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Hippocampal-neocortical functional reorganization underlies children's cognitive development

Nature Neuroscience volume 17, pages 1263–1269 (2014)Cite this article

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An Erratum to this article was published on 25 November 2015

This article has been updated

Abstract

The importance of the hippocampal system for rapid learning and memory is well recognized, but its contributions to a cardinal feature of children's cognitive development—the transition from procedure-based to memory-based problem-solving strategies—are unknown. Here we show that the hippocampal system is pivotal to this strategic transition. Longitudinal functional magnetic resonance imaging (fMRI) in 7–9-year-old children revealed that the transition from use of counting to memory-based retrieval parallels increased hippocampal and decreased prefrontal-parietal engagement during arithmetic problem solving. Longitudinal improvements in retrieval-strategy use were predicted by increased hippocampal-neocortical functional connectivity. Beyond childhood, retrieval-strategy use continued to improve through adolescence into adulthood and was associated with decreased activation but more stable interproblem representations in the hippocampus. Our findings provide insights into the dynamic role of the hippocampus in the maturation of memory-based problem solving and establish a critical link between hippocampal-neocortical reorganization and children's cognitive development.

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Figure 1: Experimental design and behavioral results.
Figure 2: Longitudinal changes in hippocampal engagement during childhood.
Figure 3: Longitudinal changes in hippocampal-neocortical functional coupling in relation to individual improvements in children's retrieval fluency.
Figure 4: Longitudinal changes in hippocampal engagement during childhood and further development through adolescence into adulthood.
Figure 5: Interproblem multivoxel pattern stability in the hippocampus in children at time 1 (T1) and time 2 (T2), adolescents and adults.

Change history

  • 04 June 2015

    In the version of this article initially published, the second set of hippocampal coordinates in the fourth Results section was given as (−26,−22,−1). The correct coordinates are (−26,−22,−16). The error has been corrected in the HTML and PDF versions of the article.

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Acknowledgements

This work was supported by grants from US National Institutes of Health (HD047520, HD059205 and MH101394), Child Health Research Institute at Stanford University, Lucile Packard Foundation for Children's Health and Stanford CTAS (UL1RR025744) and Netherlands Organization for Scientific Research (NWO446.10.010).

Author information

Authors and Affiliations

  1. Department of Psychiatry and Behavioral Sciences, Stanford University School of Medicine, Stanford, California, USA

    Shaozheng Qin, Soohyun Cho, Tianwen Chen, Miriam Rosenberg-Lee & Vinod Menon

  2. Department of Psychology, Chung-Ang University, Seoul, South Korea

    Soohyun Cho

  3. Department of Psychological Sciences, Interdisciplinary Neuroscience, University of Missouri, Columbia Missouri, USA.,

    David C Geary

  4. Department of Neurology and Neurological Sciences & Program of Neuroscience, Stanford University, Stanford, California, USA

    Vinod Menon

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Contributions

S.Q. and V.M. designed research; S.Q., S.C., T.C. and M.R.-L. performed research; S.Q. and T.C. analyzed data; S.Q., D.C.G. and V.M. wrote the paper.

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Correspondence to Shaozheng Qin or Vinod Menon.

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Integrated supplementary information

Supplementary Figure 1 Longitudinal and cross-sectional changes in accuracy and RTs during addition problem solving.

(a) Accuracy in the block design fMRI task, (b) Accuracy in the event-related fMRI task, (c) RTs in the block design fMRI task, (d) RTs in the event-related fMRI task. Data are plotted separately for children at Time-1 and Time-2 (N = 28), adolescents (N = 20) and adults (N = 20). Error bars represent standard error (s.e.m.) of the mean. Notes: T1, time-1; T2-, time-2; Addition, addition problems; Control, control problems; sec, seconds; *, P < 0.05; **, P < 0.01; ***, P < 0.001.

Supplementary Figure 2 Brain areas activated during addition problem solving in children.

