An afferent white matter pathway from the pulvinar to the amygdala facilitates fear recognition

  1. Jessica McFadyen  Is a corresponding author
  2. Jason B Mattingley
  3. Marta I Garrido
  1. University of Queensland, Australia
  2. Australian Research Council of Excellence for Integrative Brain Function, Australia
  3. Canadian Institute for Advanced Research (CIFAR), Canada
8 figures, 13 tables and 1 additional file

Figures

Global and local probabilistic tractography reconstructions of the subcortical route to the amygdala.

Fibres reconstructed between the superior colliculus and the pulvinar are shown in (A) and between the pulvinar and amygdala in (B). Both (A) and the top row of (B) show 3D-renders of the major ROIs (amygdala in pink, pulvinar in orange, superior colliculus in green), as well as the left anterior thalamic radiation (orange) and the right corticospinal tract (pink). The reconstructed fibres for all participants are rendered by semi-transparent white streamlines. Streamlines of a single example participant are shown below in boxes. The bottom half of (B) shows a different, top-down perspective of the pulvinar to amygdala pathway, illustrating the right inferior frontal occipital fasciculus (light blue) and the left inferior longitudinal fasciculus (dark blue). (C) shows the global fibre counts (left graph) and average fibre density (right graph) for global and local tractography, respectively (SC-PUL in yellow, PUL-AMG in purple). Group average is indicated by solid white line, with dotted lines indicating the 95% confidence interval. (D) shows the average number of fibres terminating in each subregion of the pulvinar and amygdala, for both global and local tractography. 3D renders of the subregions (colour-coded to match the graphs) are shown on the left. Graphs of the number of fibres terminating in pulvinar subregions are shown for tracts connecting the superior colliculus and pulvinar (first and second graphs) and the pulvinar and amygdala (third and fourth graphs), while fibres terminating in amygdala subregions are shown for tracts connecting the pulvinar and amygdala (fifth and sixth graphs). Error bars represent 95% confidence intervals.

https://doi.org/10.7554/eLife.40766.003
Relationship between behavioural performance and tractography.

(A) Histograms of scores (out of eight) for correctly recognising the emotional expression of angry, fearful, and sad faces from the Penn Recognition Test. Normal distribution function is plotted. (B) The relationships between recognition of angry (purple), fearful (red), and sad (blue) faces (x-axes) and the predicted local fibre densities for the left (top row) and right (bottom row) PUL-AMG connection (y-axes), as produced by a multivariate ANOVA. Fearful face recognition accuracy was significantly related to local fibre density for the left and right PUL-AMG connections (β and values shown for parameter estimates from multivariate ANOVA, *< .05).

https://doi.org/10.7554/eLife.40766.004
Whole-brain fMRI activation for faces and shapes.

Face activation is shown by hot colours and shape activation is shown by cool colours. MNI coordinates are shown at the bottom. Labels indicate significant (p < 0.05, whole brain FWE) activation in the superior colliculus (SC), pulvinar (PUL), amygdala (AMG), inferior occipital gyrus (IOG), and fusiform gyrus (FG). Results are overlayed on an averaged MNI152 T1 template.

https://doi.org/10.7554/eLife.40766.005
Dynamic causal modelling model space and estimated probabilities.

(A) Diagram of the model space constructed for the fMRI activation to viewing faces. The top row shows various types of model designs in the Cortical family, and the bottom row shows model designs in the Dual family (which includes a subcortical route). Each model variation included different combinations of forwards and backwards connections, indicated by dashed arrows. The model numbers are shown above each model variation. Every model contained input to the inferior occipital gyrus but some models also contained input to the superior colliculus (green) only, pulvinar (orange) only, or both (black). (B) The expected (top row) probabilities and exceedance probabilities (bottom row) for each of the 102 models. The colour of the bars indicates the different type of input for that family (i.e., SC, PUL, or both), according to A). Individual model probabilities are shown on the left (including a diagram of the winning model) and the probabilities for the families are shown on the right.

https://doi.org/10.7554/eLife.40766.006
The strength of individual connections from the winning dynamic causal model.

Parameter estimates of the modulatory connection strength of the winning model. Dot plots of up to 234 participants are shown with horizontal lines for the mean and vertical lines for one standard deviation. Density distribution is represented by each violin plot. The long horizontal dotted line across the graph represents the prior (set to 1), where * indicates the connection was significantly greater than 1 (p<0.05, corrected for multiple comparisons). A diagram of the winning model (left and right hemispheres are shown) is at the top right. Greyed-out connections indicate those that were not significant.

https://doi.org/10.7554/eLife.40766.007
The relationship between structural and effective connectivity for the subcortical route.

