Schematic memory components converge within angular gyrus during retrieval
- Radboudumc, The Netherlands
- Radboud University, The Netherlands
- New York University, United States
- University of Edinburgh, United Kingdom
Figures
Figure 1 with 2 supplements
Study timeline and schema material.
(A) Subjects underwent fMRI on two consecutive days, each containing 7 runs (day 1: encoding and retrieval; day 2: retrieval). A transfer test was completed at the end of day 2 and consisted of two …
Figure 1—figure supplement 1
Multi-voxel pattern analysis (MVPA).
(A) We used MVPA to discriminate between schema components, which were defined as (1) rule-based associations (spatial vs. non-spatial, while collapsing across circle pairs 1–4), and (2) low-level …
Figure 1—figure supplement 2
Experimental trials.
(A) During encoding trials, subjects received a cue (2 s) to apply either the spatial or non-spatial schema. Circle pairs were presented (3 s) and a response indicating the outcome was necessary (2 s…
Figure 2
Behavioral performance during schema retrieval.
(A) Data represents the % of correct responses, (B) the average reaction time (s), and (C) the % of high-confident ratings (i.e. “sure”-responses). Shaded error bars denote ± standard error of the me…
Figure 3
Activation during schema retrieval.
(A) Increased BOLD responses during rule-based schema retrieval across both days (schema retrieval > perceptual baseline), (B) during rule-based schema retrieval on day 1 (day 1 > day 2), and (C) …
Figure 4
Schema retrieval networks: MPFC and PCC.
(A) MPFC seed (x = -2, y = 35, z = -2; based on the contrast day 2 > day 1, Figure 3C; here marked in white). (B) PCC seed (x = 2, y = -45, z = 22; based on the same contrast; here marked in white). …
Figure 5
Multi-voxel representations of schema components.
(A) The searchlight MVPA revealed distributed representations of both schema components (rule-based associations, low-level visual features). These representational levels converged within the AG …
Figure 6
Schema convergence networks.
Functional connectivity of the left AG seed (defined as cluster of overlapping schema components; based on our MVPA result, Figure 5A, here marked in white) during schema retrieval (compared to the …
Figure 7
Spatial relationship between schema retrieval networks and schema component representations.
Results from connectivity analyses (seeds MPFC, PCC, AG), and MVPA are shown as a 3D rendering. During schema retrieval, MPFC and PCC were functionally connected with the same AG region (left part). …
Figure 8
Transfer test.
(A) Schema encoding: left, % of correct responses; right, average reaction time (s). (B) Schema retrieval: left, % of correct responses; middle, average reaction time (s); right, % of high-confident …
Figure 9
Behavioral performance during schema encoding.
(A) Data represents the % of correct responses, and (B) the average reaction time (s). Shaded error bars denote ± s.e.m.
Figure 10
Multi-voxel representations of low-level visual features on day 1.
Additional searchlight MVPA revealed distributed representations of low-level visual features, but not rule-based associations, during schema retrieval on day 1 (Materials and methods, Complementary …
Figure 11
Hippocampal connectivity during schema retrieval.
(A) Hippocampal connectivity during general schema retrieval (compared to the perceptual baseline) across both days (day 1 & day 2). Additionally, connectivity results are projected onto a …
Author response image 1
Hippocampal activation during schema retrieval (z = -17).
(A) Increased BOLD responses during schema memory retrieval across both days (schema retrieval > perceptual baseline), (B) during rule-based schema retrieval on day 1 (day 1 > day 2), and (C) after …
Author response image 2
Non-spatial schema performance, RTs and retrieval confidence compared to day 1, run 1.
(A) Schema Encoding: left, % of correct responses; right, average reaction time (s). (B) Schema retrieval: left, % of correct responses; middle, average reaction time (s); right, % of high-confident …
Author response image 3
Generalization of schema component representations from day 2 to day 1.
(A) Multi-voxel patterns of rule-based associations did not generalize across days. (B) Multi-voxel patterns of low-level visual features were shared across days. For display purposes, all maps were …
Author response image 4
Generalization of schema component representations from day 2 to the transfer test.
Multi-voxel patterns of rule-based associations and low-level visual features were shared across study phases. Cut-outs of the horizontal slice are magnified to appreciate the overlap of schema …
Author response image 5
Multi-voxel representations of schema components within left AG.
