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

ABSTRACT: The inferior parietal lobule (IPL) is one of the most expanded cortical regions in humans relative to other primates. It is also among the most structurally and functionally asymmetric regions in the human cerebral cortex. Whether the structural and connectional asymmetries of IPL subdivisions differ across primate species and how this relates to functional asymmetries remain unclear. We identified IPL subregions that exhibited positive allometric in both hemispheres, scaling across rhesus macaque monkeys, chimpanzees, and humans. The patterns of IPL subregions asymmetry were similar in chimpanzees and humans, but no IPL asymmetries were evident in macaques. Among the comparative sample of primates, humans showed the most widespread asymmetric connections in the frontal, parietal, and temporal cortices, constituting leftward asymmetric networks that may provide an anatomical basis for language and tool use. Unique human asymmetric connectivity between the IPL and primary motor cortex might be related to handedness. These findings suggest that structural and connectional asymmetries may underlie hemispheric specialization of the human brain.

SUBMITTER: Cheng L

PROVIDER: S-EPMC8257252 | biostudies-literature | 2021 Jul

REPOSITORIES: biostudies-literature

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

Cheng Luqi L Zhang Yuanchao Y Li Gang G Wang Jiaojian J Sherwood Chet C Gong Gaolang G Fan Lingzhong L Jiang Tianzi T

eLife 20210702

The inferior parietal lobule (IPL) is one of the most expanded cortical regions in humans relative to other primates. It is also among the most structurally and functionally asymmetric regions in the human cerebral cortex. Whether the structural and connectional asymmetries of IPL subdivisions differ across primate species and how this relates to functional asymmetries remain unclear. We identified IPL subregions that exhibited positive allometric in both hemispheres, scaling across rhesus macaq ...[more]

PMID: 34219649

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Project description:Humans have a distinguishing ability for fine motor control that is subserved by a highly evolved cortico-motor neuronal network. The acquisition of a particular motor skill involves a long series of practice movements, trial and error, adjustment and refinement. At the cortical level, this acquisition begins in the parieto-temporal sensory regions and is subsequently consolidated and stratified in the premotor-motor cortex. Task-specific dystonia can be viewed as a corruption or loss of motor control confined to a single motor skill. Using a multimodal experimental approach combining neuroimaging and non-invasive brain stimulation, we explored interactions between the principal nodes of the fine motor control network in patients with writer's cramp and healthy matched controls. Patients and healthy volunteers underwent clinical assessment, diffusion-weighted MRI for tractography, and functional MRI during a finger tapping task. Activation maps from the task-functional MRI scans were used for target selection and neuro-navigation of the transcranial magnetic stimulation. Single- and double-pulse TMS evaluation included measurement of the input-output recruitment curve, cortical silent period, and amplitude of the motor evoked potentials conditioned by cortico-cortical interactions between premotor ventral (PMv)-motor cortex (M1), anterior inferior parietal lobule (aIPL)-M1, and dorsal inferior parietal lobule (dIPL)-M1 before and after inducing a long term depression-like plastic change to dIPL node with continuous theta-burst transcranial magnetic stimulation in a randomized, sham-controlled design. Baseline dIPL-M1 and aIPL-M1 cortico-cortical interactions were facilitatory and inhibitory, respectively, in healthy volunteers, whereas the interactions were converse and significantly different in writer's cramp. Baseline PMv-M1 interactions were inhibitory and similar between the groups. The dIPL-PMv resting state functional connectivity was increased in patients compared to controls, but no differences in structural connectivity between the nodes were observed. Cortical silent period was significantly prolonged in writer's cramp. Making a long term depression-like plastic change to dIPL node transformed the aIPL-M1 interaction to inhibitory (similar to healthy volunteers) and cancelled the PMv-M1 inhibition only in the writer's cramp group. These findings suggest that the parietal multimodal sensory association region could have an aberrant downstream influence on the fine motor control network in writer's cramp, which could be artificially restored to its normal function.

Project description:The nature of the relationship between structure and function is a fundamental question in neuroscience, especially at the macroscopic neuroimaging level. Although mounting studies have revealed that functional connectivity reflects structural connectivity, whether similar structural and functional connectivity patterns can reveal corresponding similarities in the structural and functional topography remains an open problem. In our current study, we used the right inferior parietal lobule (RIPL), which has been demonstrated to have similar anatomical and functional connectivity patterns at the subregional level, to directly test the hypothesis that similar structural and functional connectivity patterns can inform the corresponding topography of this area. In addition, since the association between the RIPL regions and particular functions and networks is still largely unknown, post-hoc functional characterizations and connectivity analyses were performed to identify the main functions and cortical networks in which each subregion participated. Anatomical and functional connectivity-based parcellations of the RIPL have consistently identified five subregions. Our functional characterization using meta-analysis-based behavioral and connectivity analyses revealed that the two anterior subregions (Cl1 and Cl2) primarily participate in interoception and execution, respectively; whereas the posterior subregion (Cl3) in the SMG primarily participates in attention and action inhibition. The two posterior subregions (Cl4, Cl5) in the AG were primarily involved in social cognition and spatial cognition, respectively. These results indicated that similar anatomical and functional connectivity patterns of the RIPL are reflected in corresponding structural and functional topographies. The identified cortical connectivity and functional characterization of each subregion may facilitate RIPL-related clinical research. Hum Brain Mapp 37:4316-4332, 2016. © 2016 Wiley Periodicals, Inc.

Dataset Information

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

Publications

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

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