(A and B) show 3D renders of the ROIs used in the dynamic causal modelling stage. A = anterior, p = posterior, R = right, L = left. (A) 3D-rendered tracks generated by global tractography overlaid for all 622 participants (pink/orange for PUL-AMG, green/yellow for SC-PUL). (B) Direction of information flow according to the winning dynamic causal model (exceedance probability = 98.01%) illustrated using an axial view of the network. Dotted lines indicate subcortical input/connections. (C) Positive correlation between global track count for the left and right PUL-AMG connections and the modulatory strength of the same connection in the winning effective connectivity model (with 95% CI shown).

https://doi.org/10.7554/eLife.40766.008
Appendix 1—figure 1
Participants with above or below threshold fMRI signal in all VOIs for inclusion into DCM stage.

Threshold was set at p<0.05 uncorrected, using the [Faces – Shapes] contrast. Each column is a participant (N = 622) and each row is a different region (SC = superior colliculus, PUL = pulvinar, AMG = amygdala, FG = fusiform gyrus, IOG = inferior occipital gyrus) with two sessions each (i.e. each fMRI run) per hemisphere (L = left, R = right). Red indicates below-threshold signal and green indicates above-threshold signal. The bottom row (‘ALL’) indicates whether the participants were included or excluded from further DCM analysis, based on whether they had any below-threshold VOIs.

https://doi.org/10.7554/eLife.40766.024

Tables

Appendix 1—table 1
Global tractography fibre counts.

2 (pathway: SC-PUL, PUL-AMG)×2 (hemisphere: left, right) design. Four outliers removed out of 622.

https://doi.org/10.7554/eLife.40766.011
Outliers removedANOVA main effectst-tests for
Simple Effects
EffectDfFPηp2DfTP
* Pathway(3,4)433.2862.842 × 10−73*0.413
* Hemisphere(3,4)7.5830.006 *0.012
* Pathway × Hemisphere(1,616)16.0257.000 × 10−5*0.025
Left vs.Right SC-PUL6171.013.311
* Left vs. Right PUL-AMG617−9.7854.070 × 10−21*
Pathway × Head Motion(1,616)0.313.5765.090 × 10-4 *
Hemisphere × Head Motion(1,616)0.055.8139.100 × 10-5 *
Pathway × Hemisphere ×
Head Motion
(1,616)0.332.7102.250 × 10-4 *
No Outliers Removed* Pathway(1,620)32.4162.194 × 10−8*.049
* Hemisphere(1,620)9.175.003 *.015
* Pathway × Hemisphere(1,620)5.807.016 *.009
Left vs. Right SC-PUL6210.654.514
* Left vs. Right PUL-AMG621−8.9045.906 × 10−18*
Pathway × Head Motion(1,620)0.030.8634.800 × 10−5
Hemisphere × Head Motion(1,620)1.155.283.002
Pathway × Hemisphere ×
Head Motion
(1,620)0.332.565.001
  1. *p <.05

Appendix 1—table 2
Local tractography fibre counts.

2 (pathway: SC-PUL, PUL-AMG)×2 (hemisphere: left, right) design. Thirteen outliers removed out of 622.

https://doi.org/10.7554/eLife.40766.012
Outliers removedANOVA main effectst-tests for Simple Effects
EffectDfFPηp2DfTP
* Pathway(1,607)69.5864.930 × 10−16*0.103
Hemisphere(1,607)1.3870.2390.002
* Pathway × Hemisphere(1,607)162.483.828 × 10−33*0.211
* Left vs. Right SC-PUL60810.7498.596 × 10−25*
* Left vs. Right PUL-AMG608−18.2051.960 × 10−59*
Pathway × Head Motion(1,607)1.815.178.003
Hemisphere × Head Motion(1,607)1.39.239.002
Pathway ×
Hemisphere × Head
Motion
(1,607)1.425.233.002
No Outliers Removed* Pathway(1,620)59.7494.365 × 10−14*.088
Hemisphere(1,620)0.757.385.001
* Pathway ×Hemisphere(1,620)116.9624.316 × 10−25*.159
* Left vs. Right SC-PUL6219.3781.243 × 10−19*
* Left vs. Right PUL-AMG621−17.5154.068 × 10−56*
Pathway × Head Motion(1,620)1.222.269.002
Hemisphere × Head Motion(1,620)1.511.219.002
Pathway × Hemisphere ×
Head Motion
(1,620)0.617.433.001
  1. *p <.05 

Appendix 1—table 3
Global tractography fibre counts (terminations in pulvinar subregions) for SC-PUL.

