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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 4 - 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: 2022-03-01 to 2024-02-29

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 as the expense of another behavioral asymmetry: production of communicativegestures. Considering the strong language/gesture links in humans and the continuities found between gestural communication in nonhuman primates and some language properties, handedness for communicative gestures specifically has been suggested as a potential better candidate to predict language lateralization. In the present project, we proposed to investigate our recent 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, we evaluated 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 was to explore the functional brain lateralization of communication and hand movement processing in baboons using non-invasive wireless Infrared Spectroscopy.
A last innovative objective was to investigate, through the first non-invasive longitudinal MRI study conducted from birth to sexual maturity in primates, the development brain structural asymmetries and their correlates with gesture asymmetries in 30 baboons as well as external environmental factors such as maternal cradling on the development of brain and manual asymmetry of the offspring.

In conclusion, our research speak for the evolutionary human/monkey continuities for (1) the communicative gestural system with language lateralization, (2) handedness for manipulation with the motor cortex plasticity, dating back – not to Hominidae – but to a much older common ancestor shared with old-world monkeys, 25-35 million years ago.
WP1 Comparative asymmetries in baboons & humans
We found that, in both humans and baboons, unlike typical handedness measures, communicative gesturing’s hand preference is clearly related to markers of language-related hemispheric specialization. In contrast, handedness for manipulation in baboons was exclusively related to the cerebral asymmetry of the motor hand area within the depth of the central sulcus of the brain, just like human handedness.
These collective findings clearly 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.

WP2 Functional brain lateralization using fNIRS
We successfully tested for the first time non-invasive optical fNIRS imaging (near infrared spectroscopy) on anesthetized baboons to infer hemispheric difference in functional activation of the brain for both arms movement in the motor cortex and audio stimulation in the temporal cortex. This critical development of this technique opened further data acquisition of brain activity for communication tasks in a more ecological environment by training monkeys to wear the device.

WP3 Longitudinal development
We found that, similarly than in human infants, baboon newborns shows leftward asymmetry for a key structure for language, the Planum Temporale, which increases with age and predict the future development on right-handedness for gestural communication once juveniles, suggesting this feature might be not human- or language-specific but related to a ancient prewired lateralized system for gesture inherited from our last common ancestor with monkeys.
In contrast, maternal baby cradling bias in baboons’ mother shape not only the early neuroanatomical asymmetry of the motor hand area in their baby but also the first manifestation of their early hand preference for reaching. Such an external maternal factor seems thus to shape the baby’s brain by plasticity, but finally disappears when the baboons is wean at 9 month old. At this age, their pattern of handedness further evolved independently from their mother, likely in relation to novel and more complex manipulative experience (bimanual coordination), which ultimately affect their central sulcus asymmetry.

WP4 Dissemination
35 published papers (+ 6 to be submitted + 5 in prep)
- 21 original research papers
- 9 review or theory chapters
- 5 science popularization article in French journals for the general public
95 communications
- 36 to international conf/workshops including 4 published abstracts & 13 invited
- 33 to francophone conf/workshops including 11 published abstracts & 19 invited
- 26 to general-public events (Schools, Theaters, Prison, Coffees, Festival, Social Center, Public Library or Museum)
These significant progress beyond the state of the art addressed the key theoretical objectives of the GESTIMAGE’s project.

To sump, first, we found that in both humans and baboons, communicative gesturing’s hand preference is clearly related to markers of language-related hemispheric specialization, while handedness for manipulation is exclusively related to the cerebral asymmetry of the motor hand area.
Second, our developmental studies further drawn two ground-breaking theories for the ontogeny of lateralization in growing primate, namely two opposite directional brain-behavior links across development between communication versus manipulation : (1) whereas early language-like brain asymmetry seems already determined at birth and shape the further development of gestural communication’s lateralization, (2) the emergence of handedness for manipulative action affects by brain plasticity their related cerebral asymmetry within the central sulcus.

These collective findings speak for the evolutionary human/monkey continuities for (1) the communicative gestural system with language lateralization, (2) handedness for manipulation with the motor cortex plasticity, dating back – not to Hominidae – but to a much older common ancestor shared with old-world monkeys, 25-35 million years ago.

Our work also has clinical implications in epileptology for evaluating the viability of brain surgery. Our findings suggest that simple measures of manual preference for producing communicative gestures in a patient might provide additional cues to investigate which hemisphere is dominant for language. It may thus help the neurologists to better apprehend - before a potential excision of a part of the cortex including the epileptogenic epicenter – the profiles of brain organization for language in the patients in order to minimize the risks of post-surgery aphasia.

At both evolutionary and developmental levels, the project has thus ultimately contributed to enhance our understanding on the origins of brain specialization for handedness, for language and its closed links with gestural communication, making the baboon a relevant model for investigating their respective ontogeny.
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