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Developmental change in prefrontal cortex recruitment supports the emergence of value-guided memory

  1. Kate Nussenbaum
  2. Catherine A Hartley  Is a corresponding author
  1. New York University, United States
Research Article
Cite this article as: eLife 2021;10:e69796 doi: 10.7554/eLife.69796
13 figures, 36 tables and 1 additional file

Figures

Task structure.

Participants first learned the frequencies of each item (A) by viewing them in a continuous stream. They then were shown the information associated with each item (B). During retrieval, participants had to report the information associated with each item (C) as well as the item’s original frequency (D).

Neural activation during frequency learning.

(A) During frequency learning, participants demonstrated increased recruitment of regions in the frontal cortex, angular gyrus, and striatum on the last vs. first appearance of high-frequency items. (B) They demonstrated decreased activation in the lateral occipital cortex, temporal occipital cortex, and parahippocampal cortex. (C) Within a parahippocampal ROI (shown in green), the decrease in responses to each stimulus on its last vs. first appearance was greater in older participants.

Repetition suppression during frequency learning.

(A) Neural activation within a bilateral parahippocampal cortex ROI decreased across stimulus repetitions both linearly, F(1, 5015.9) = 30.64, p < 0.001, and quadratically, F(1, 9881.0) = 7.47, p = 0.006. Repetition suppression increased with linear age, F(1, 7267.5) = 7.2, p = 0.007, and quadratic age F(1, 7260.8) = 6.9, p = 0.009. The horizontal black lines indicate median neural activation values. The lower and upper edges of the boxes indicate the first and third quartiles of the grouped data, and the vertical lines extend to the smallest value no further than 1.5 times the interquartile range. Grey dots indicate data points outside those values. (B) The decrease in neural activation in the bilateral PHC ROI from the first to fifth repetition of each item also increased with both linear age, F(1, 78.32) = 3.97, p = 0.05, and quadratic age, F(1, 77.55) = 4.8, p = 0.031. The line on the scatter plot represents the best-fitting regression line from the model including both linear and quadratic age terms. The shaded region represents 95% confidence intervals.

Memory accuracy by age and frequency condition.

Participants demonstrated prioritization of memory for high-value information, as indicated by higher memory accuracy for associations involving items in the five- relative to the one-frequency condition (χ2(1) = 19.73, p < 0.001). The effects of item frequency on associative memory increased throughout childhood and into adolescence (linear age x frequency condition: χ2(1) = 10.74, p = 0.001; quadratic age x frequency condition: χ2(1) = 9.27, p = 0.002). The thin grey lines connect each dots representing each participant's memory accuracy for items in the one- and five-frequency condition. The thicker colored lines represent the best-fitting regression lines from models including linear and quadratic age terms. The shaded regions represent 95% confidence intervals.

Neural activation during encoding.

(A) During encoding of associations involving high- vs. low-frequency items, participants demonstrated greater engagement of the lateral PFC and caudate. (B) Participants who demonstrated the greatest value-based modulation of memory also demonstrated the greatest modulation of left prefrontal cortical activation during encoding of high- vs. low-value associations. (C) During encoding of both high- and low-value pairs, older participants demonstrated greater recruitment of the PFC relative to younger participants.

PFC activation mediates the relation between age and value-guided memory.

The increased engagement of left lateral PFC (ROI depicted in red) during encoding of high- vs. low-value information mediated the relation between age and memory difference scores (standardized indirect effect: .07, 95% confidence interval: [0.01, 0.15], p = 0.017; standardized direct effect: .15, 95% confidence interval: [−0.03, 0.33], p = 0.108). Path a shows the regression coefficient of the relation between age and PFC modulation. Path b shows the regression coefficient of the relation between PFC activation and memory difference scores, while controlling for age. Paths c and c’ show the regression coefficient of the relation between age and memory difference scores without and while controlling for PFC activation, respectively. † denotes p<0.06, * denotes p<0.05, ** denotes p<0.01.

Neural activation during retrieval.

(A) During retrieval, older participants demonstrated greater recruitment of the inferior frontal cortex relative to younger participants. (B) During retrieval of associations involving high- vs. low-frequency items, participants demonstrated greater engagement of the left lateral PFC and bilateral caudate.

