Brain intrinsic connection patterns underlying tool processing in human adults are present in neonates and not in macaques

Wen, Haojie; Xu, Ting; Wang, Xiaoying; Yu, Xianchuan; Bi, Yanchao

doi:10.1016/j.neuroimage.2022.119339

Cited by 5 publications

(5 citation statements)

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“…3.2, Ps corrected , 0.01; df = 167). Using the HCP RSFC data preprocessed in Wen at al. (2022), the results again showed strong alignment between the RSFC pattern and the functional activation pattern in pulvinar (for animals: within-domain r = 0.43, between-domain mean r = 0.03, within-vs betweendomain, Hotelling's t values .…”

Section: Individual Lateralization Resultsmentioning

confidence: 99%

“…One of the broad principles of visual object processing in the human cortex is domain structure. Viewing several domains of objects, including animals, small manipulable objects (tools), and large nonmanipulable objects, has been found to elicit different patterns of response in distributed cortical regions, including and beyond the ventral temporal cortex, which has been explained by their association with evolutionary-salient functions, such as fight-or-flight (animals) or manipulation (tools) (He et al, 2013;Konkle and Caramazza, 2013;Garcea and Buxbaum, 2019;Schone et al, 2021;Wen et al, 2022; for review, see Bi et al, 2016;Peelen and Downing, 2017). Viewing tools elicits activation in a left-lateralized cortical network, including the left lateral occipitotemporal cortex, the inferior and superior parietal lobule, and the medial fusiform gyrus, which have been proposed to process various properties of tools that support its shape, use, and function (Brandi et al, 2014;Fabbri et al, 2016;Chen et al, 2018;Wang et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

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Pulvinar Response Profiles and Connectivity Patterns to Object Domains

et al. 2023

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Distributed cortical regions show differential responses to visual objects belonging to different domains varying by animacy (e.g., animals vs tools), yet it remains unclear whether this is an organization principle also applying to the subcortical structures. Combining multiple fMRI activation experiments (two main experiments and six validation datasets; 12 females and 9 males in the main Experiment 1; 10 females and 10 males in the main Experiment 2), resting-state functional connectivity, and task-based dynamic causal modeling analysis in human subjects, we found that visual processing of images of animals and tools elicited different patterns of response in the pulvinar, with robust left lateralization for tools, and distinct, bilateral (with rightward tendency) clusters for animals. Such domain-preferring activity distribution in the pulvinar was associated with the magnitude with which the voxels were intrinsically connected with the corresponding domain-preferring regions in the cortex. The pulvinar-to-right-amygdala path showed a one-way shortcut supporting the perception of animals, and the modulation connection from pulvinar to parietal showed an advantage to the perception of tools. These results incorporate the subcortical regions into the object processing network and highlight that domain organization appears to be an overarching principle across various processing stages in the brain.Significance Statement:Viewing objects belonging to different domains elicited different cortical regions, but whether the domain organization applied to the subcortical structures (e.g., pulvinar) was unknown. Multiple fMRI activation experiments revealed that object pictures belonging to different domains elicited differential patterns of response in the pulvinar, with robust left lateralization for tool pictures, and distinct, bilateral (with rightward tendency) clusters for animals. Combining the resting-state functional connectivity and dynamic causal modeling analysis on task-based fMRI data, we found domain-preferring activity distribution in the pulvinar aligned with that in cortical regions. These results highlight the need for coherent visual theories that explain the mechanisms underlying the domain organization across various processing stages.

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Section: Individual Lateralization Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Pulvinar Response Profiles and Connectivity Patterns to Object Domains

et al. 2023

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“…Since the Brainnetome Atlases in both humans and macaques have been completed, they offer a potential path for understanding brain evolution by comparative connectivities based on fine-grained brain parcellations across species. Many interesting topics related to evolutionary mechanisms, such as language and tool use, could be explored from the perspective of the Brainnetome Atlases 30,93,94 .…”

Section: Discussionmentioning

confidence: 99%

Macaque Brainnetome Atlas: A Multifaceted Brain Map with Parcellation, Connection, and Histology

