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

Margiotoudi, Konstantina; Marié, Damien; Claidière, Nicolas; Coulon, Olivier; Roth, Muriel; Nazarian, Bruno; Lacoste, Romain; Hopkins, William D.; Molesti, Sandra; Fresnais, Pauline; Anton, Jean-Luc; Meguerditchian, Adrien

doi:10.1016/j.cortex.2019.01.001

Cited by 37 publications

(48 citation statements)

References 52 publications

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“…Some scholars (Prieur et al, 2016(Prieur et al, , 2019Marie et al, 2018) noted the presence of a low-frequency right-handedness bias in bimanual tasks in chimpanzees and gorillas (Hopkins et al, 2019). Although several studies (McGrew and Marchant, 2001;Mosquera et al, 2007;Harrison and Nystrom, 2008) indicate that great apes do not display any hand preference at the population level (Fitch and Braccini, 2013;Uomini, 2015), some groups can have a majority of left-handers (Cashmore et al, 2008;Uomini, 2009;Chapelain et al, 2011), chimpanzee groups were reported to be predominantly right-handed (Hopkins et al, 2004), and even in monkeys, handedness is related to hemispheric specialization (Margiotoudi et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

From Smart Apes to Human Brain Boxes. A Uniquely Derived Brain Shape in Late Hominins Clade

et al. 2020

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Section: Discussionmentioning

confidence: 99%

From Smart Apes to Human Brain Boxes. A Uniquely Derived Brain Shape in Late Hominins Clade

et al. 2020

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“…The evolution of sulcal asymmetry and its related asymmetrical characteristics among primate species. The sulcal asymmetry, its related asymmetrical characteristics, and influencing factors for sulcal asymmetry are summarized in reference to previous reports [4,5,13,20,[28][29][30][31][32][33][34][35][36][37][38][39][40][41][42][43][44][45][46][47]. An asterisk (*) indicates that the cs symmetry is inconsistent in the Old World monkeys.…”

Section: Introductionmentioning

confidence: 87%

“…Among baboons, which belong to the genus Papio in the Old World monkeys, right-handed and left-handed individuals were equally prevalent. Additionally, the cs depth was lateralized contralaterally to the handedness in baboons [40]. On the other hand, the length and/or surface area of the cs were lateralized contralaterally to the handedness in humans [21,22].…”

Section: Comparison To Other Nonhuman Primatesmentioning

confidence: 99%

Cerebral Sulcal Asymmetry in Macaque Monkeys

Sawada

2020

Symmetry

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The asymmetry of the cerebral sulcal morphology is particularly obvious in higher primates. The sulcal asymmetry in macaque monkeys, a genus of the Old World monkeys, in our previous studies and others is summarized, and its evolutionary significance is speculated. Cynomolgus macaques displayed fetal sulcation and gyration symmetrically, and the sulcal asymmetry appeared after adolescence. Population-level rightward asymmetry was revealed in the length of arcuate sulcus (ars) and the surface area of superior temporal sulcus (sts) in adult macaques. When compared to other nonhuman primates, the superior postcentral sulcus (spcs) was left-lateralized in chimpanzees, opposite of the direction of asymmetry in the ars, anatomically-identical to the spcs, in macaques. This may be associated with handedness: either right-handedness in chimpanzees or left-handedness/ambidexterity in macaques. The rightward asymmetry in the sts surface area was seen in macaques, and it was similar to humans. However, no left/right side differences were identified in the sts morphology among great apes, which suggests the evolutionary discontinuity of the sts asymmetry. The diversity of the cortical lateralization among primate species suggests that the sulcal asymmetry reflects the species-related specialization of the cortical morphology and function, which is facilitated by evolutionary expansion in higher primates.

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“…Whether this functional differentiation, essential for speech perception in humans (30), is also present in non-humans is unclear. Baboons appear in this respect a particularly interesting animal model to study for lateralization, with several recent studies underlying the similarities in manual and brain asymmetries with humans (5,14,31). Furthermore, the baboon brain is on average twice as large as the macaque brain (32), which may facilitate the specific investigation of sensory regions.…”

Section: At the Neural Functional Level Using Functional Magnetic Resmentioning

confidence: 99%

“…Lateralization is often presented as a key characteristic of the human brain, which separates it from other animal brains (1,2); yet, an increasing number of studies, particularly in non-human primates (from here onward, primates), dispute this claim in a broad array of topics ranging from object manipulation, gestural communication to producing or listening to species-specific vocalizations (3)(4)(5)(6)(7)(8). For instance, several primate studies present behavioral evidence of manual lateralization (4,9), which have been associated with contralateral hemispheric correlates at the neurostructural level (5,6). Other examples show orofacial asymmetries during vocal production, as evidenced by more pronounced grimaces on the left side of the mouth, which is suggestive of right hemisphere dominance in monkeys and great apes (7,8), as has been documented in humans (10).…”

Section: Introductionmentioning

confidence: 99%

Brain activation lateralization in monkeys (Papio Anubis) following asymmetric motor and auditory stimulations through functional Near Infrared Spectroscopy

Debracque

Gruber

Lacoste

et al. 2020

Preprint

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Hemispheric asymmetries have long been seen as characterizing the human brain; yet, an increasing number of reports suggest the presence of such brain asymmetries in our closest primate relatives. However, most available data in non-human primates have so far been acquired as part of neurostructural approaches such as MRI, while comparative data in humans are often dynamically acquired as part of neurofunctional studies. In the present exploratory study in baboons (Papio Anubis), we tested whether brain lateralization could be recorded non-invasively using a functional Near-Infrared Spectroscopy (fNIRS) device in two contexts: motor and auditory passive stimulations. Under light propofol anaesthesia monitoring, three adult female baboons were exposed to a series of (1) left-versus right-arm passive movement stimulations; and (2) left-versus right-ear versus stereo auditory stimulations while recording fNIRS signals in the related brain areas (i.e., motor central sulcus and superior temporal cortices respectively). For the motor condition our results show that left-arm versus right-arm stimulations induced typical contralateral difference in hemispheric activation asymmetries in the three subjects for all three channels. For the auditory condition, we also revealed typical human-like patterns of hemispheric asymmetries in one subject for all three channels, namely (1) typical contralateral differences in hemispheric asymmetry between left-ear versus right-ear stimulations, and (2) a rightward asymmetry for stereo stimulations. Overall, our findings support the use of fNIRS to investigate brain processing in non-human primates from a functional perspective, opening the way for the development of non-invasive procedures in non-human primate brain research.

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

Cited by 37 publications

References 52 publications

From Smart Apes to Human Brain Boxes. A Uniquely Derived Brain Shape in Late Hominins Clade

From Smart Apes to Human Brain Boxes. A Uniquely Derived Brain Shape in Late Hominins Clade

Cerebral Sulcal Asymmetry in Macaque Monkeys

Brain activation lateralization in monkeys (Papio Anubis) following asymmetric motor and auditory stimulations through functional Near Infrared Spectroscopy

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