5 (cluster: inferior, medial, anterior, superior, lateral)×2 (hemisphere: left, right) design. Ten outliers removed out of 622.

https://doi.org/10.7554/eLife.40766.013
Outliers removedANOVA main effectst-tests for Simple Effects
EffectDfFPηp2DfTP
Hemisphere(1,610)3.817.051.090
* Cluster(3,2060)214.0151.584 × 10−133*.260
*Hemisphere
 × Cluster
(3,2014)23.6242.870 × 10−16*.037
* Left: Inferior vs. Anterior6114.8201.815 × 10−6*
* Left: Anterior vs. Medial6112.7540.006 *
* Left: Medial vs. Lateral61111.6352.114 × 10−28*
* Left: Lateral vs. Superior61115.9384.456 × 10−48*
* Right:Anterior vs. Inferior6114.2282.715 × 10−5*
* Right: Inferior vs. Lateral61113.9829.574 × 10−39*
Right: Lateral
vs. Medial
6112.0450.041
* Right: Medial vs. Superior61121.1081.076 × 10−74*
Hemisphere ×
Head
Motion
(1,610)0.6200.431.001
Cluster × Head Motion(3,2060)0.4780.720.001
Hemisphere × Cluster ×
Head Motion
(3,2014)0.3060.840.001
No Outliers
Removed
* Hemisphere(1,620)5.749.017 *.009
* Cluster(1,913)52.1742.998 × 10−17*.078
*Hemisphere × Cluster(3,1743)16.5914.129 × 10−10*.026
* Left: Inferior vs. Anterior6214.1913.200 × 10-5 *
Left: Anterior vs. Medial6212.314.021
* Left: Medial vs. Lateral6216.3853.361 × 10-10 *
* Left: Lateral vs. Superior62114.2355.357 × 10-40 *
* Right: Anterior vs. Inferior6213.6952.390 × 10-5 *
* Right: Inferior vs. Lateral6217.6199.590 × 10-14 *
Right:Lateral vs. Medial621−0.187.852
* Right: Medial vs. Superior62112.9573.715 × 10-34 *
Hemisphere ×
Head Motion
(1,620)1.555.213.003
Cluster × Head Motion(1,913)0.159.7862.570 × 10−4
Hemisphere × Cluster × Head Motion(3,1743)0.706.539.001
  1. *p <.05 (for t-tests, only * if <0.05 Bonferroni corrected)

Appendix 1—table 4
Global tractography fibre counts (terminations in pulvinar subregions) for PUL-AMG.

5 (cluster: inferior, medial, anterior, superior, lateral)×2 (hemisphere: left, right) design. Sixty-eight outliers removed out of 622.

https://doi.org/10.7554/eLife.40766.014
Outliers removedANOVA main effectst-tests for Simple Effects
EffectDfFPηp2DfTP
* Hemisphere(1,552)22.1473.197 × 10−6*.039
* Cluster(2,1139)354.2612.662 × 10−123*.391
*Hemisphere × Cluster(2,1135)15.3341.946 × 10−7*.027
* Left: Inferior vs. Medial53324.8494.248 × 10−92*
* Left: Medial vs. Lateral5334.2092.998 × 10−5*
Left: Lateral vs. Anterior5332.458.014
* Left: Anterior vs. Superior5334.6653.868 × 10−6*
* Right:Inferior vs. Lateral53325.7421.184 × 10−96*
* Right: Lateral vs. Superior5337.6091.197 × 10−13*
Right: Superior vs. Medial5332.044.041
Right: Medial vs. Anterior5334.1334.141 × 10−5*
Hemisphere × Head Motion(1,552)1.067.302.002
Cluster × Head Motion(2,1139)1.885.151.003
Hemisphere ×Cluster ×
Head Motion
(2,1135)0.601.553.001
No Outliers
Removed
* Hemisphere(1,620)33.4641.152 × 10-8 *.051
* Cluster(2,1153)320.4063.145 × 10-105 *.341
*Hemisphere × Cluster(2,1390)14.9359.810 × 10-8 *.024
* Left:Inferior vs. Anterior62123.8658.002 × 10-90 *
Left: Anterior vs. Medial6213.099.002
* Left: Medial vs. Lateral6213.021.003
* Left:Lateral vs. Superior6213.8351.380 × 10-4 *
* Right: Anterior
vs. Inferior
62125.4242.827 × 10-98 *
* Right: Inferior
vs. Lateral
6217.9091.190 × 10-14 *
Right: Lateral vs. Medial6210.657.511
* Right: Medial vs. Superior6213.9259.600 × 10-5 *
Hemisphere × Head Motion(1,620)0.278.5984.490 × 10−4
Cluster × Head Motion(2,1153)1.134.319.002
Hemisphere × Cluster ×
Head Motion
(2,1390)0.512.620.001
  1. *p <.05 (for t-tests, only * if <0.05 Bonferroni corrected).

