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Research ArticleResearch Article: New Research, Sensory and Motor Systems

Parallel Streams of Direct Corticogeniculate Feedback from Mid-level Extrastriate Cortex in the Macaque Monkey

Matthew Adusei, Edward M. Callaway, W. Martin Usrey and Farran Briggs
eNeuro 13 March 2024, 11 (3) ENEURO.0364-23.2024; https://doi.org/10.1523/ENEURO.0364-23.2024
Matthew Adusei
1Neuroscience Graduate Program, University of Rochester, Rochester, New York 14642
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Edward M. Callaway
2Systems Neurobiology Laboratory, Salk Institute for Biological Sciences, La Jolla, California 92037
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W. Martin Usrey
3Center for Neuroscience, University of California Davis, Davis, California 95618
4Department of Neurobiology, Physiology, and Behavior, University of California Davis, Davis, California 95616
5Department of Neurology, University of California Davis, Davis, California 95618
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Farran Briggs
1Neuroscience Graduate Program, University of Rochester, Rochester, New York 14642
6Del Monte Institute for Neuroscience, University of Rochester School of Medicine and Dentistry, Rochester, New York 14642
7Department of Neuroscience, University of Rochester School of Medicine and Dentistry, Rochester, New York 14642
8Department of Brain and Cognitive Sciences, University of Rochester, Rochester, New York 14627
9Center for Visual Science, University of Rochester, Rochester, New York 14627
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  • Figure 1.
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    Figure 1.

    Virus-labeled corticogeniculate neurons originating in mid-level extrastriate areas MT, MST, and V4. A–H, Photographs of coronal sections through area MT (A,F), MST (C,E), and V4 (B,D,G,H), showing representative examples of reconstructed virus-labeled corticogeniculate neurons. Scale bar is 750 µm and applies to all images. Colored reconstructions are overlaid onto photographs and indicate cluster assignment described in Figure 2. The same eight reconstructions are reproduced in Figure 2B to visualize the arbors more clearly. I, Contour tracing of a coronal section showing relative locations of corticogeniculate neurons in A–H. Medial is left and dorsal is up. Area boundaries are indicated by white dashed lines and areas are labeled. Note that the single representative coronal section tracing was not the home section for each corticogeniculate reconstruction, but a section chosen because all three areas of interest were represented.

  • Figure 2.
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    Figure 2.

    Clustering of extrastriate corticogeniculate neurons by morphological type and area of origin. A, Dendrogram showing clustering of reconstructed extrastriate corticogeniculate neurons based on least-squared linkage distances between groups of neurons in an 11-dimensional space which represents each morphological metric (Tables 1–3). Colors indicate extrastriate area of origin of each corticogeniculate neuron: orange indicates MT, lime green indicates MST, and magenta indicates V4. Clusters are indicated by thin boxes with colored outlines representing cluster assignment (see legend). B, Representative examples of reconstructed corticogeniculate neurons in each cluster (color-coded based on cluster assignment). These are the same reconstructions illustrated in Figure 1A–H; additional reconstructions per cluster are illustrated in Figure 3. Layers are indicated by black lines, labeled at left, and are aligned to the layer 5/6 border per reconstruction. Scale bar at right is 750 µm and applies to all reconstructions. Area of origin is listed above each reconstruction; cluster number is listed below. Cell bodies are indicated by black outlines. C, Relationships between first, second, and third PC scores (arbitrary units) following PCA of the same 11 morphological metrics used in the cluster analysis; color coded from cluster analysis as in A and B. D, t-SNE plot generated from all PCA scores illustrating the first and second embeddings (arbitrary units); color coded from cluster analysis as in A and B. E, Pie charts illustrate the proportional distribution of extrastriate corticogeniculate neurons from each cluster within each area (cluster number indicated and clusters color-coded as in A).

  • Figure 3.
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    Figure 3.

    Corticogeniculate neurons per cluster. Additional examples of reconstructed corticogeniculate neurons in each cluster (color-coded based on cluster assignment as in Fig. 2 and labeled below each group). Layers are indicated by black lines, labeled at left, and are aligned to the layer 5/6 border per reconstruction. Scale bar at left is 750 µm and applies to all reconstructions. Cell bodies are indicated by black outlines.

  • Figure 4.
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    Figure 4.

    Quantitative assessment of morphological metrics for each cluster of extrastriate corticogeniculate neurons. Clusters are color coded according to cluster assignment (as in Figs. 1, 2; see legend at right). Notched box and whisker plots illustrate medians (horizontal black lines), 25th and 75th percentiles (notched boxes), data distributions (black lines above, below boxes), and outliers (black crosses). Asterisks with panel titles indicate the number of comparisons across clusters that were statistically significant (i.e., * = 1 or more significant differences between clusters, ** = 2+ statistically significant differences between clusters, etc.). See Tables 1–3 for all statistics. A, Cell body area, z-scored. B, Cell body position as percent depth in layer 6; WM indicates the white matter boundary. C, Height of the apical dendrite or tallest point on basal dendrite for spiny stellate cells. D–G, Percentage of apical dendrite (AD) in layers 6 (D), 5 (E), 4 (F), and 2/3 (G). H–K, Percentage of basal dendrite (BD) in WM (H), and in layers 6 (I), 5 (J), 4 (K).

Tables

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    Table 1.

