Motor skill for tool-use is associated with asymmetries in Broca’s area and the motor hand area of the precentral gyrus in chimpanzees ( Pan troglodytes )

Abstract

Among nonhuman primates, chimpanzees are well known for their sophistication and diversity of tool use in both captivity and the wild. The evolution of tool manufacture and use has been proposed as a driving mechanism for the development of increasing brain size, complex cognition and motor skills, as well as the population-level handedness observed in modern humans. Notwithstanding, our understanding of the neurological correlates of tool use in chimpanzees and other primates remains poorly understood. Here, we assessed the hand preference and performance skill of chimpanzees on a tool use task and correlated these data with measures of neuroanatomical asymmetries in the inferior frontal gyrus (IFG) and the pli-de-passage fronto-parietal moyen (PPFM). The IFG is the homolog to Broca’s area in the chimpanzee brain and the PPFM is a buried gyrus that connects the pre- and post-central gyri and corresponds to the motor-hand area of the precentral gyrus. We found that chimpanzees that performed the task better with their right compared to left hand showed greater leftward asymmetries in the IFG and PPFM. This association between hand performance and PPFM asymmetry was particularly robust for right-handed individuals. Based on these findings, we propose that the evolution of tool use was associated with increased left hemisphere specialization for motor skill. We further suggest that lateralization in motor planning, rather than hand preference per se, was selected for with increasing tool manufacture and use in Hominid evolution.

Hand preferences and differences in extractive foraging in seven capuchin monkey species

“…Moreover, the manipulative complexity of extractive foraging seems to intensify during tool use, which requires diverse manual actions combined with strength, precision, bimanually coordinated movements, and more cognitive skills (Heldstab et al, ; Parker & Gibson, ; Resende, Nagy‐Reis, Lacerda, Pagnnota, & Savalli, ). Tool use is considered as a driver for right handedness (e.g., Forrester, Quaresmini, Leavens, Mareschal, & Thomas, ; Frost, ; Hopkins et al, ; Moura, ). Thus, we expected that S. libidinosus , a species that evolved in the dry forests of Brazil (Cerrado & Caatinga, Alfaro, Boubli, et al, ) should be more right handed.…”

“…These populations of capuchins spend significantly more time consuming leaves than capuchins from the Caatinga dry forest, which tend to spend more time foraging for mobile prey (Izar et al, ). It is possible that capuchin monkeys from the Atlantic forest evolved under a stronger selective pressure for high reliance on bimanual feeding and extractive foraging, which requires more sequential actions and planning and might put a stronger selective pressure on left hemisphere/right hand use (Cochet & Byrne, ; Hopkins et al, ). Unfortunately, there is no published study on the feeding ecology of S. flavius and detailed data on manipulative and extractive foraging techniques employed by Atlantic forest capuchins is also lacking.…”

“…Indeed, when the tasks being performed are skillful, requiring fine motor control, and cognitive abilities (e.g., activities requiring complementary use of hands, extractive foraging, and tool use) increased laterality and hand preference emerges (e.g., Bardo, Pouydebat, & Meunier, ; Fagot & Vauclair, ; Hopkins, ; Hopkins, Russell, & Cantalupo, ; MacNeilage, ; Marchant & McGrew, ). According to some authors the consequences of the increasing demand for higher motor skill associated with tool use could lead to right handedness (Frost, ; Hopkins et al, ; MacNeilage, ; Westergaard & Suomi, ). Yet, conflicting results occur even when these cognitively demanding tasks are used (Schweitzer, Bec, & Blois‐Heulin, ).…”

Mapping hemispheric asymmetries of the macaque cerebral cortex during early brain development

“…In fact, neuroimaging studies of nonhuman primates have shown that certain hemispheric asymmetries found in human brains are also present in chimpanzees (Gannon, Holloway, Broadfield, & Braun, ; Hopkins et al, ; Lyn et al, ) and Old World monkeys, such as baboons (Marie et al, ) and macaque monkeys (Bogart et al, ). For instance, the left inferior frontal gyrus (IFG) and left planum temporale (PT), which are involved in language production and comprehension skills in human (Bogart et al, ), have been shown larger and deeper than those on the right hemisphere in chimpanzees and baboons (Gannon et al, ; Hopkins, Marino, Rilling, & MacGregor, ; Lyn et al, ; Marie et al, ), similar to the findings in human infants, old children, and adults (Glasel et al, ; Hill et al, ; Li, Nie, Wang, et al, ).…”

Handedness in gestural and manipulative actions in male hunter‐gatherer Aka pygmies from Central African Republic

“…The tool theory (Forrester, Quaresmini, Leavens, Mareschal, & Thomas, ; Kimura, ) states that manual specialization when using tools, and more broadly in manipulative actions, is related to the necessary hemispheric lateralization to support language functions. However, neuroanatomical investigations revealed contrasting results (Balzeau, Gilissen, Holloway, Prima, & Grimaud‐Hervé, ; Hopkins & Cantalupo, ; Hopkins et al, ). Around 63% of strong left‐handers had after all a dominant left‐hemisphere for language (Knecht et al, ).…”