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Research Articles, Behavioral/Cognitive

Pulvinar Response Profiles and Connectivity Patterns to Object Domains

Haojie Wen, Yingchao Song, Meng Liang, Peng Zhang, Xiaoying Wang and Yanchao Bi
Journal of Neuroscience 1 February 2023, 43 (5) 812-826; DOI: https://doi.org/10.1523/JNEUROSCI.0613-22.2022
Haojie Wen
1State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, 100875, China
2IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, 100875, China
3Beijing Key Laboratory of Brain Imaging and Connectomics, Beijing Normal University, Beijing, 100875, China
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Yingchao Song
4School of Medical Technology, School of Medical Imaging, Tianjin Key Laboratory of Functional Imaging, Tianjin Medical University, Tianjin, 300070, China
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Meng Liang
4School of Medical Technology, School of Medical Imaging, Tianjin Key Laboratory of Functional Imaging, Tianjin Medical University, Tianjin, 300070, China
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Peng Zhang
5State Key Laboratory of Brain and Cognitive Science, Beijing MRI Center for Brain Research, Institute of Biophysics, Chinese Academy of Sciences, Beijing, 100101, China
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Xiaoying Wang
1State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, 100875, China
2IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, 100875, China
3Beijing Key Laboratory of Brain Imaging and Connectomics, Beijing Normal University, Beijing, 100875, China
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Yanchao Bi
1State Key Laboratory of Cognitive Neuroscience and Learning, Beijing Normal University, Beijing, 100875, China
2IDG/McGovern Institute for Brain Research, Beijing Normal University, Beijing, 100875, China
3Beijing Key Laboratory of Brain Imaging and Connectomics, Beijing Normal University, Beijing, 100875, China
6Chinese Institute for Brain Research, Beijing, 102206, China
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Abstract

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.

  • animal domain network
  • domain selectivity
  • pulvinar
  • subcortical
  • tool domain network

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The Journal of Neuroscience: 43 (5)
Journal of Neuroscience
Vol. 43, Issue 5
1 Feb 2023
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Pulvinar Response Profiles and Connectivity Patterns to Object Domains
Haojie Wen, Yingchao Song, Meng Liang, Peng Zhang, Xiaoying Wang, Yanchao Bi
Journal of Neuroscience 1 February 2023, 43 (5) 812-826; DOI: 10.1523/JNEUROSCI.0613-22.2022

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Pulvinar Response Profiles and Connectivity Patterns to Object Domains
Haojie Wen, Yingchao Song, Meng Liang, Peng Zhang, Xiaoying Wang, Yanchao Bi
Journal of Neuroscience 1 February 2023, 43 (5) 812-826; DOI: 10.1523/JNEUROSCI.0613-22.2022
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Keywords

  • animal domain network
  • domain selectivity
  • pulvinar
  • subcortical
  • tool domain network

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