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Research Articles, Systems/Circuits

Cortico-Subcortical Functional Connectivity Profiles of Resting-State Networks in Marmosets and Humans

Yuki Hori, David J. Schaeffer, Atsushi Yoshida, Justine C. Cléry, Lauren K. Hayrynen, Joseph S. Gati, Ravi S. Menon and Stefan Everling
Journal of Neuroscience 25 November 2020, 40 (48) 9236-9249; DOI: https://doi.org/10.1523/JNEUROSCI.1984-20.2020
Yuki Hori
1Centre for Functional and Metabolic Mapping, Robarts Research Institute, University of Western Ontario, London, Ontario N6A 5B7, Canada
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David J. Schaeffer
1Centre for Functional and Metabolic Mapping, Robarts Research Institute, University of Western Ontario, London, Ontario N6A 5B7, Canada
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Atsushi Yoshida
2Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, Maryland 20892
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Justine C. Cléry
1Centre for Functional and Metabolic Mapping, Robarts Research Institute, University of Western Ontario, London, Ontario N6A 5B7, Canada
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Lauren K. Hayrynen
1Centre for Functional and Metabolic Mapping, Robarts Research Institute, University of Western Ontario, London, Ontario N6A 5B7, Canada
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Joseph S. Gati
1Centre for Functional and Metabolic Mapping, Robarts Research Institute, University of Western Ontario, London, Ontario N6A 5B7, Canada
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Ravi S. Menon
1Centre for Functional and Metabolic Mapping, Robarts Research Institute, University of Western Ontario, London, Ontario N6A 5B7, Canada
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Stefan Everling
1Centre for Functional and Metabolic Mapping, Robarts Research Institute, University of Western Ontario, London, Ontario N6A 5B7, Canada
3Department of Physiology and Pharmacology, University of Western Ontario, London, Ontario N6A 5C1, Canada
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Figures

  • Figure 1.
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    Figure 1.

    Flowchart of analysis to calculate the subcortical connectivity maps. Each RS-fMRI scan was preprocessed, and (1) cortical and (2) subcortical regions were extracted using masks. (3) Using all cortical RS-fMRI datasets, group ICA (gICA) was performed so that 14 and 10 cortical RSNs were identified for marmosets and humans, respectively. (4) The time courses of each network in each scan were calculated using spatial regression technique and obtained cortical RSNs. (5) Then correlation coefficients between the time courses in each cortical network and the time courses in each subcortical voxel were calculated. Obtained correlation coefficient maps in each network were averaged across scans.

  • Figure 2.
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    Figure 2.

    Subcortical VOIs for marmosets (A) and humans (B). Subcortical volume of interests (VOIs) for marmosets (A) and humans (B). Only right-side VOIs are presented. SC: superior colliculus; IC: inferior colliculus; LGN: lateral geniculate nucleus; ANT: anterior part 735 of thalamic nucleus; LD: laterodorsal thalamic nucleus; MD: mediodorsal thalamic nucleus; VA: ventral anterior thalamic nucleus; VL: ventral lateral thalamic nucleus; VP: ventral posterior 737 thalamic nucleus; PUL: pulvinar nucleus.

  • Figure 3.
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    Figure 3.

    Fourteen components identified as RSNs in the marmosets. These networks were labeled based on previous studies (Belcher et al., 2013; Hori et al., 2020b) as follows: A, DMN. B, ATN. C, SAN. D, Left primary visual network (pVIS-Lt). E, Right primary VIS (pVIS-Rt). F, ORN. G–J, hVIS1-4. K-M, Somatomotor networks ventral (SMNv), dorsal (SMNd), and medial (SMNm). N, Premotor network (PMN). Color bar represents the z score of these correlation patterns thresholding at 2.3. White lines indicate the cytoarchitectonic borders for reference (Liu et al., 2018).

  • Figure 4.
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    Figure 4.

    Mean z score values in each subcortical area in each marmoset RSN. Error bars indicate SEM. The RSNs described here are corresponding to those in Figure 1. CAU, Caudate; PUT, putamen; HIPPO, hippocampus; AMY, amygdala.

  • Figure 5.
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    Figure 5.

    Representative subcortical z score maps for each RSN in marmosets. The z score maps were normalized to be maximum z value equal to 1, and were shown in sagittal, coronal, and axial slices deemed most representative of the activation patterns. A, DMN (corresponding to Fig. 3A). B, ATN (corresponding to Fig. 3B). C, SAN (corresponding to Fig. 3C). D, Primary visual network (pVIS: corresponding to Fig. 3E). E, ORN (corresponding to Fig. 3F). F, High-order VIS (corresponding to Fig. 3I). G, Somatomotor network (SMN) medial sensory part (corresponding to Fig. 3M). H, Premotor network (PMN) (corresponding to Fig. 3N).

  • Figure 6.
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    Figure 6.

    A parcellation of the marmoset subcortical area. The network with the highest z value among all networks was assigned as the main network related to the voxel. Colors on the surfaces and volumes are corresponding to the name of networks in Figure 3.

  • Figure 7.
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    Figure 7.

    Ten components identified as RSNs in humans. These networks were labeled based on a previous study (Ji et al., 2019) as follows: A, DMN. B, FPN. C, ATN. D, Somatomotor network ventral part (SMN1). E, SMN dorsomedial part (SMN2). F, AUD. G, Primary visual network (pVIS). H, High-order VIS (hVIS). I, LAN. J, CON. Color bar represents the z score of these correlation patterns thresholding at 3.1. White lines indicate the parcellation borders created based on the multimodal magnetic resonance images from Human Connectome Project (Glasser et al., 2016).

