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Gestures in nonhuman and human primates, a landmark of language in the brain? Searching for the origins of brain specialization for language

Periodic Reporting for period 2 - GESTIMAGE (Gestures in nonhuman and human primates, a landmark of language in the brain? Searching for the origins of brain specialization for language)

Reporting period: 2019-03-01 to 2020-08-31

Most of language functions are under the left brain control in both left- and right-handers and involve structural asymmetries between the two hemispheres. While this asymmetry was considered as associated with handedness, such a relation has been recently questioned. Considering the strong language/gesture links in humans and the continuities between the gestural system in apes and monkeys and some language properties, we recently suggested the hypothesis of a continuity between language lateralization and asymmetry of communicative gestures in both human and nonhuman primates. Given the phylogenetical proximity between those species, comparative research on brain specialization between a non-linguistic gestural system (i.e. in monkeys) versus a linguistic gestural systems in humans (i.e. pointing gestures, sign language in deaf) might help evaluating the gestural continuities with language lateralization in term of manual asymmetries, structural and functional lateralization of the brain.
To this purpose, a first objective is to evaluate the continuities of manual and brain asymmetries between (1) a linguistic gestural system in humans using MRI in 100 participants, and (2) a non-linguistic gestural system of adult baboons Papio anubis using 106 MRI brain images.
A second objective is to explore the functional brain lateralization of gestures production in baboons (versus manipulation) using non-invasive wireless Infrared Spectroscopy in 8 trained subjects within interactions with humans.
A last innovative objective is to investigate, through the first non-invasive longitudinal MRI study conducted from birth to sexual maturity in primates, the development and heritability of brain structural asymmetries and their correlates with gesture asymmetries in 30 baboons.
At both evolutionary and developmental levels, the project will thus ultimately contribute to enhance our understanding on the role of gestures in the origins of brain specialization for language.
The GESTIMAGE ERC project successfully started in developing the 4 work packages which led to the following major achievements:

- WP1: human/primate continuities of brain & manual asymmetries
Within a comparative framework with human language brain organization, analyses of the MRI scans in our adult brain data base in baboons allow us to fully quantified in both hemispheres: (1) Brain, white & grey matters volumes as well as critical cortical language homolog regions such as (2) Planum temporale’s & (3) Insula’s grey matter volumes and sulcal depth and surface of the (4) central sulcus, (5) Superior Temporal sulcus, (6) Inferior arcuate sulcus, (7) cingulate sulcus.
In preliminary results, we found in both humans and baboons that, unlike typical handedness measures, communicative gesturing’s hand lateralization is clearly related to markers of language-related hemispheric specialization.

- WP2: Functional brain lateralization in baboons using fNIRS
As a first major step, we successful tested for the first time the noninvasive functional optical imaging technique - fNIRS - on 3 anesthetized female baboons. As predicted, we found (1) activations hemispheric asymmetries of the motor cortex related to right versus left arm & hand movements as well as (2) lateralized activations of the temporal cortex under audio stimulation (silent vs white noise vs baboons vs other screams).

- WP3: Longitudinal brain development of hemispheric structural asymmetries
Unique longitudinal daily data and video corpus collection on motor, gestural & mother-infant behaviours as well as noninvasive brain MRI scanning have successfully been collected on developing 30 new-born baboons living in social groups, out of which 21 became old enough to be scanned a second time at 8-10 months old, and 3 a third time at 2 years old.
Quantification of early brain structural asymmetry of a key structure for language, the planum temporale, in new born baboons revealed the typical left-lateralization found in human infants and adults.

- WP4: Dissemination
Research resulted in 12 papers including 5 accepted in Cortex, Nature Comm, Anim Cogn, Sci Rep, Evol Hum Behav; 1 book chapter; 6 manuscripts submitted or to be submitted in international journals. In addition, out of a total of 38 communications, we presented our GESTIMAGE works to 11 international meetings (including 1 published abstract and 3 invited plenary), 10 francophone conferences (including 2 invited plenaries and 3 invited lab seminars) as well as 17 general-public invited talks (Schools, Theaters, Prison, Coffees, Festival, Social Center, Public Library, Museum).
At the midterm period of the GESTIMAGE’s project, significant progress beyond the state of the art could be mentioned given the importance of their theoretical implications for the GESTIMAGE’s objectives. First, we found in both humans and baboons that, unlike typical handedness measures, hand preference for communicative gestures is clearly related to markers of language-related hemispheric lateralization. These collective findings speak for the evolutionary continuities of the gestural system with language lateralization, dating back – not to Hominidae – but to a much older common ancestor shared with old-world monkeys, 25-35 million years ago. Interestingly we also report that typical leftward brain structural asymmetries found for language regions in human adults and infants, is also seen in new born baboons such as the planum temporale, suggesting that this early neuroanatomical feature are clearly not human- or language- specific.
The main challenges and expected results for the next period of the project will be to determinate:
(1) Whether the language brain lateralization effect we found in a pilot study on gestural pointing in humans extend to signing in deaf;
(2) Whether the successful testing of the noninvasive functional optical brain imaging technique (fNIRS) in anesthetized baboons would be replicated in fully awaked and trained baboons in ecological conditions in order to further investigate whether production of communicative gestures in monkeys involves, as predicted, specific asymmetric frontal activation in comparison to non-communicative actions;
(3) Whether early language-related hemispheric lateralization found in new born baboons could predict the development of gestural communication’s lateralization.