Appendix 1—table 5
Global tractography fibre counts (terminations in amygdala subregions) for PUL-AMG.

3 (cluster: centromedial, basolateral, superficial)×2 (hemisphere: left, right) design. Sixteen outliers removed.

https://doi.org/10.7554/eLife.40766.015
Outliers removedANOVA main effectst-tests for Simple Effects
EffectDfFPηp2DfTP
Hemisphere(1,604)1.419.234.002
* Cluster(2,1161)80.7791.909 × 10-32 *.118
* Hemisphere × Cluster(2,1171)28.2782.060 × 10-12 *.045
* Left:
Basolateral vs.
Centromedial
6058.7412.279 × 10-17 *
* Left:
Centromedial vs.
Superficial
6055.3541.222 × 10-7 *
* Right:
Basolateral vs.
Superficial
60511.5157.018 × 10-28 *
* Right:
Superficial vs.
Centromedial
60510.7001.376 × 10-24 *
Hemisphere × Head
Motion
(1,604)0.586.444.695 × 10−4
Cluster ×
Head Motion
(2,1161)0.892.407.001
Hemisphere × Cluster ×
Head Motion
(2,1171)0.261.7644.315 × 10−4
No Outliers
Removed
Hemisphere(1,620)2.295.130.004
* Cluster(2,1212)79.2532.017 × 10-32 *.113
* Hemisphere ×
Cluster
(2,1201)27.7543.363 × 10-12 *.043
* Left: Basolateral vs.
Centromedial
6218.8061.284 × 10-17 *
* Left: Centromedial vs.
Superficial
6215.1194.098 × 10-7 *
* Right: Basolateral vs.
Superficial
62111.7536.132 × 10-29 *
* Right: Superficial vs.
Centromedial
62110.0274.961 × 10-22 *
Hemisphere × Head Motion(1,620)0.014.9072.200 × 10−4
Cluster × Head Motion(2,1212)0.515.593.001
Hemisphere ×
Cluster ×
Head Motion
(2,1201)0.164.8422.650 × 10−4
  1. *p <.05 (for t-tests, only * if <0.05 Bonferroni corrected)

Appendix 1—table 6
Local tractography fibre counts (terminations in pulvinar subregions) for SC-PUL.

5 (cluster: inferior, medial, anterior, superior, lateral)×2 (hemisphere: left, right) design. Sixty-seven outliers removed out of 622.