  • Figure 8.
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    Figure 8.

    Mean z score values in each subcortical area in each human RSN. Error bars indicate SEM. RSNs (corresponding to those in Fig. 7). CAU, Caudate; PUT, putamen; HIPPO, hippocampus; AMY, amygdala.

  • Figure 9.
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    Figure 9.

    Representative subcortical z score maps for each RSN. The z score maps were normalized to be maximum z value equal to 1, and were shown in sagittal, coronal, and axial slices deemed most representative of the activation patterns. A, DMN (corresponding to Fig. 4A). B, FPN (corresponding to Fig. 4B). C, ATN (corresponding to Fig. 4C). D, Somatomotor network dorsal part (SMNd: corresponding to Fig. 4E). E, AUD (corresponding to Fig. 4F). F, Primary visual network (corresponding to Fig. 4G). G, LGN (corresponding to Fig. 4I). H, CON (corresponding to Fig. 4J).

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    Figure 10.

    The similarity of subcortical network patterns between marmosets and humans. Manhattan distance between these species were plotted in matrix form. Significant similarities were marked by an asterisk within the matrix.

  • Figure 11.
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    Figure 11.

    Matching human DMN to marmoset DMN in subcortical areas. A, z score maps were shown in sagittal slices focused on the hippocampus, which has the strongest connections in both species. A single-color palette applies to two species but is scaled according to percentile ranges within each species rather than to absolute values. B, A fingerprint shows the matching connectivity patterns between marmosets and humans. Red and green areas represent marmoset and human fingerprints, respectively. CAU, Caudate; PUT, putamen; HIPPO, hippocampus; AMY, amygdala.

  • Figure 12.
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    Figure 12.

    Matching human FPN to marmoset ATN, ORN, and hVIS1 in subcortical area. A, z score maps were shown in axial slices focused on the caudate, which has the strongest connections in both species. A single-color palette applies to two species but is scaled according to percentile ranges within each species rather than to absolute values. B–D, Fingerprints show the matching connectivity patterns between marmosets and humans. Red and green areas represent marmoset and human fingerprints, respectively. CAU, Caudate; PUT, putamen; HIPPO, hippocampus; AMY, amygdala.

  • Figure 13.
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    Figure 13.

    Matching human LAN to marmoset ATN in subcortical area. A, z score maps were shown in coronal slices focused on the caudate and amygdala, which have strong connections in both species. A single-color palette applies to two species but is scaled according to percentile ranges within each species rather than to absolute values. B, Fingerprint shows the matching connectivity pattern between marmosets and humans. Red and green areas represent marmoset and human fingerprints, respectively. CAU, Caudate; PUT, putamen; HIPPO, hippocampus; AMY, amygdala.

  • Figure 14.
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    Figure 14.

    Matching human pVIS to marmoset VISs (pVIS-Lt, pVIS-Rt, hVIS3, and hVIS4) in subcortical area. A, z score maps for each were shown in axial slices focused on the superior colliculus and LGN, which have strong connections in both species. A single-color palette applies to two species but is scaled according to percentile ranges within each species rather than to absolute values. B–E, Fingerprints show the matching connectivity patterns between marmosets and humans. Red and green areas represent marmoset and human fingerprints, respectively. CAU, Caudate; PUT, putamen; HIPPO, hippocampus; AMY, amygdala.

  • Figure 15.
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    Figure 15.

    Matching human secondary visual network (hVIS) to marmoset high-order visual network (hVIS4) in subcortical area. A, z score maps were shown in axial slices focused on the superior colliculus and LGN, which have strong connections in both species. A single-color palette applies to two species but is scaled according to percentile ranges within each species rather than to absolute values. B, A fingerprint shows the matching connectivity patterns between marmosets and humans. Red and green areas represent marmoset and human fingerprints, respectively. CAU, Caudate; PUT, putamen; HIPPO, hippocampus; AMY, amygdala.

  • Figure 16.
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    Figure 16.

    Matching human CON to marmoset ORN and high-order visual networks (hVIS1) in subcortical area. A, z score maps were shown in axial slices focused on the caudate and putamen, which have strong connections in both species. A single-color palette applies to two species but is scaled according to percentile ranges within each species rather than to absolute values. B, C, Fingerprints show the matching connectivity patterns between marmosets and humans. Red and green areas represent marmoset and human fingerprints, respectively. CAU, Caudate; PUT, putamen; HIPPO, hippocampus; AMY, amygdala.

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The Journal of Neuroscience: 40 (48)
Journal of Neuroscience
Vol. 40, Issue 48
25 Nov 2020
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Cortico-Subcortical Functional Connectivity Profiles of Resting-State Networks in Marmosets and Humans
Yuki Hori, David J. Schaeffer, Atsushi Yoshida, Justine C. Cléry, Lauren K. Hayrynen, Joseph S. Gati, Ravi S. Menon, Stefan Everling
Journal of Neuroscience 25 November 2020, 40 (48) 9236-9249; DOI: 10.1523/JNEUROSCI.1984-20.2020

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Cortico-Subcortical Functional Connectivity Profiles of Resting-State Networks in Marmosets and Humans
Yuki Hori, David J. Schaeffer, Atsushi Yoshida, Justine C. Cléry, Lauren K. Hayrynen, Joseph S. Gati, Ravi S. Menon, Stefan Everling
Journal of Neuroscience 25 November 2020, 40 (48) 9236-9249; DOI: 10.1523/JNEUROSCI.1984-20.2020
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Keywords

  • cortex
  • marmoset
  • resting-state fMRI
  • subcortex

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