The image shows magnified, horizontal cut-outs at the level of AG. Data represents significant discrimination of rule-based associations. Upper row: original MVPA results as reported in the …
Author response image 6
Schema retrieval across days.
Data represents the % of correct responses. Error bars denote ± Standard Error of the Mean (SEM). * marks a significant (P < 0.05) difference between the schema conditions within the first run of …
Author response image 7
Changes in activation as a function of run on day 1.
Increases in activation are shown in warm colors, decreases in cool colors. For display purposes, all maps were resliced to a voxel dimension of 0.5 mm isotropic and are shown at P < 0.001, …
Author response image 8
Multi-voxel representations of schema components on day 1.
(A) We did not find any significant representations of rule-based associations during retrieval on day 1. (B) Representations of low-level visual features were located within occipital regions, …
Tables
Table 1
Activation during schema retrieval.
MNI | |||||
|---|---|---|---|---|---|
| Brain region | x | y | z | Z value | Cluster size |
| Day 1 & day 2 | |||||
| L superior frontal gyrus | -5 | 5 | 52 | 766 | |
| L superior parietal gyrus | -22 | -60 | 40 | 9440 | |
| L middle frontal gyrus | -28 | -5 | 45 | 938 | |
| R middle frontal gyrus | 32 | -2 | 48 | 260 | |
| L insular cortex | -32 | 20 | 8 | 5.53 | 126 |
| Day 1 > day 2 | |||||
| L cuneus | -2 | -95 | 10 | 2814 | |
| L superior frontal gyrus | -5 | 5 | 52 | 6.14 | 165 |
| Cerebellum | -35 | -50 | -32 | 4.37 | 161 |
| Day 2 > day 1 | |||||
| L cingulate gyrus | 0 | -40 | 42 | 5.38 | 593 |
| R supramarginal gyrus | 55 | -22 | 30 | 4.32 | 156 |
| R superior frontal gyrus | 5 | -45 | -2 | 3.93 | 95 |
| R middle temporal gyrus | 58 | -50 | 0 | 3.85 | 106 |
-
Clusters that showed significant BOLD increases during retrieval of rule-based schema memories across days, before, and after a 24-hour-delay. Bold font indicates contrasts. Retrieval was compared to the perceptual baseline. MNI coordinates represent the location of peak voxels. We report the local maximum of each cluster. Effects were tested for significance using cluster-inference with a cluster-defining threshold of P < 0.001 and a cluster-probability of P < 0.05 family-wise error (FWE) corrected for multiple comparisons (critical cluster size: 86). L – left, R – right.
Table 2
Schema retrieval networks: MPFC and PCC.
MNI | |||||
|---|---|---|---|---|---|
| Brain region | x | y | z | Z value | Cluster size |
| Seed MPFC, spatial > perceptual baseline | |||||
| R superior frontal gyrus | 10 | 58 | 5 | 5.11 | 362 |
| L angular gyrus | -45 | -72 | 35 | 4.84 | 206 |
| R parahippocampal gyrus | 28 | -35 | -10 | 4.69 | 126 |
| L precuneus | -10 | -60 | 20 | 4.66 | 1008 |
| L precentral gyrus | -52 | -12 | 45 | 4.11 | 96 |
| L parahippocampal gyrus | -28 | -38 | -10 | 3.82 | 141 |
| Seed MPFC, non-spatial > perceptual baseline | |||||
| L cingulate gyrus | -5 | 38 | 8 | 4.26 | 314 |
| Seed PCC, spatial > perceptual baseline | |||||
| L cingulate gyrus | -10 | -45 | 8 | 5.07 | 1746 |