https://doi.org/10.7554/eLife.40766.016
Outliers
removed
ANOVA main effectst-tests for Simple Effects
EffectDfFPηp2DfTP
* Hemisphere(1,553)23.5771.564 × 10-6 *.041
* Cluster(2,1010)873.9226.337 × 10-209 *.612
*Hemisphere
 × Cluster
(2,1176)64.3701.002 × 10-28 *.104
* Left: Anterior vs.
Inferior
55422.3731.709 × 10-79 *
* Left: Inferior
vs. Medial
5549.7428.353 × 10-21 *
* Left:Medial
vs. Lateral
55430.7101.089 × 10-121 *
*Left:Lateral vs.
Superior
55416.5144.103 × 10-50 *
* Right:Anterior vs.
Inferior
55439.2414.436 × 10-162 *
* Right: Inferior vs.
Medial
5549.1571.022 × 10-18 *
* Right: Medial vs.
Lateral
55425.2872.203 × 10-94 *
* Right:Lateral vs.
Superior
55415.2136.282 × 10-44 *
Hemisphere × Head Motion(1,553)0.3580.550.001
Cluster × Head Motion(2,1010)0.4950.593.001
Hemisphere ×
Cluster ×
Head Motion
(2,1176)0.6040.557.001
No Outliers
Removed
* Hemisphere(1,620)23.6002.000 × 10-6 *.037
* Cluster(2,1244)831.7641.817 × 10-230 *.573
*Hemisphere
 × Cluster
(2,1354)69.2621.107 × 10-31 *.100
* Left: Anterior vs.
Inferior
62122.7459.069 × 10-84 *
* Left:Inferior vs.
Medial
6218.4362.312 × 10-16 *
* Left:Medial vs.
Lateral
62129.5621.448 × 10-120 *
*Left:Lateral vs.
Superior
62113.8323.972 × 10-39 *
* Right: Anterior vs.
Inferior
62139.1001.326 × 10-169 *
* Right:Inferior
vs. Medial
6217.4363.463 × 10-13 *
* Right:Medial
vs. Lateral
62123.5444.380 × 10-88 *
* Right:Lateral
vs. Superior
62112.9643.461 × 10-34 *
Hemisphere ×
Head Motion
(1,620)0.161.6882.60 × 10−4
Cluster ×
Head Motion
(2,1244)0.830.437.001
Hemisphere ×
Cluster ×
Head Motion
(2,1354)1.023.365.002
  1. *p <.05 (for t-tests, only * if <0.05 Bonferroni corrected)

Appendix 1—table 7
Local tractography fibre counts (terminations in pulvinar subregions) for AMG-PUL.

5 (cluster: inferior, medial, anterior, superior, lateral)×2 (hemisphere: left, right) design. Seventy-eight outliers removed out of 622.

https://doi.org/10.7554/eLife.40766.017
Outliers removedANOVA main effectst-tests for Simple Effects
EffectDfFPηp2DfTP
* Hemisphere(1,542)108.3013.019 × 10-23 *.167
* Cluster(1,544)2159.8279.415 × 10-192 *.799
*Hemisphere ×
Cluster
(1,544)105.7727.093 × 10-23 *.163
* Left: Inferior
vs. Lateral
54357.6948.996 × 10-234 *
* Left: Lateral
vs. Medial
54310.6334.080 × 10-24 *
* Left: Medial
vs. Anterior
54312.7449.913 × 10-33 *
* Left: Anterior
vs. Superior
5435.8976.503 × 10-9 *
* Right: Inferior
vs. Lateral
54359.0791.332 × 10-238 *
* Right: Lateral
vs. Superior
54327.2777.886 × 10-104 *
* Right: Superior
vs. Anterior
54314.0062.839 × 10-38 *
Right: Anterior
vs. Medial
5430.815.416
Hemisphere ×
Head Motion
(1,542)4.749.030 *0.009
Cluster ×
Head Motion
(1,544)19.5691.146 × 10-5 *0.035
Hemisphere ×
Cluster ×
Head Motion
(1,544)4.689.031 *0.009
No Outliers
Removed
* Hemisphere(1,620)110.5876.523 × 10-24 *.151
* Cluster(1,622)2139.6494.887 × 10-204 *.775
*Hemisphere ×
Cluster
(1,624)107.0102.219 × 10-23 *.147
* Left: Inferior
vs. Lateral
62157.1202.174 × 10-249 *
* Left: Lateral
vs. Medial
62110.1691.427 × 10-22 *
* Left:Medial vs. Anterior62110.6092.812 × 10-24 *
*Left: Anterior
vs. Superior
6215.1533.446 × 10-7 *
* Right: Inferior
vs. Lateral
62161.5291.963 × 10-266 *
* Right:Lateral
vs. Superior
62124.2417.327 × 10-92 *
Right: Superior
vs. Anterior
62110.8912.122 × 10-25 *
Right: Anterior
vs. Medial
6210.227.821
Hemisphere ×
Head Motion
(1,620)4.775.029 *.147
Cluster ×
Head Motion
(1,622)19.7391.000 × 10-5 *.031
Hemisphere ×
Cluster ×
Head Motion
(1,624)4.568.033.007
  1. *p <.05 (for t-tests, only * if <0.05 Bonferroni corrected)

Appendix 1—table 8
Local tractography fibre counts (terminations in amygdala subregions) for PUL-AMG.