Memory accuracy by reported frequency.

(A) Participants demonstrated increased associative memory accuracy for items that they reported as being more frequent (χ2(1) = 31.20, p < 0.001). This effect strengthened with increasing age (frequency report x linear age: χ2(1) = 10.37, p = 0.001; frequency report x quadratic age: χ2(1) = 9.50, p = 0.002). (B) Participants also demonstrated better memory for associations involving high-frequency items to which they demonstrated the greatest repetition suppression during frequency learning (χ2(1) = 11.21, p < 0.001). In both panels, the shading of the bars represents the number of trials included in each bin.

Appendix 1—figure 1
Participant age and sex distribution.
Appendix 2—figure 1
Frequency learning accuracy and reaction times.

(A) During frequency learning, older participants were more accurate in identifying items as new (χ2(1) = 25.54, p < 0.001) and as repeated (χ2(1) = 33.81, p < 0.001). All participants became more accurate in identifying items as repeated as the number of repetitions increased (χ2 = 138.20, p < 0.001), though younger participants demonstrated a greater increase in accuracy throughout learning (χ2(1) = 17.52, p < 0.001). (B) Older participants also responded to both new (F(1, 85.99) = 32.51, p < 0.001) and repeated (F(1, 87.55) = 21.82, p < 0.001) items more quickly than younger participants. Reaction times to old items became faster as the a function of item repetition number (F(1, 69.94) = 282.21, p < 0.001).

Appendix 2—figure 2
Relation between age and associative memory.

Results from the two-lines test (Simonsohn, 2018) revealed that the influence of frequency condition on memory accuracy increased throughout childhood and early adolescence, and did not significantly decrease from adolescence into early adulthood.

Appendix 2—figure 3
Prefrontal cortex activation during encoding.

Mean beta weights averaged over voxels within a prefrontal cortex ROI (see ‘methods’ in main text) during encoding of associations involving high- vs. low-frequency items increased with age. The increase was greatest in childhood before leveling out into late adolescence and early adulthood. The line represents the best-fitting regression line from the model including both linear and quadratic age. The shaded region represents 95% confidence intervals.

Appendix 2—figure 4
Associative memory across blocks.

Participants demonstrated a greater influence of frequency condition on associative memory in the task block involving postcards and stamps relative to the task block involving pictures and frames (χ2(1) = 0.4.40, p = 0.036).