| R cingulate gyrus | 12 | 30 | 20 | 4.68 | 685 |
| L precentral gyrus | -55 | 8 | 2 | 4.64 | 1002 |
| R insular cortex | 35 | -22 | 8 | 4.62 | 120 |
| L parahippocampal gyrus | -32 | -35 | -15 | 4.49 | 553 |
| R inferior frontal gyrus | 52 | 18 | 12 | 4.44 | 279 |
| L angular gyrus | -48 | 70 | 40 | 4.42 | 106 |
| R superior temporal gyrus | 45 | -2 | -12 | 4.30 | 663 |
| Cerebellum | 12 | -72 | -28 | 4.23 | 142 |
| Cerebellum | -15 | -58 | -35 | 4.00 | 164 |
| Seed PCC, non-spatial > perceptual baseline | |||||
| L precuneus | -2 | -65 | 30 | 5.49 | 3597 |
| L precentral gyrus | -55 | -8 | 45 | 4.89 | 680 |
| R middle temporal gyrus | 65 | -18 | -8 | 4.58 | 716 |
| R superior frontal gyrus | 12 | 25 | 28 | 4.27 | 587 |
| L angular gyrus | -48 | -70 | 38 | 4.19 | 184 |
| Cerebellum | -20 | -68 | -28 | 4.03 | 282 |
| R middle frontal gyrus | 18 | 65 | 12 | 3.81 | 156 |
-
Clusters that showed a significant increase in connectivity during schema retrieval: MPFC (x = -2, y = 35, z = -2) and PCC (x = 2, y = -45, z = 22). Bold font indicates contrasts. Retrieval was compared to the perceptual baseline. MNI coordinates represent the location of peak voxels. We report the local maximum of each cluster. Effects were tested for significance using cluster-inference with a cluster-defining threshold of P < 0.001 and a cluster-probability of P < 0.05 family-wise error (FWE) corrected for multiple comparisons (critical cluster sizes; MPFC seed: spatial, 89 voxels; non-spatial, 95 voxels; PCC seed: 89 voxels for both conditions). L – left, R – right.
Table 3
Multi-voxel representations of schema components.
MNI | |||||
|---|---|---|---|---|---|
| Brain region | x | y | z | Z value | Cluster size |
| MVPA day 2, rule-based associations | |||||
| R lateral orbitofrontal gyrus | 42 | 42 | -18 | 4.14 | 75 |
| L middle occipital gyrus | -30 | -75 | 32 | 4.13 | 102 |
| L angular gyrus | -38 | -70 | 32 | 3.73 | |
| MVPA day 2, low-level visual features | |||||
| L cuneus | 0 | -82 | 8 | 16630 | |
| MVPA day 1, low-level visual features | |||||
| R lingual gyrus | 2 | -78 | -2 | 15599 | |
-
Clusters that significantly discriminated schema component representations (rule-based associations, low-level visual features). Bold font indicates the type of MVPA analysis (day 1, training the classifier on day 2 and testing it on day 1; day 2, training the classifier on day 2 and testing it on day 2 using cross-validation; Materials and methods, Multi-voxel pattern analysis). MNI coordinates represent the location of peak voxels. We report the first two local maxima (> 8 mm apart) within each cluster (rule-based associations), and the local maximum for the low-level visual feature MVPAs. Effects were tested for significance using cluster-inference with a cluster-defining threshold of P < 0.001 and a cluster-probability of P < 0.05 family-wise error (FWE) corrected for multiple comparisons (critical cluster sizes: day 2, rule-based associations, 74 voxels; day 2, low-level visual features, 72 voxels; day 1, low-level visual features, 70 voxels). L – left, R – right.
Table 4
Schema convergence networks.
