflects hemispheric specialization within the central sulcus. An in vivo MRI study in right- and left-handed olive baboons

    Cortex 118:203–211.

    https://doi.org/10.1016/j.cortex.2019.01.001

    • PubMed
    • Google Scholar
40. 1. Marie D
    2. Roth M
    3. Lacoste R
    4. Nazarian B
    5. Bertello A
    6. Anton JL
    7. Hopkins WD
    8. Margiotoudi K
    9. Love SA
    10. Meguerditchian A

    (2018) Left Brain Asymmetry of the Planum Temporale in a Nonhominid Primate: Redefining the Origin of Brain Specialization for Language

    Cerebral Cortex 28:1808–1815.

    https://doi.org/10.1093/cercor/bhx096

    • PubMed
    • Google Scholar
41. 1. Maris E
    2. Oostenveld R

    (2007) Nonparametric statistical testing of EEG- and MEG-data

    Journal of Neuroscience Methods 164:177–190.

    https://doi.org/10.1016/j.jneumeth.2007.03.024

    • PubMed
    • Google Scholar
42. 1. Mazoyer B
    2. Zago L
    3. Jobard G
    4. Crivello F
    5. Joliot M
    6. Perchey G
    7. Mellet E
    8. Petit L
    9. Tzourio-Mazoyer N

    (2014) Gaussian mixture modeling of hemispheric lateralization for language in a large sample of healthy individuals balanced for handedness

    PLOS ONE 9:e101165.

    https://doi.org/10.1371/journal.pone.0101165

    • PubMed
    • Google Scholar
43. 1. Meguerditchian A
    2. Vauclair J

    (2006) Baboons communicate with their right hand

    Behavioural Brain Research 171:170–174.

    https://doi.org/10.1016/j.bbr.2006.03.018

    • PubMed
    • Google Scholar
44. 1. Meguerditchian A
    2. Vauclair J

    (2009) Contrast of hand preferences between communicative gestures and non-communicative actions in baboons: implications for the origins of hemispheric specialization for language

    Brain and Language 108:167–174.

    https://doi.org/10.1016/j.bandl.2008.10.004

    • PubMed
    • Google Scholar
45. 1. Meguerditchian A
    2. Vauclair J
    3. Hopkins WD

    (2010) Captive chimpanzees use their right hand to communicate with each other: implications for the origin of the cerebral substrate for language

    Cortex 46:40–48.

    https://doi.org/10.1016/j.cortex.2009.02.013

    • PubMed
    • Google Scholar
46. 1. Meguerditchian A
    2. Molesti S
    3. Vauclair J

    (2011) Right-handedness predominance in 162 baboons (Papio anubis) for gestural communication: consistency across time and groups

    Behavioral Neuroscience 125:653–660.

    https://doi.org/10.1037/a0023823

    • PubMed
    • Google Scholar
47. 1. Meguerditchian A
    2. Gardner MJ
    3. Schapiro SJ
    4. Hopkins WD

    (2012) The sound of one-hand clapping: handedness and perisylvian neural correlates of a communicative gesture in chimpanzees

    Proceedings of the Royal Society B: Biological Sciences 279:1959–1966.

    https://doi.org/10.1098/rspb.2011.2485

    • PubMed
    • Google Scholar
48. 1. Meguerditchian A
    2. Vauclair J
    3. Hopkins WD

    (2013) On the origins of human handedness and language: a comparative review of hand preferences for bimanual coordinated actions and gestural communication in nonhuman primates

    Developmental Psychobiology 55:637–650.

    https://doi.org/10.1002/dev.21150

    • PubMed
    • Google Scholar
49. 1. Meguerditchian A
    2. Vauclair J

    (2014) Communicative Signaling, Lateralization and Brain Substrate in Nonhuman Primates: Toward a Gestural or a Multimodal Origin of Language

    Humana Mente: Journal of Philosophical Studies 7:135–160.

    https://doi.org/10.3378/027.083.0203

    • Google Scholar
50. 1. Molesti S
    2. Vauclair J
    3. Meguerditchian A

    (2016) Hand preferences for unimanual and bimanual coordinated actions in olive baboons (Papio anubis): Consistency over time and across populations

    Journal of Comparative Psychology 130:341–350.

    https://doi.org/10.1037/com0000040

    • PubMed
    • Google Scholar
51. 1. Molesti S
    2. Meguerditchian A
    3. Bourjade M

    (2020) Gestural communication in olive baboons (Papio anubis): repertoire and intentionality