3 (cluster: centromedial, basolateral, superficial)×2 (hemisphere: left, right) design. Thirty-seven outliers removed out of 622.

https://doi.org/10.7554/eLife.40766.018
Outliers removedANOVA main effectst-tests for Simple Effects
EffectDfFPηp2DfTP
Hemisphere(1,620)511.2785.154 × 10-83 *.452
* Cluster(2,989)308.0797.593 × 10-88 *.332
*Hemisphere
 × Cluster
(2,1201)27.7543.363 × 10-12 *.043
* Left:
Basolateral
vs. Centremedial
62110.3742.323 × 10-23 *
* Left:
Centromedial
vs. Superficial
62119.5738.248 × 10-67 *
* Right:
Centromedial
vs. Basolateral
62125.1361.037 × 10-96 *
* Right:
Basolateral
vs. Superficial
62127.0375.308 × 10-107 *
Hemisphere ×
Head Motion
(1,620)296.624.015 *.009
Cluster ×
Head Motion
(2,989)0.0504.774 × 10−84.324
Hemisphere ×
Cluster ×
Head Motion
(2,1201)0.917.380.001
No Outliers
Removed
Hemisphere(1,620)511.2785.154 × 10-83 *.452
* Cluster(2,989)308.0797.593 × 10-88 *.332
*Hemisphere
 × Cluster
(2,1201)27.7543.363 × 10-12 *.043
* Left:
Basolateral vs.
Centremedial
62110.3742.323 × 10-23 *
* Left:
Centromedial
vs. Superficial
62119.5738.248 × 10-67 *
* Right:
Centromedial
vs. Basolateral
62125.1361.037 × 10-96 *
* Right:
Basolateral vs.
Superficial
62127.0375.308 × 10-107 *
Hemisphere ×
Head Motion
(1,620)296.624.015 *.009
Cluster ×
Head Motion
(2,989)0.0504.774 × 10−84.324
Hemisphere ×
Cluster ×
Head Motion
(2,1201)0.917.380.001
  1. *p <.05 (for t-tests, only * if <0.05 Bonferroni corrected)

Appendix 1—table 9
Paired t-tests between local streamline count and null distribution.
https://doi.org/10.7554/eLife.40766.019
ComparisonNMSEM95%TDfP
Left SC-
PUL
6181384.87616.704[1352.073, 1417.68]82.907617<1 × 10-243 *
Right SC-
PUL
618−499.55516.430[−531.821,
–467.289]
−30.4046178.832 × 10-125 *
Left PUL-
AMG
618351.6698.535[334.908, 368.431]41.2026172.722 × 10-179 *
Right PUL-AMG620577.53510.385[557.142, 597.929]55.6146196.091 × 10-243 *
  1. *p <.05

Appendix 1—table 10
Global tractography multivariate GLM.

Fibre counts for left and right SC-PUL and PUL-AMG entered as dependent variables. Recognition scores (out of eight) for fearful, sad, and angry expressions entered as covariates of interest. Head motion entered as covariate of no interest. Bootstrapping at 1000 iterations. Four outliers removed with residuals more than three standard deviations from the mean.