MNI | |||||
|---|---|---|---|---|---|
| Brain region | x | y | z | Z value | Cluster size |
| Spatial > perceptual baseline | |||||
| L middle occipital gyrus | -30 | -80 | 32 | 5.90 | 553 |
| R middle frontal gyrus | 42 | 22 | 45 | 5.37 | 182 |
| L middle frontal gyrus | -32 | 18 | 52 | 5.19 | 380 |
| Cerebellum | 15 | -75 | -28 | 4.96 | 1553 |
| R inferior temporal gyrus | 55 | -58 | -12 | 4.94 | 259 |
| L inferior frontal gyrus | -40 | 20 | 2 | 4.61 | 922 |
| R angular gyurs | 42 | -65 | 50 | 4.56 | 701 |
| L fusiform gyrus | -32 | -35 | -25 | 4.50 | 352 |
| L middle frontal gyrus | -18 | 45 | 28 | 4.50 | 509 |
| L superior parietal gyrus | -15 | -60 | 18 | 4.39 | 261 |
| R superior parietal gyrus | 20 | -55 | 18 | 4.19 | 109 |
| R precuneus | 8 | -55 | 40 | 4.12 | 152 |
| R insular cortex | 38 | -8 | 0 | 4.08 | 95 |
| R superior temporal gyrus | 65 | -18 | 2 | 4.03 | 107 |
| R inferior frontal gyrus | 52 | 35 | 22 | 3.95 | 456 |
| Non-spatial > perceptual baseline | |||||
| L superior frontal gyrus | 0 | -5 | 48 | 5.87 | 22582 |
| L inferior frontal gyrus | -38 | 15 | 5 | 5.77 | |
| Cerebellum | -15 | -75 | -38 | 5.76 | |
| L angular gyrus | -32 | -78 | 42 | 5.63 | |
| R fusiform gyrus | 48 | -55 | -22 | 5.54 | |
| L inferior frontal gyrus | -35 | 28 | 2 | 5.52 | |
| R middle temporal gyrus | 62 | -12 | -12 | 5.43 | |
| R fusiform gyrus | 45 | -45 | -22 | 5.42 | |
| L middle frontal gyrus | -38 | 12 | 52 | 5.42 | |
| R superior frontal gyrus | 2 | 28 | 52 | 5.42 | |
| L superior temporal gyrus | -52 | -5 | -8 | 5.40 | |
| R superior frontal gyrus | 8 | 8 | 52 | 5.32 | |
| Cerebellum | -25 | -60 | -35 | 5.32 | |
| L middle temporal gyrus | -62 | -58 | 2 | 5.31 | |
| R superior frontal gyrus | 8 | 28 | 40 | 5.30 | |
-
Clusters that showed a significant increase in AG connectivity during schema retrieval. Retrieval was compared to the perceptual baseline. The seed was defined as overlap between schema components, as determined with MVPA (Figure 5A). Bold font indicates contrasts. MNI coordinates represent the location of peak voxels. We report the local maximum of each cluster. For the non-spatial schema condition we report the first 15 local maxima (> 8 mm apart). Effects were tested for significance using cluster-inference with a cluster-defining threshold of P < 0.001 and a cluster-probability of P < 0.05 family-wise error (FWE) corrected for multiple comparisons (critical cluster sizes: spatial, 88 voxels; non-spatial, 83 voxels). L – left, R – right.
Table 5
Transfer test: multi-voxel representations of schema components.
MNI | |||||
|---|---|---|---|---|---|
| Brain region | x | y | z | Z value | Cluster size |
| MVPA transfer test, rule-based associations | |||||
| L superior occipital gyrus | -15 | -78 | 22 | 3.63 | 211 |
| L angular gyrus | -35 | -72 | 35 | 3.57 | |
| L superior occipital gyrus | -12 | -90 | 20 | 3.23 | |
| MVPA transfer test, low-level visual features | |||||
| L lingual gyrus | -12 | -82 | 8 | 11692 | |
-
Clusters that significantly discriminated schema component representations (rule-based associations, low-level visual features) during the transfer test. Bold font indicates the type of MVPA analysis. MNI coordinates represent the location of peak voxels. We report the first three local maxima (>8 mm apart) within each cluster (rule-based associations), and the local maximum for the low-level visual features analysis. Effects were tested for significance using cluster-inference with a cluster-defining threshold of P < 0.005 (rule-based associations) or P < 0.001 (low-level visual features) and a cluster-probability of P < 0.05 family-wise error (FWE) corrected for multiple comparisons (critical cluster sizes: rule-based associations, 172 voxels; low-level visual features, 60 voxels). L – left, R – right.
Table 6
Multi-voxel representations of low-level visual features on day 1.