Tables

Appendix 1—table 1
Number of participants included in each analysis.
BlockData typeFrequency- learningAssociative encodingRetrievalFrequency reports
1Behavioral89NA9090
1Neural889090NA
2Behavioral86NA8585
2Neural848181NA
Appendix 2—table 1
Associative memory accuracy by frequency condition with block order.
Estimate95% CIΧ2p
Intercept0.260.12–0.40
Age1.420.52–2.338.970.003
Age2−0.97−1.87 - −0.084.390.036
WASI0.280.14–0.4115.09<0.001
Frequency Condition−0.22−0.31 - −0.1319.47<0.001
Block Order−0.02−0.11–0.070.180.676
Age x WASI0.15−0.80–1.100.100.756
Age2 x WASI−0.10−1.00–0.800.040.833
Age x Block Order−0.23−0.85–0.390.530.468
Age2 x Block Order0.13−0.48–0.750.180.675
Age x Frequency Condition−1.05−1.68 - −0.4310.310.001
Age2 x Frequency Condition0.97−0.35–1.598.940.003
WASI x Frequency Condition−0.04−0.13–0.050.650.419
Block Order x Frequency Condition−0.03−0.10–0.050.760.384
Block Order x WASI−0.05−0.15–0.041.130.288
Age x WASI x Frequency Condition−0.53−1.19–0.132.430.119
Age2 x WASI x Frequency Condition0.54−0.08–1.172.830.092
Age x Block Order x Frequency Condition−0.35−0.86–0.161.800.180
Age2 x Block Order x Frequency Condition0.27−0.23–0.771.100.294
WASI x Block Order x Frequency Condition−0.05−0.12–0.031.350.246
WASI x Age x Block Order0.05−0.61–0.700.020.887
WASI x Age2 x Block Order−0.01−0.63–0.620.000.985
Age x WASI x Frequency Condition x Block Order0.35−0.19–0.891.610.205
Age2 x WASI x Frequency Condition x Block Order−0.33−0.85–0.181.620.203
Appendix 2—table 2
Associative memory accuracy by frequency condition with block type.
Estimate95% CIΧ2p
Intercept0.260.12–0.40
Age1.400.49–2.318.610.003
Age2−0.95−1.85 - −0.054.160.041
WASI0.270.14–0.4014.46<0.001
Frequency Condition−0.22−0.31 - −0.1320.07<0.001
Block Type−0.10−0.20–0.003.520.061
Age x WASI0.17−0.79–1.120.120.734
Age2 x WASI−0.10−1.01–0.800.050.822
Age x Block Type0.23−0.39–0.850.530.465
Age2 x Block Type−0.28−0.89–0.330.790.375
Age x Frequency Condition−1.05−1.68 - −0.4210.060.002
Age2 x Frequency Condition0.960.34–1.598.640.003
WASI x Frequency Condition−0.04−0.13–0.050.650.419
Block Type x Frequency Condition−0.08−0.15 - −0.014.400.036
Block Type x WASI0.01−0.08–0.100.030.866
Age x WASI x Frequency Condition−0.51−1.18–0.152.240.135
Age2 x WASI x Frequency Condition0.52−0.11–1.152.560.109
Age x Block Type x Frequency Condition0.31−0.19–0.821.440.230
Age2 x Block Type x Frequency Condition−0.29−0.79–0.211.280.258
WASI x Block Type x Frequency Condition−0.03−0.10–0.050.440.505
WASI x Age x Block Type0.62−0.03–1.273.440.064
WASI x Age2 x Block Type−0.60−1.22–0.023.570.059
Age x WASI x Frequency Condition x Block Type−0.31−0.84–0.231.280.258
Age2 x WASI x Frequency Condition x Block Type0.34−0.17–0.851.680.195
Appendix 2—table 3
High- vs. low-value encoding PFC activation by age with block type.
Estimate95% CIdfFp
Intercept−0.01−0.17–0.15
Age1.600.47–2.731, 79.467.760.007
Age2−1.39−2.50 - −0.281, 79.246.040.016
WASI0.15−0.02–0.321, 86.823.060.084
Block Type−0.04−0.19–0.111, 80.300.300.585
Age x WASI0.45−0.79–1.691, 87.350.500.479
Age2 x WASI−0.53−1.69–0.631, 86.030.790.376
Age x Block Type0.11−0.94–1.161, 78.810.040.843
Age2 x Block Type−0.12−1.16–0.911, 78.590.050.818
WASI x Block Type−0.06−0.22–0.101, 86.370.540.462
Age x WASI x Block Type−0.73−1.89–0.441, 86.581.490.226