https://doi.org/10.7554/eLife.40766.020
Outliers removedMultivariate tests
EffectWilk’s ΛDfFPηp2
Fearful.995(4, 609)0.715.582.005
Sad.994(4, 609)0.915.455.006
Angry.998(4, 609)0.294.882.002
Head Motion.999(4, 609)0.223.926.001
Parameter estimates
Dependent variableParameterBTPηp295%
Left SC-PULFearful−0.350−1.583.114.004[−0.784, 0.084]
Sad−0.312−1.520.129.004[−0.715, 0.091]
Angry−0.157−0.687.493.001[−0.607, 0.292]
Head Motion−0.359−0.677.498.001[−1.401, 0.682]
Right SC-PUL Fearful−0.208−0.933.351.001[−0.645, 0.23]
Sad−0.042−0.202.8406.700 × 10−5[−0.448, 0.364]
Angry−0.046−0.197.8446.400 × 10−5[−0.499, 0.408]
Head Motion−0.268−0.501.6164.110 × 10−4[−1.317, 0.781]
Left PUL-AMGFearful−0.006−0.051.9594.000 × 10−6[−0.225, 0.213]
Sad−0.010−0.099.9211.600 × 10−5[−0.213, 0.193]
Angry−0.024−0.205.8376.900 × 10−5[−0.251, 0.203]
Head Motion0.1030.386.7002.430 × 10−4[−0.422, 0.628]
Left PUL-AMGFearful−0.071−0.611.541.001[−0.297, 0.156]
Sad0.1010.941.347.001[−0.11, 0.311]
Angry−0.101−0.846.398.001[−0.336, 0.134]
Head Motion−0.103−0.373.7092.280 × 10−4[−0.647, 0.44]
No Outliers
Removed
Multivariate Tests
EffectWilk’s ΛdfFpηp2
Fearful.998(4,613)0.349.845.002
Sad.994(4,613)0.957.430.006
Angry.996(4,613)0.569.685.004
Head Motion.998(4,613)0.287.886.002
Parameter Estimates
Dependent VariableParameterBtpηp295% CI
Left SC-PULFearful−0.794−0.809.419.001[−2.723, 1.134]
Sad0.0530.058.9545.000 × 10−7[−1.736, 1.842]
Angry0.0570.056.9555.000 × 10−7[−1.938, 2.052]
Head Motion−0.147−0.062.9506.000 × 10−7[−4.763, 4.47]
Right SC-PULFearful−0.612−0.605.546.001[−2.597, 1.374]
Sad0.4820.514.6074.290 × 10−4[−1.36, 2.325]
Angry0.3140.3.7641.460 × 10−4[−1.74, 2.369]
Head Motion−0.703−0.29.7721.370 × 10−4[−5.458, 4.052]
Left PUL-AMGFearful−0.072−0.433.6653.050 × 10−4[−0.4, 0.255]
Sad0.0180.117.9072.200 × 10−5[−0.286, 0.322]
Angry−0.109−0.631.529.001[−0.448, 0.23]
Head Motion0.1910.479.6323.720 × 10−4[−0.593, 0.976]
Left PUL-AMGFearful−0.126−0.871.384.001[−0.41, 0.158]
Sad0.120.894.372.001[−0.144, 0.384]
Angry−0.135−0.905.366.001[−0.429, 0.158]
Head Motion−0.012−0.033.9732.000 × 10−6[−0.692, 0.669]
Appendix 1—table 11
Local tractography multivariate GLM.

Average apparent fibre density for left and right SC-PUL and PUL-AMG entered as dependent variables. Recognition scores (out of eight) for fearful, sad, and angry expressions entered as covariates of interest. Head motion entered as covariate of no interest. Bootstrapping at 1000 iterations. Fifteen outliers removed with residuals more than three standard deviations from the mean.

https://doi.org/10.7554/eLife.40766.021
Outliers removedMultivariate tests
EffectWilk’s ΛDfFPηp2
* Fearful.984(4,598)2.501.042 *.016
Sad.991(4,598)1.363.245.009
Angry.993(4,598)1.111.350.007
* Head Motion.977(4,598)3.451.008 *.023
Parameter estimates
Dependent variableParameterBTPηp295%
Left SC-PULFearful0−0.0030.9981.093 × 10−8[−0.163, 0.162]
Sad0.0841.0990.2720.002[−0.066, 0.235]
Angry−0.078−0.9010.3680.001[−0.249, 0.093]
Head Motion−0.135−0.6810.4960.001[−0.526, 0.255]
Right SC-PULFearful−0.046−0.6450.5190.001[−0.185, 0.094]
Sad−0.008−0.1230.9022.500 × 10−5[−0.137, 0.121]
Angry0.0430.5740.5660.001[−0.104, 0.189]
Head Motion−0.146−0.8590.390.001[−0.48, 0.188]
Left PUL-AMG*fearful0.142.8870.004 *0.014[0.045, 0.235]
Sad−0.084−1.8550.0640.006[−0.172, 0.005]
Angry−0.052−1.0180.3090.002[−0.152, 0.048]
Head Motion−0.21−1.8020.0720.005[−0.438, 0.019]
Right PUL
AMG
*fearful0.1432.5230.012 *0.010[0.032, 0.255]
Sad−0.042−0.7870.4310.001[−0.145, 0.062]
Angry0.0410.6860.4930.001[−0.076, 0.158]
* Head
Motion
−0.484−3.554.150 × 10−4 *0.021[−0.752,–0.216]
No Outliers
Removed
Multivariate Tests
EffectWilk’s ΛdfFpηp2
* Fearful.983(4,613)2.669.031 *.017
Sad.993(4,613)1.080.366.007
Angry.997(4,613)0.499.736.003
* Head Motion.982(4,613)2.792.026 *.018
Parameter Estimates
Dependent VariableParameterBtpηp295% CI
Left SC-PULFearful−0.006−0.051.9604.000 × 10−6[−0.231, 0.22]
 Sad0.1211.138.255.002[−0.088, 0.33]
 Angry−0.080−0.674.500.001[−0.313, 0.153]
 Head Motion−0.063−0.229.8198.500 × 10−5[−0.602, 0.477]
Right SC-PULFearful−0.097−1.037.300.002[−0.28, 0.086]
 Sad0.0170.197.8446.300 × 10−5[−0.153, 0.187]
 Angry0.0230.233.8168.800 × 10−5[−0.167, 0.212]
 Head Motion−0.165−0.738.461.001[−0.604, 0.274]
Left PUL-AMG* Fearful0.1372.650.008 *.011[0.036, 0.239]
 Sad−0.075−1.563.119.004[−0.17, 0.019]
 Angry−0.049−0.904.366.001[−0.154, 0.057]
 Head Motion−0.193−1.554.121.004[−0.437, 0.051]
Left PUL-AMG* Fearful0.1372.334.020 *.009[0.022, 0.253]
 Sad−0.053−0.976.330.002[−0.16, 0.054]
 Angry0.0010.019.9856.126 × 10−7[−0.118, 0.121]
 * Head Motion−0.465−3.303.001 *.017[−0.741,–0.189]
Appendix 1—table 12
Partial correlations between fibre density of each pathway and the corresponding DCM parameter estimate.

