Connectional asymmetry of the inferior parietal lobule shapes hemispheric specialization in humans, chimpanzees, and rhesus macaques

Cheng, Luqi; Zhang, Yuanchao; Li, Gang; Wang, Jiaojian; Sherwood, Chet C.; Gong, Gaolang; Fan, Lingzhong; Jiang, Tianzi

doi:10.7554/elife.67600

Cited by 32 publications

(25 citation statements)

References 76 publications

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“…Our study even points to one specific anterior subdivision of the supramarginal gyrus, namely area PFt, missing in earlier monkey neurophysiology models 7 , 30 . This typically human area 16 emerged via expansion of the left hemisphere partly due to pressure on development of tool production and tool use skills 6 , 31 , 32 . Yet, here we have identified and emphasize a new role of the right PFt in controlling/using complex tools in humans.…”

Section: Discussionmentioning

confidence: 99%

“…Consistent with this notion, only in humans does the rostral part of the inferior parietal lobule (IPL) in the left hemisphere respond to observation of tool use actions 4 , even when the tools just extend or amplify the acting hand. Whether or not left IPL, one of the most expanded and lateralized association regions in the human brain 5 , 6 , is the seat of the ability for skilled use of complex tools is still an open question.…”

Section: Introductionmentioning

confidence: 99%

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Complex tools and motor-to-mechanical transformations

Ras

Wyrwa

Stachowiak

et al. 2022

Sci Rep

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The ability to use complex tools is thought to depend on multifaceted motor-to-mechanical transformations within the left inferior parietal lobule (IPL), linked to cognitive control over compound actions. Here we show using neuroimaging that demanding transformations of finger movements into proper mechanical movements of functional parts of complex tools invoke significantly the right rather than left rostral IPL, and bilateral posterior-to-mid and left anterior intraparietal sulci. These findings emerged during the functional grasp and tool-use programming phase. The expected engagement of left IPL was partly revealed by traditional region-of-interest analyses, and further modeling/estimations at the hand-independent level. Thus, our results point to a special role of right IPL in supporting sensory-motor spatial mechanisms which enable an effective control of fingers in skillful handling of complex tools. The resulting motor-to-mechanical transformations involve dynamic hand-centered to target-centered reference frame conversions indispensable for efficient interactions with the environment.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Complex tools and motor-to-mechanical transformations

Ras

Wyrwa

Stachowiak

et al. 2022

Sci Rep

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“…The ventral premotor mainly controlled the hand (Kraskov et al 2009) and orofacial (Ferrari et al 2003) musculature. IPL also was demonstrated by the recent study to be homologous in the primate and was mainly involved in the tool use and language (Cheng et al 2021). Taken together, the Idd and Igd may be a participant in the hand control and orofacial motor in the rhesus monkey, such as vocalization.…”

Section: Discussionmentioning

confidence: 94%

Structural connectivity gradient associated with a dichotomy reveals the topographic organization of the macaque insular cortex

Cao

Cui

et al. 2022

Preprint

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Histology studies revealed that the macaque insular cortex was characterized by the gradual organizations containing agranular, dysgranular and granular insula. However, no consensus has been reached on the elaborate subdivisions of macaque insula. Until now, no neuroimaging study to our knowledge combining connectivity-based gradients and parcellation has been performed to investigate the topographic organization of the macaque insular cortex. In this study, we used high-resolution ex vivo diffusion-weighted imaging data to explore the macaque insular cortex's global gradient organization and subdivisions. We found a rostrocaudal organization of the dominant gradient in the macaque insula using a diffusion map embedding. Meanwhile, extracting the 25% top and bottom components from the dominant and second gradient, which explained variance over 60% in total within ten gradients, the connectivity-based parcellation method was performed to subdivide each component into two subregions confirmed by the cross-validation analysis. Furthermore, permutations tests identified that two subregions from each component showed significant differences between their connectivity fingerprints. Finally, we found that the dominant and second gradients were significantly correlated with the T1w/T2w and cortical thickness maps in the macaque insula. Taken together, the global gradients combining the subdivisions examined the topographic organization of the macaque insular cortex based on the structural connectivity, which may contribute to a better understanding of the intricate insular cortex anatomy.

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“…Such mental processes are absent in chimpanzees (Povinelli 2000), although this species can make and use simple tools and construct simple artifacts as nests. These mental processes are only present in humans, probably due to the expansion of the parietal lobe, to the inferior parietal cortex connectional asymmetries and to the emergence of hemispheric specialization across evolution (Cheng et al 2021).…”

Section: Introductionmentioning

confidence: 99%

The parietal lobe evolution and the emergence of material culture in the human genus

2022

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Traditional and new disciplines converge in suggesting that the parietal lobe underwent a considerable expansion during human evolution. Through the study of endocasts and shape analysis, paleoneurology has shown an increased globularity of the braincase and bulging of the parietal region in modern humans, as compared to other human species, including Neandertals. Cortical complexity increased in both the superior and inferior parietal lobules. Emerging fields bridging archaeology and neuroscience supply further evidence of the involvement of the parietal cortex in human-specific behaviors related to visuospatial capacity, technological integration, self-awareness, numerosity, mathematical reasoning and language. Here, we complement these inferences on the parietal lobe evolution, with results from more classical neuroscience disciplines, such as behavioral neurophysiology, functional neuroimaging, and brain lesions; and apply these to define the neural substrates and the role of the parietal lobes in the emergence of functions at the core of material culture, such as tool-making, tool use and constructional abilities.

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Connectional asymmetry of the inferior parietal lobule shapes hemispheric specialization in humans, chimpanzees, and rhesus macaques

Cited by 32 publications

References 76 publications

Complex tools and motor-to-mechanical transformations

Complex tools and motor-to-mechanical transformations

Structural connectivity gradient associated with a dichotomy reveals the topographic organization of the macaque insular cortex

The parietal lobe evolution and the emergence of material culture in the human genus

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