Age2 x WASI x Block Type0.68−0.41–1.771, 85.261.480.227
Appendix 2—table 4
Memory difference scores by PFC activation and age with block type.
Estimate95% CIdfFp
Intercept0.090.05–0.13
PFC Activation0.060.02–0.101, 153.789.850.002
Age0.02−0.01–0.061, 84.351.520.221
WASI−0.00−0.04–0.041, 86.860.040.836
Block Type0.03−0.00–0.071, 82.482.920.091
PFC Activation x Age0.01−0.03–0.061, 153.530.280.598
PFC Activation x WASI0.03−0.01–0.081, 154.292.130.147
Age x WASI−0.01−0.05–0.031, 86.370.220.642
PFC Activation x Block Type−0.01−0.04–0.031, 151.410.090.770
Age x Block Type0.01−0.03–0.041, 82.910.130.718
WASI x Block Type0.02−0.02–0.051, 85.400.760.385
PFC Activation x Age x WASI−0.01−0.06–0.041, 152.590.140.711
PFC Activation x Age x Block Type0.03−0.02–0.081, 152.381.560.214
PFC Activation x WASI x Block Type−0.04−0.09–0.001, 151.643.490.064
Age x WASI x Block Type−0.02−0.05–0.011, 85.201.230.270
PFC Activation x Age x WASI x Block Type0.05−0.01–0.101, 154.253.000.085
Appendix 3—table 1
Frequency-learning accuracy: new items.
Estimate95% CIΧ2p
Intercept3.082.73–3.44
Age0.920.58–1.2525.52<0.001
WASI0.430.09–0.776.180.013
Age x WASI0.25−0.08–0.572.250.134
Appendix 3—table 2
Frequency-learning accuracy: repeated item appearances.
Estimate95% CIΧ2p
Intercept3.833.46–4.20
Appearance1.531.28–1.78138.03<0.001
Age0.970.64–1.2933.43<0.001
WASI0.460.13–0.797.580.006
Appearance x Age0.450.24–0.6717.41<0.001
Appearance x WASI0.05−0.17–0.260.180.672
Age x WASI0.12−0.20–0.450.570.449
Appearance x Age x WASI0.04−0.17–0.250.140.707
Appendix 3—table 3
Frequency-learning reaction times: new items.
Estimate95% CIdfFp
Intercept1.121.09–1.15
Age−0.08−0.11 - −0.051, 85.9932.51<.001
WASI−0.01−0.04–0.021, 82.340.56.457
Age x WASI−0.02−0.05 - −0.011, 83.142.12.149
Appendix 3—table 4
Frequency-learning reaction times: repeated items.
Estimate95% CIdfFp
Intercept1.031.00–1.06
Age−0.07−0.10 – −0.041, 87.5521.82<0.001
WASI−0.03−0.06 – −0.011, 86.272.650.108
Appearance−0.08−0.09 – −0.071, 69.94282.21<0.001
Age x WASI−0.01−0.03–0.021, 84.970.220.641
Age x Appearance−0.01−0.01–0.001, 77.061.260.265
WASI x Appearance0.00−0.01–0.011, 75.790.000.992
Age x WASI x Appearance0.00−0.01–0.011, 74.960.680.413
Appendix 3—table 5
Parahippocampal cortex neural activation by stimulus repetition and age.
Estimate95% CIdfFp
Intercept65.7052.23–79.17
Age−78.41−164.25–7.431, 82.783.210.077
Age282.54−2.27–167.351, 82.773.640.060
Repetition−30.20−40.89 – −19.501, 5015.9430.64<0.001
Repetition214.524.10–24.931, 9881.007.470.006
WASI−1.11−13.49–11.271, 83.310.030.861
Age x Repetition101.6527.40–175.901, 7267.467.200.007
Age x Repetition2−88.18161.49 - −14.871, 9857.855.560.018
Age2 x Repetition97.99−171.28 - −24.711, 7260.706.870.009
Age2 x Repetition282.7610.40–155.111, 9854.925.030.025
WASI x Age28.87−61.72–119.471, 83.510.390.534
WASI x Age2−20.73−106.34–64.881, 83.470.230.636
WASI x Repetition−7.56−18.46–3.351, 7402.991.840.175
WASI x Repetition27.40−3.38–18.181, 7857.101.810.178
WASI x Age x Repetition−52.32−130.26–25.611, 7243.451.730.188
WASI x Age x Repetition242.15−34.79–119.081, 9868.651.150.283
WASI x Age2 x Repetition45.97−27.58–119.531, 7235.301.500.221
WASI x Age2 x Repetition2−38.01−110.62–34.591, 9867.591.050.305
Appendix 3—table 6
Repetition suppression indices.
Estimate95% CIdfFp
Intercept45.5435.63–55.45
Age−61.34−8.56–10.771, 78.323.970.050