Cui

Cao

et al. 2022

Preprint

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The rhesus macaque (Macaca mulatta) is a crucial experimental animal that shares many genetic, brain organizational, and behavioral characteristics with humans. A macaque brain atlas that identifies anatomically and functionally distinct regions is fundamental to biomedical and evolutionary research. However, even though connectivity information is vital for understanding brain functions, a connectivity-based whole-brain atlas of the macaque has not previously been made. In this study, we created a new whole-brain map, the Macaque Brainnetome Atlas, based on the anatomical connectivity profile provided by high-resolution angular and spatial diffusion MRI data. The new atlas consists of 248 cortical and 56 subcortical regions as well as their structural and resting-state functional connections. We systematically evaluated the parcellations and connections using multi-site and multi-modal datasets to ensure reproducibility and reliability. The resulting resource, which is downloadable fromhttp://atlas.brainnetome.org, includes (1) the thoroughly delineated Macaque Brainnetome Atlas (MacBNA), (2) the multi-modal connections, (3) the largest postmortem high resolution macaque dMRI dataset, and (4) ex vivo MRI, block-face, and Nissl-stained images obtained from a different macaque. We provide an exemplar use of the resource with a joint multi-modal and multi-scale utilization of MRI and Nissl data with our atlas as a reference system. The goals of the resource are not only to provide a backbone of the mesoscopic connectivity and a multi-omics (such as transcriptomes and proteomes) atlas but also to facilitate translational medicine, cross-species comparisons, and computational modelling, enriching the collaborative resource platform of nonhuman primate data.

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“…Although non-human primates share many tool capabilities, humans uniquely show greater manual dexterity and conceptual knowledge of tool use 70 . Considerable divergence was found in the tool processing network nodes 70,77 , the inferior frontal gyrus, and the most rostroventral inferior parietal lobule (A40rv). These two regions were connected by the IFOF and SLF3, which have been linked with the human tool-use circuit [78][79][80] and showed a different connectivity pattern between chimpanzees and humans.…”

Section: Connectivity Divergence Between Speciesmentioning

confidence: 99%

Comparative Analysis of Human-Chimpanzee Divergence in Brain Connectivity and its Genetic Correlates

Wang,

Cheng,

et al. 2024

Preprint

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Chimpanzees (Pan troglodytes) are humans’ closest living evolutionary relatives, making them the most directly relevant comparison point for understanding human brain evolution. By zeroing in on the differences in brain connectivity between humans and chimpanzees, it can provide key insights into the specific evolutionary changes that occurred along the human lineage. However, conducting fair comparisons of brain connectivity between humans and chimpanzees remains challenging, as cross-species brain atlases established within the same framework are currently lacking. Without the availability of cross-species brain atlases, the region-wise connectivity patterns between humans and chimpanzees cannot be directly compared. To address this gap, we built the first Chimpanzee Brainnetome Atlas (ChimpBNA) by following the well-established connectivity-based parcellation framework. Leveraging this new resource, we found substantial divergence in connectivity patterns across most association cortices, notably in the lateral temporal and dorsolateral prefrontal cortex between the two species. Intriguingly, these patterns significantly deviate from the expected cortical expansion during brain evolution. Additionally, we identified regions displaying connectional asymmetries between species, likely resulting from evolutionary divergence. Genes associated with these divergent connectivities were found to be enriched in cell types crucial for cortical projection circuits and synapse formation. These genes exhibited more pronounced differences in expression patterns in regions with higher connectivity divergence, suggesting a potential foundation for brain connectivity evolution. Therefore, our study not only provides a fine-scale brain atlas of chimpanzees but also highlights the connectivity divergence between humans and chimpanzees in a more rigorous and comparative manner and suggests potential genetic underpinnings for the observed divergence in brain connectivity patterns between the two species. This can help us better understand the origins and development of uniquely human cognitive capabilities.

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Brain intrinsic connection patterns underlying tool processing in human adults are present in neonates and not in macaques

Cited by 5 publications

References 81 publications

Pulvinar Response Profiles and Connectivity Patterns to Object Domains

Pulvinar Response Profiles and Connectivity Patterns to Object Domains

Macaque Brainnetome Atlas: A Multifaceted Brain Map with Parcellation, Connection, and Histology

Comparative Analysis of Human-Chimpanzee Divergence in Brain Connectivity and its Genetic Correlates

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