MNI | |||||
|---|---|---|---|---|---|
| Brain region | x | y | z | Z value | Cluster size |
| MVPA day 1, all trials, N = 23 | |||||
| R middle occipital gyrus | 12 | -88 | 10 | 16470 | |
| R inferior temporal gyrus | 40 | 12 | -40 | 3.92 | 180 |
| MVPA day 1, correct and high confidence trials, N = 14 | |||||
| R middle occipital gyrus | 12 | -88 | 10 | 6.24 | 12975 |
| L postcentral gyrus | -52 | -22 | 40 | 4.32 | 83 |
| L insular cortex | -35 | 10 | 2 | 4.27 | 75 |
| R inferior frontal gyrus | 50 | 5 | 0 | 3.88 | 91 |
-
Clusters that significantly discriminated the low-level visual features during retrieval on day 1. Bold font indicates the type of MVPA analysis (day 1, training and testing the classifier on day 1 using cross-validation; Materials and methods, Complementary analysis: AG involvement in schema retrieval on day 1). MNI coordinates represent the location of peak voxels. We report the local maximum of each cluster. Effects were tested for significance using cluster-inference with a cluster-defining threshold of P < 0.001 and a cluster-probability of P < 0.05 family-wise error (FWE) corrected for multiple comparisons (critical cluster sizes: upper part, 80 voxels; lower part, 65 voxels). L – left, R – right.
Table 7
Hippocampal connectivity during schema retrieval.
MNI | |||||
|---|---|---|---|---|---|
| Brain region | x | y | z | Z value | Cluster size |
| Day 1 & day 2 | |||||
| R precuneus | 2 | -55 | 18 | 7.06 | 18139 |
| Cerebellum | -5 | -52 | -45 | 6.04 | 602 |
| R angular gyrus | 52 | -60 | 30 | 4.84 | 339 |
| R superior parietal gyrus | 28 | -38 | 58 | 4.62 | 139 |
| L insular cortex | -32 | -20 | 20 | 4.57 | 90 |
| R middle occipital gyrus | 32 | -80 | 40 | 3.94 | 111 |
| Day 1 > day 2 | |||||
| R cingulate gyrus | 2 | 22 | -5 | 5.12 | 162 |
| R middle occipital gyrus | 35 | -90 | 0 | 4.91 | 279 |
| L middle occipital gyrus | -38 | -88 | -2 | 4.43 | 295 |
| R superior frontal gyrus | 28 | 5 | 70 | 4.23 | 108 |
| R middle frontal gyrus | 22 | 58 | 18 | 4.01 | 144 |
| R cingulate gyrus | 5 | 40 | 15 | 4.01 | 87 |
-
Clusters that showed a significant increase in hippocampal connectivity during schema retrieval (Materials and methods, Complementary analysis: hippocampal connectivity during schema retrieval). Bold font indicates contrasts. Retrieval (collapsed across spatial and non-spatial schema conditions) was compared to the perceptual baseline. MNI coordinates represent the location of peak voxels. We report the local maximum of each cluster. Effects were tested for significance using cluster-inference with a cluster-defining threshold of P < 0.001 and a cluster-probability of P < 0.05 family-wise error (FWE) corrected for multiple comparisons (critical cluster size = 76 voxels). L – left, R – right.
Author response table 1
Changes in activation as a function of run on day 1. Retrieval (collapsed across spatial and non-spatial schema conditions) was compared to the perceptual baseline. Bold font indicates contrasts. …
MNI | |||||
|---|---|---|---|---|---|
Brain region | x | y | z | Z value | Cluster size |
Increase, run 1 to 7 | |||||
L cingulate gyrus | -5 | -48 | 20 | 4.37 | 95 |
L superior frontal gyrus | -8 | 48 | 35 | 4.33 | 473 |
R superior frontal gyrus | 5 | 60 | 18 | 4.31 | |
R superior frontal gyrus | 15 | 58 | 0 | 4.21 | |
L angular gyrus | -52 | -62 | 22 | 3.74 | 68 |
L angular gyrus | -38 | -58 | 28 | 3.57 | |
Decrease, run 1 to 7 | |||||
R middle occipital gyrus | 35 | -70 | 30 | 4.69 | 313 |
R angular gyrus | 35 | -58 | 45 | 3.87 | |
R superior parietal gyrus | 35 | -45 | 42 | 3.85 | |
L supramarginal gyrus | -42 | -40 | 38 | 4.45 | 122 |
L superior parietal gyrus | -45 | -45 | 58 | 4.27 | |
cerebellum | 12 | -60 | -15 | 4.23 | 301 |
cerebellum | 0 | -48 | -10 | 4.22 | |
R fusiform gyrus | 32 | -40 | -18 | 3.92 | |
L inferior occipital gyrus | -32 | -68 | -18 | 4.17 | 199 |
cerebellum | -38 | -65 | -28 | 4.02 |