Age266.52−121.70 - −0.981, 77.554.800.031
WASI1.117.01–126.031, 58.060.050.823
Age x WASI60.90−2.53–124.341, 77.383.540.064
Age2 x WASI−51.17−111.03–8.701, 77.162.810.098
Appendix 3—table 7
Frequency report error magnitudes.
Estimate95% CIdfFp
Intercept1.211.12–1.30
Age−0.18−0.27 - - 0.101, 94.3017.57<0.001
WASI−0.11−0.19 - −0.021, 83.806.470.014
Frequency Condition−0.00−0.11–0.111, 93.810.000.993
Age x WASI−0.07−0.15–0.011, 86.353.240.075
Age x Frequency Condition−0.05−0.17–0.061, 85.480.950.332
WASI x Frequency Condition−0.03−0.14–0.091, 86.550.200.652
Age x WASI x Frequency Condition−0.07−0.17–0.031, 85.941.770.187
Appendix 3—table 8
Frequency reports by repetition suppression.
Estimate95% CIdfFp
Intercept4.444.26–4.63
Age0.260.09–0.421, 82.878.930.004
WASI0.190.02–0.361, 85.194.770.032
Repetition Suppression0.00−0.06–0.071, 1360.740.010.903
Age x WASI0.09−0.07–0.251, 84.131.340.251
Age x Repetition Suppression0.06−0.00–0.121, 938.873.610.058
WASI x Repetition Suppression0.04−0.02–0.101, 58.811.520.222
Age x WASI x Repetition Suppression−0.03−0.08–0.031, 313.721.100.296
Appendix 3—table 9
Associative memory accuracy by frequency condition.
Estimate95% CIΧ2p
Intercept0.260.12–0.40
Age1.380.49–2.288.680.003
Age2−0.95−1.83 – −0.064.240.039
WASI0.260.13–0.3914.18<0.001
Frequency Condition−0.21−0.30 – −0.1319.73<0.001
Age x WASI0.18−0.76–1.120.140.704
Age2 x WASI−0.12−1.01–0.770.070.789
Age x Frequency Condition−1.06−1.68 – −0.4510.740.001
Age2 x Frequency Condition0.980.37–1.599.270.002
WASI x Frequency Condition−0.04−0.13–0.050.860.355
Age x WASI x Frequency Condition−0.50−1.15–0.152.260.133
Age2 x WASI x Frequency Condition0.52−0.10–1.132.650.104
Appendix 3—table 10
Associative memory accuracy by frequency condition (below-chance subjects excluded).
Estimate95% CIΧ2p
Intercept0.300.16–0.44
Age1.190.29–2.096.480.011
Age2−0.79−1.68–0.102.980.084
WASI0.240.11–0.3712.44<0.001
Frequency Condition−0.22−0.31 – −0.1320.04<0.001
Age x WASI0.31−0.62–1.240.430.513
Age2 x WASI−0.23−1.11–0.660.250.615
Age x Frequency Condition−1.07−1.70 - −0.4310.250.001
Age2 x Frequency Condition0.990.36–1.618.970.003
WASI x Frequency Condition−0.04−0.14–0.050.810.368
Age x WASI x Frequency Condition−0.50−1.16–0.162.170.141
Age2 x WASI x Frequency Condition0.52−0.11–1.152.540.111
Appendix 3—table 11
Associative memory accuracy by frequency condition (with frequency-learning covariates).
Estimate95% CIΧ2p
Intercept0.250.12–0.38
Age0.59−0.31–1.491.620.203
Age2−0.30−1.17–0.560.470.491
WASI0.160.03–0.296.020.014
Frequency Condition−0.21−0.30 – −0.1319.65<0.001
Mean Frequency Report Error Magnitude−0.26−0.39 – −0.1213.05<0.001
Frequency-learning Accuracy0.17−0.04–0.382.360.125
Frequency-learning Accuracy (last item appearance)−0.10−0.30–0.091.060.304
Age x WASI0.11−0.75–0.960.060.807
Age2 x WASI−0.08−0.89–0.720.040.843
Age x Frequency Condition−1.06−1.67 - −0.4410.590.001
Age2 x Frequency Condition0.970.36–1.589.150.002
WASI x Frequency Condition−0.04−0.13–0.050.830.362
Age x WASI x Frequency Condition−0.50−1.15–0.152.220.136
Age2 x WASI x Frequency Condition0.51−0.10–1.132.610.106
Appendix 3—table 12
High vs. low-value encoding caudate activation by age.
EstimateSEtp
Intercept−0.07.104
Age0.16.1071.550.126
WASI0.18.1101.640.105
Age x WASI−0.29.101−2.860.005
Appendix 3—table 13