    Animal Cognition 23:19–40.

    https://doi.org/10.1007/s10071-019-01312-y

    • PubMed
    • Google Scholar
52. 1. Nudo RJ
    2. Jenkins WM
    3. Merzenich MM
    4. Prejean T
    5. Grenda R

    (1992) Neurophysiological correlates of hand preference in primary motor cortex of adult squirrel monkeys

    The Journal of Neuroscience 12:2918–2947.

    https://doi.org/10.1523/JNEUROSCI.12-08-02918.1992

    • PubMed
    • Google Scholar
53. 1. Ocklenburg S
    2. Beste C
    3. Arning L
    4. Peterburs J
    5. Güntürkün O

    (2014) The ontogenesis of language lateralization and its relation to handedness

    Neuroscience and Biobehavioral Reviews 43:191–198.

    https://doi.org/10.1016/j.neubiorev.2014.04.008

    • PubMed
    • Google Scholar
54. 1. Petrides M
    2. Cadoret G
    3. Mackey S

    (2005) Orofacial somatomotor responses in the macaque monkey homologue of Broca’s area

    Nature 435:1235–1238.

    https://doi.org/10.1038/nature03628

    • PubMed
    • Google Scholar
55. 1. Phillips KA
    2. Sherwood CC

    (2005) Primary motor cortex asymmetry is correlated with handedness in capuchin monkeys (Cebus apella)

    Behavioral Neuroscience 119:1701–1704.

    https://doi.org/10.1037/0735-7044.119.6.1701

    • PubMed
    • Google Scholar
56. 1. Rizzolatti G
    2. Craighero L

    (2004) The mirror-neuron system

    Annual Review of Neuroscience 27:169–192.

    https://doi.org/10.1146/annurev.neuro.27.070203.144230

    • PubMed
    • Google Scholar
57. 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

    • PubMed
    • Google Scholar
58. 1. Stout D
    2. Hecht E
    3. Khreisheh N
    4. Bradley B
    5. Chaminade T

    (2015) Cognitive demands of lower paleolithic toolmaking

    PLOS ONE 10:e0121804.

    https://doi.org/10.1371/journal.pone.0121804

    • PubMed
    • Google Scholar
59. 1. Taglialatela JP
    2. Cantalupo C
    3. Hopkins WD

    (2006) Gesture handedness predicts asymmetry in the chimpanzee inferior frontal gyrus

    Neuroreport 17:923–927.

    https://doi.org/10.1097/01.wnr.0000221835.26093.5e

    • PubMed
    • Google Scholar
60. Book

    1. Tomasello M

    (2008) Origins of Human Communication

    Cambridge, MA: MIT Press.

    https://doi.org/10.7551/mitpress/7551.001.0001

    • Google Scholar
61. 1. Vauclair J
    2. Meguerditchian A
    3. Hopkins WD

    (2005) Hand preferences for unimanual and coordinated bimanual tasks in baboons (Papio anubis)

    Brain Research. Cognitive Brain Research 25:210–216.

    https://doi.org/10.1016/j.cogbrainres.2005.05.012

    • PubMed
    • Google Scholar
62. 1. Wakita M

    (2014) Broca’s area processes the hierarchical organization of observed action

    Frontiers in Human Neuroscience 7:937.

    https://doi.org/10.3389/fnhum.2013.00937

    • PubMed
    • Google Scholar
63. 1. Watanabe-Sawaguchi K
    2. Kubota K
    3. Arikuni T

    (1991) Cytoarchitecture and intrafrontal connections of the frontal cortex of the brain of the hamadryas baboon (Papio hamadryas)

    The Journal of Comparative Neurology 311:108–133.

    https://doi.org/10.1002/cne.903110109

    • PubMed
    • Google Scholar
64. 1. Wilson B
    2. Marslen-Wilson WD
    3. Petkov CI

    (2017) Conserved Sequence Processing in Primate Frontal Cortex

    Trends in Neurosciences 40:72–82.

    https://doi.org/10.1016/j.tins.2016.11.004

    • PubMed
    • Google Scholar
65. 1. Zaccarella E
    2. Papitto G
    3. Friederici AD

    (2021) Language and action in Broca’s area: Computational differentiation and cortical segregation

    Brain and Cognition 147:105651.

    https://doi.org/10.1016/j.bandc.2020.105651

    • PubMed
    • Google Scholar

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

• 1,692

  views

• 216

  downloads

• 18

  citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.