Scatterplots show the fibre density (x-axis) residuals (after regressing against head motion) and the DCM parameter estimate (y-axis) residuals (after regressing against head motion). *p<0.05, Bonferroni-corrected

https://doi.org/10.7554/eLife.40766.022
Global Tractography
Local Tractography
Global Tractography
Local Tractography
  1. Local Tractography

Appendix 1—table 13
Significance of DCM parameter estimates.
https://doi.org/10.7554/eLife.40766.023
Outliers removedParameterMSDDfTP95%
* Left SC-
PUL
1.0630.1152298.285<0.001[1.048, 1.078]
* Right
SC-PUL
1.0590.1242337.295<0.001[1.043, 1.075]
* Left
PUL-AMG
1.8341.00023312.753<0.001[1.705, 1.962]
* Right
PUL-AMG
1.7310.76523014.514<0.001[1.632, 1.83]
* Left
IOG-FG
1.6850.71522814.485<0.001[1.592, 1.778]
* Right
IOG-FG
2.4152.14023310.111<0.001[2.139, 2.69]
* Left FG-AMG1.2130.25823312.614<0.001[1.18, 1.246]
* Right
FG-AMG
1.1900.21723013.308<0.001[1.162, 1.218]
Left FG-
IOG
0.9880.211230−0.8420.401[0.961, 1.016]
Right
FG-
IOG
1.0370.2702312.0950.037[1.002, 1.072]
* Left
AMG-FG
1.8131.3302319.306<0.001[1.641, 1.985]
* Right
AMG-FG
1.8781.10122812.078<0.001[1.735, 2.022]
No Outliers
Removed
ParameterMSDdftp95% CI
* Left SC-
PUL
1.0660.1572366.481<0.001[1.046, 1.086]
* Right
SC-PUL
1.0680.1902365.510<0.001[1.044, 1.093]
* Left
PUL-AMG
1.9161.23523611.415<0.001[1.758, 2.074]
* Right
PUL-AMG
1.8210.94423613.382<0.001[1.7, 1.942]
* Left
IOG-FG
1.8641.21423610.957<0.001[1.709, 2.02]
* Right
IOG-FG
2.7724.2492366.422<0.001[2.229, 3.316]
* Left
FG-
AMG
1.2510.4462368.661<0.001[1.194, 1.308]
* Right
FG-AMG
1.2180.27823612.081<0.001[1.182, 1.253]
Left FG-
IOG
1.0280.3292361.3110.191[0.986, 1.07]
Right
FG-
IOG
1.0690.3482363.0710.002[1.025, 1.114]
* Left
AMG-FG
2.0572.1662367.517<0.001[1.78, 2.335]
* Right
AMG-FG
2.0921.59623610.536<0.001[1.888, 2.296]
  1. *p <.001

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  1. Jessica McFadyen
  2. Jason B Mattingley
  3. Marta I Garrido
(2019)
An afferent white matter pathway from the pulvinar to the amygdala facilitates fear recognition
eLife 8:e40766.
https://doi.org/10.7554/eLife.40766