High vs. low-value encoding PFC activation by age.
EstimateSEtp
Intercept0.00.105
Age1.97.7432.650.009
Age2−1.73.734−2.350.021
WASI0.26.1092.340.022
Age x WASI0.93.7891.180.240
Age2 x WASI−1.02.745−1.370.174
Appendix 3—table 14
Associative memory accuracy by frequency report.
Estimate95% CIΧ2p
Intercept0.260.12–0.40
Age1.460.55–2.389.250.002
Age2−1.01−1.92 – −0.114.640.031
WASI0.270.13–0.4013.94<0.001
Frequency Report0.280.19–0.3731.20<0.001
Age x WASI0.15−0.81–1.120.090.759
Age2 x WASI−0.10−1.01–0.820.040.838
Age x Frequency Report1.130.46–1.7910.370.001
Age2 x Frequency Report−1.07−1.73 – −0.419.500.002
WASI x Frequency Report0.02−0.08–0.110.100.754
Age x WASI x Frequency Report0.37−0.35–1.091.000.316
Age2 x WASI x Frequency Report−0.33−1.01–0.350.890.345
Appendix 3—table 15
Associative memory accuracy by repetition suppression.
Estimate95% CIΧ2p
Intercept0.510.32–0.69
Age2.631.43–3.8316.87<0.001
Age2−2.13−3.31 – −0.9411.55<0.001
WASI0.310.14–0.4911.47<0.001
Repetition Suppression0.230.10–0.3711.21<0.001
Age x WASI0.78−0.49–2.051.440.230
Age2 x WASI−0.75−1.95–0.451.470.225
Age x Repetition Suppression−0.42−1.32–0.490.790.374
Age2 x Repetition Suppression0.64−0.28–1.571.790.181
WASI x Repetition Suppression0.00−0.13–0.140.000.954
Age x WASI x Repetition Suppression−0.17−1.02–0.680.150.700
Age2 x WASI x Repetition Suppression0.27−0.57–1.100.370.541
Appendix 3—table 16
Associative memory accuracy by repetition suppression and frequency reports.
Estimate95% CIΧ2p
Intercept0.510.32–0.69
Repetition Suppression0.230.09–0.3610.250.001
WASI0.260.08–0.447.590.006
Frequency Report0.30.17–0.4221.16<0.001
Age2.471.25–3.6914.4<0.001
Age2−2.02−3.23 – −0.819.980.002
Repetition Suppression x WASI0.00−0.13–0.140.000.968
Repetition Suppression x Frequency Report−0.11−0.25–0.042.180.140
WASI x Frequency Report−0.05−0.18–0.080.480.488
Repetition Suppression x Age−0.12−1.05–0.810.060.804
Repetition Suppression x Age20.33−0.62–1.270.450.503
WASI x Age0.92−0.36–2.211.960.161
WASI x Age2−0.89−2.12–0.332.040.153
Frequency Report x Age0.12−0.74–0.990.080.783
Frequency Report x Age2−0.09−0.97–0.790.040.843
RS x WASI x Frequency Report−0.04−0.19–0.110.270.603
RS x WASI x Age−0.28−1.16–0.610.360.550
RS x WASI x Age20.39−0.49–1.260.710.400
RS x Frequency Report x Age0.13−0.78–1.030.070.786
RS x Frequency Report x Age2−0.12−1.09–0.850.060.809
WASI x Frequency Report x Age−0.33−1.31–0.650.440.509
WASI x Frequency Report x Age20.44−0.52–1.400.790.374
RS x WASI x Frequency Report x Age−0.73−1.68–0.222.290.130
RS x WASI x Frequency Report x Age20.83−0.14–1.802.860.091
Appendix 3—table 17
Mean repetition suppression indices by age.
EstimateSEtp
Intercept44.764.53
Age−59.0031.82−1.850.067
Age264.9331.372.070.042
WASI1.864.720.390.695
Age x WASI57.0633.891.680.096
Age2 x WASI−48.0231.93−1.500.136
Appendix 3—table 18
Caudate activation by repetition suppression indices.
EstimateSEtp
Intercept8.231.54
Repetition Suppression2.311.601.440.153
Age1.481.640.910.367
WASI1.931.641.170.244
Repetition Suppression x Age1.291.420.910.366
Repetition Suppression x WASI0.261.540.170.864
Age x WASI−4.401.50−2.940.004
Repetition Suppression x Age x WASI−0.091.22−0.070.945
Appendix 3—table 19
PFC activation by repetition suppression indices.
EstimateSEtp
Intercept28.664.51
Repetition Suppression−6.784.83−1.400.165
Age103.3635.332.930.004