    Average ± SEM for three morphological metrics included in the cluster analysis: cell body (CB) area (z-scored), cell body position as percent depth in layer 6 (L6) where larger values indicate deeper position closer to the white matter, and height of the apical dendrite (AD) as percent depth in the cortical layers where smaller values indicate shallower position closer to layer 1

    CB area (µm2)CB position in L6AD height
    Cluster 1 (n = 23)0.36 ± 0.2141.0 ± 4.276.9 ± 1.4
    Cluster 2 (n = 22)0.64 ± 0.2919.3 ± 2.163.7 ± 2.8
    Cluster 3 (n = 22)0.03 ± 0.2321.5 ± 2.624.0 ± 3.0
    Cluster 4 (n = 7)−0.14 ± 0.2111.1 ± 1.346.2 ± 3.6
    Cluster 5 (n = 25)0.08 ± 0.1618.8 ± 2.57.6 ± 1.7
    Cluster 6 (n = 13)−0.76 ± 0.1059.0 ± 2.06.8 ± 0.8
    Cluster 7 (n = 24)−0.31 ± 0.1669.8 ± 3.234.8 ± 3.2
    Cluster 8 (n = 14)−0.48 ± 0.1550.7 ± 6.333.3 ± 4.3
    p values5.8 × 10−51.2 × 10−171.2 × 10−23
    Differences1,2,3,5 > 61 > 2,4,5; 6,7,8 > 2,3,4,51 > 3,5,6,7,8; 2 > 3,5,6,8; 4,7 > 5,6
    • p values for statistical differences across clusters are Bonferroni corrected for multiple comparisons at α = 0.0045; Significant differences between clusters are also listed below.

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    Table 2.

    Average ± SEM for four morphological metrics included in the cluster analysis: percent of apical dendrite (AD) in layer 6 (L6), layer 5 (L5), layer 4 (L4), and layer 2/3 (L2/3)

    AD in L6AD in L5AD in L4AD in L2/3
    Cluster 1 (n = 23)0000
    Cluster 2 (n = 22)0000
    Cluster 3 (n = 22)14.2 ± 2.222.9 ± 2.445.4 ± 2.617.6 ± 2.2
    Cluster 4 (n = 7)15.9 ± 3.048.2 ± 2.035.2 ± 4.00.7 ± 0.6
    Cluster 5 (n = 25)7.4 ± 1.311.3 ± 1.220.9 ± 1.660.4 ± 2.5
    Cluster 6 (n = 13)28.3 ± 2.612.5 ± 1.322.9 ± 3.236.4 ± 4.9
    Cluster 7 (n = 24)40.0 ± 3.319.0 ± 2.827.0 ± 2.69.9 ± 2.5
    Cluster 8 (n = 14)66.3 ± 3.915.6 ± 2.611.3 ± 1.56.8 ± 2.8
    p values6.9 × 10−253.4 × 10−212.1 × 10−225.6 × 10−23
    Differences3,4,5,6 > 1,2; 7,8 > 1,2,3,53,5,6,7,8 > 1,2; 4 > 1,2,5,64,5,6,7,8 > 1,2; 3 > 1,2,5,7,83,8 > 1,2; 5 > 1,2,3,4,7,8; 6 > 1,2,4,7
    • Conventions as in Table 1.

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    Table 3.

    Average ± SEM for four morphological metrics included in the cluster analysis: percent of basal dendrite (BD) in the white matter (WM), and in layer 6 (L6), layer 5 (L5), and layer 4 (L4)

    BD in WMBD in L6BD in L5BD in L4
    Cluster 1 (n = 23)0.4 ± 0.498.4 ± 0.81.2 ± 0.50
    Cluster 2 (n = 22)0.4 ± 0.379.4 ± 2.820.3 ± 2.80
    Cluster 3 (n = 22)0.1 ± 0.191.4 ± 2.17.9 ± 1.90.6 ± 0.5
    Cluster 4 (n = 7)1.8 ± 1.691.5 ± 3.06.7 ± 3.10
    Cluster 5 (n = 25)091.0 ± 2.56.0 ± 1.73.0 ± 1.1
    Cluster 6 (n = 13)2.2 ± 0.896.1 ± 1.31.1 ± 0.70.5 ± 0.4
    Cluster 7 (n = 24)2.8 ± 1.591.5 ± 1.84.5 ± 1.01.2 ± 0.7
    Cluster 8 (n = 14)0.7 ± 0.497.3 ± 1.41.7 ± 0.90.3 ± 0.3
    p values5.0 × 10−61.5 × 10−75.7 × 10−101.7 × 10−5
    Differences6 > 1,2,3,5; 8 > 1,5; 7 > 51 > 2,3,5; 5,6,7 > 22 > 1,3,5,6,7,8; 3 > 1,65 > 1,2,3,4
    • Conventions as in Table 1.

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Parallel Streams of Direct Corticogeniculate Feedback from Mid-level Extrastriate Cortex in the Macaque Monkey
Matthew Adusei, Edward M. Callaway, W. Martin Usrey, Farran Briggs
eNeuro 13 March 2024, 11 (3) ENEURO.0364-23.2024; DOI: 10.1523/ENEURO.0364-23.2024

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Parallel Streams of Direct Corticogeniculate Feedback from Mid-level Extrastriate Cortex in the Macaque Monkey
Matthew Adusei, Edward M. Callaway, W. Martin Usrey, Farran Briggs
eNeuro 13 March 2024, 11 (3) ENEURO.0364-23.2024; DOI: 10.1523/ENEURO.0364-23.2024
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Keywords

  • corticogeniculate
  • extrastriate
  • LGN
  • virus-mediated circuit tracing
  • visual cortex

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