Age2−94.2535.13−2.680.009
WASI13.594.742.870.005
Repetition Suppression x Age−54.1534.13−1.590.112
Repetition Suppression x Age253.8532.791.640.105
Repetition Suppression x WASI−3.284.49−0.730.467
Age x WASI30.4334.440.880.380
Age2 x WASI−38.5932.41−1.910.237
Repetition Suppression x Age x WASI−41.3329.80−1.390.169
Repetition Suppression x Age2 x WASI41.4627.581.500.137
Appendix 3—table 20
Frequency distance by age.
EstimateSETp
Intercept2.23.09
Age2.75.674.10<0.001
Age2−2.28.66−3.44<0.001
WASI0.38.103.89<0.001
Age x WASI0.33.710.460.646
Age2 x WASI−0.12.67−0.180.857
Appendix 3—table 21
Caudate activation by frequency distance.
EstimateSEtp
Intercept7.001.78
Frequency Distance2.551.861.370.175
Age1.391.890.740.463
WASI1.131.770.640.526
Frequency Distance x Age2.271.771.290.202
Frequency Distance x WASI−1.501.77−0.850.399
Age x WASI−5.491.64−3.430.001
Frequency Distance x Age x WASI1.711.401.220.227
Appendix 3—table 22
PFC activation by frequency distance.
EstimateSEtp
Intercept−0.020.12
Frequency Distance0.420.123.360.001
Age−0.030.13−0.220.824
WASI0.080.120.640.522
Frequency Distance x Age−0.180.12−1.510.136
Frequency Distance x WASI0.150.121.230.223
Age x WASI−0.170.11−1.520.132
Frequency Distance x Age x WASI0.050.090.520.607
Appendix 3—table 23
Memory difference scores by PFC activation and frequency distance.
EstimateSEtp
Intercept0.07
Frequency Distance−0.020.03−0.550.582
Age0.560.22.830.006
Age2−0.510.2−2.60.012
WASI0.020.030.850.398
PFC Activation0.080.041.950.055
Frequency Distance x Age0.290.21.50.139
Frequency Distance x Age2−0.270.2−1.360.178
Frequency Distance x WASI0.010.030.380.709
Age x WASI0.030.190.170.866
Age2 x WASI−0.050.18−0.250.800
Frequency Distance x PFC Activation0.010.040.250.800
Age x PFC Activation−0.150.34−0.430.672
Age2 x PFC Activation0.210.340.620.538
WASI x PFC Activation−0.040.04−0.840.406
Frequency Distance x Age x WASI−0.360.22−1.660.102
Frequency Distance x Age2 x WASI0.330.21.620.111
Frequency Distance x Age x PFC Activation−0.070.27−0.240.809
Frequency Distance x Age2 x PFC Activation0.080.280.280.778
Frequency Distance x WASI x PFC Activation−0.050.03−1.490.142
Age2 x WASI x PFC Activation0.460.361.290.202
Age2 x WASI x PFC Activation−0.460.36−1.280.204
Frequency Distance x Age2 x WASI x PFC Activation0.270.270.990.324
Frequency Distance x Age2 x WASI x PFC Activation−0.280.27−1.070.288
Appendix 4—table 1
Frequency-learning: Last vs. first item appearance cluster table.
RegionxyzCluster sizez-max
Frontal pole−4251024196.33
Precuneus0−663313228.99
Left lateral occipital cortex / angular gyrus−57−663013197.2
Right lateral occipital cortex / angular gyrus51−63336376.03
Right middle temporal gyrus66−33−123045.48
Right cerebellum15−87−271645.33
Precentral gyrus3−18751244.53
Left cerebellum−42−75−42924.72
Left middle temporal gyrus−57-3−27734.44
Left caudate-6129624.91
Right caudate9246605.04
Occipital pole-3−9612464.81
Appendix 4—table 2
Frequency-learning: First vs. last item appearance cluster table.
RegionxyzCluster sizez-max
Right temporal fusiform cortex / lateral occipital cortex / parahippocampal gyrus30−39−1521378.62
Left temporal fusiform cortex / lateral occipital cortex / parahippocampal gyrus−33−63−1518587.53
Cingulate gyrus99421006
Right precuneus18−519806.05
Left postcentral gyrus−51−1557744.73
Right precentral gyrus42333735.54
Juxtapositional lobule cortex6657244.11
Left amygdala−24-6−15224.23
Cingulate gyrus3-333224.68
Central opercular cortex39-315214.8
Appendix 4—table 3
Encoding: Encoding vs. baseline by linear age cluster table.
RegionxyzCluster sizez-max
Right lateral occipital cortex45−81211325
Left precentral gyrus / middle frontal gyrus−5412331205.9
Left lateral occipital cortex−45−8421544.69
Left lateral occipital cortex−27−7242504.32
Right lateral occipital cortex30−6945444.17
Left cerebellum−18−45−48394.55
Superior frontal gyrus-31260394.35
Left supramarginal gyrus−36−4536374.57
Left middle frontal gyrus−33363334.6
Right superior parietal lobule33−4542313.76
Right inferior frontal gyrus481230243.97
Appendix 4—table 4
Encoding: High- vs. low-value cluster table.
RegionxyzCluster sizez-max
Superior parietal lobule / lateral occipital cortex / temporal occipital fusiform cortex / cerebellum−33−545142626.23
Left frontal pole / inferior frontal gyrus / middle frontal gyrus−5142917656.92
Left caudate / thalamus−181262325.67
Right caudate181812544.17
Right precentral gyrus51933504.26
Right precentral gyrus24-954474.79
Left cerebellum-3−510384.73
Right frontal pole513912354.53
Right postcentral gyrus42−3651284.32
Right putamen2715-3264.52
Left thalamus-3−24-3234.65
Left putamen−30−15-6205.7
Appendix 4—table 5
Encoding: High- vs. low-value by memory difference scores cluster table.
RegionxyzCluster sizez-max
Left lateral occipital cortex−45−69-63774.78
Left middle frontal gyrus / inferior frontal gyrus−4821272324.95
Right lateral occipital cortex (inferior)39−9031894.89
Right temporal occipital fusiform cortex42−57-9874.45
Right lateral occipital cortex (superior)27−6633614.83
Appendix 4—table 6
Encoding: Remembered vs. not remembered cluster table.
RegionxyzCluster sizez-max
Right lateral occipital cortex / temporal occipital fusiform gyrus48−75-912965.75
Left lateral occipital cortex / temporal occipital fusiform gyrus / inferior temporal gyrus−48−72-612735.97
Left inferior frontal gyrus−489271034.22
Left inferior frontal gyrus−5721-3403.81
Right hippocampus / amygdala24-6−21214.06
Appendix 4—table 7
Retrieval: Retrieval vs. baseline by linear age cluster table.
RegionxyzCluster sizez-max
Right lateral occipital cortex45−81211475.28
Left lateral occipital cortex−39−8721594.25
Right precentral gyrus / inferior frontal gyrus51321424.21
Right precentral gyrus39−1239414.4
Left postcentral gyrus / supramarginal gyrus−63−2448384.45
Left precentral gyrus−60621364.39
Right lateral occipital cortex27−6057343.76
Cingulate gyrus / left thalamus3−330304.74
Left supramarginal gyrus−69−2424284.33
Appendix 4—table 8
Retrieval: High- vs. low-value cluster table.
RegionxyzCluster sizez-max
Precuneus cortex0−72392994.81
Left lateral occipital cortex−33−69512365.28
Left caudate / thalamus−12-6151285.15
Right cerebellum3−81−301256.12
Left inferior frontal gyrus / middle frontal gyrus−4821241164.57
Left frontal orbital cortex−3030-3884.82
Right cerebellum39−69−36854.65
Right caudate15-321774.96
Left middle frontal gyrus−451248744.31
Cerebellum-3−60−36604.57
Left inferior temporal gyrus−57−60−15604.33
Cingulate gyrus0−333254.09
Right frontal orbital cortex33333214.69
Left frontal pole−36573203.79
Right lateral occipital cortex27−6642204.24

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