Surface rendering of brain regions in the left and right hemispheres showing a significant main effect of task (Addition vs. Control). Data were collapsed across Time-1 and Time-2 of the longitudinal fMRI sample. Hippocampus and prefrontal cortex areas are highlighted in panels (a), (b) and (c). These regions can be broadly classified into the following three functional systems: (1) a fronto-parietal network, including the dorsolateral prefrontal cortex (DLPFC), the inferior frontal gyrus (IFG) extending into the insula (a), and the inferior parietal sulcus (IPS), regions important for working memory and mathematical cognition; (2) an anterior and medial temporal lobe network, including the hippocampus and the anterior temporal lobe, regions critical for episodic and semantic memory; (3) a motor, basal ganglia and cerebellar network, including the supplemental motor area and primary motor cortex (PMC), the striatum and cerebellum, regions (see Table S2) important for learning procedures and sequencing operations. Significant clusters of activation are overlaid on a high-resolution anatomical template in MNI space. Notes: L, left; R, right.

Supplementary Figure 3 Longitudinal changes in task-related activation in the prefrontal cortex and the parietal cortex during addition problem solving.

(a-c) Bilateral dorsolateral prefrontal cortex (DLPFC), left superior parietal lobule (SPL), right parietal-occipital regions (i.e., angular gyrus, AG) that show significant decreases in task-related activation from Time-2 to Time-1. (d-f) Each line represents each individual’s developmental trajectories of the DLPFC, SPL, AG engagement over time. Bold green lines represent the mean across all individuals for Time-1 and Time-2 separately. Significant clusters of activation are overlaid on a high-resolution anatomical template in MNI space. Notes: L, left; R, right.

Supplementary Figure 4 Longitudinal changes in task-related hippocampal functional connectivity.

Right hippocampus seed region (red circle) used in task-dependent functional connectivity analysis using a psychophysiological interaction (PPI) approach1. Between Time-1 and Time 2, significant increases in the hippocampal functional connectivity were observed with (a) ventromedial prefrontal cortex (vmPFC), (b) left inferior frontal gyrus (IFG) and left anterior temporal lobe (ATL), and (c) right dorsolateral prefrontal cortex (DLPFC). Significant clusters of activation are overlaid on a high-resolution anatomical template in MNI space. (d-g) Individual trajectories representing longitudinal changes in connectivity strength were plotted for corresponding brain regions. Notes: L, left; R, Right; T1 & T2, two time points in the longitudinal fMRI in children.

Supplementary Figure 5 Developmental changes in task-related activation in the medial temporal lobe from childhood through adolescence into adulthood.

Coronal view of activation patterns in the medial temporal lobe during Addition (vs. Control) problem solving in children at Time-1 (a), Time-2 (b), adolescents (c) and adults (d). The most prominent activation of the medial temporal lobe was observed in children at Time-2, but not in children at Time-1, adolescents or adults. Details about other brain regions are listed in Table S2 and S6. Notes: Hipp, hippocampus; BG, basal ganglia; L, left; R, right.

Supplementary Figure 6 Correlation between task-related activation and addition task performance across children, adolescents and adults.

(a-c) Significant clusters in the left dorsolateral prefrontal cortex (DLPFC), the left middle temporal gyrus (MTG), and the right temporal pole (TP) show negative correlations with accuracy; (d) A significant cluster in the right motor cortex (MC) shows positive correlation with accuracy; (e) A significant cluster in the left superior parietal lobe (SPL) shows negative correlation with reaction times (RTs) – that is, a positive correlation with improved performance. (f) A significant cluster in the left insula shows positive correlations with RTs, or negative correlation with improved performance. (g-j) No reliable associations between hippocampal mean activation (extracted from the entire AAL hippocampal masks), accuracy and RTs were observed. The red box highlights null correlations between hippocampal activation and improvement in accuracy and RTs.

Supplementary Figure 7 Developmental changes in interproblem multivoxel pattern stability in frontal cortex and ventral-temporal cortex.

Significant clusters were derived from an omnibus F-contrast in children at Time-2, adolescents, and adults. Separate paired t-tests were conducted for longitudinal changes between Time-1 and Time-2 in children for each region. Separate ANOVAs were conducted to define cross-sectional changes from childhood through adolescence into adulthood, and post-hoc Scheffe’s procedures were used to control for multiple group comparisons. Notes: IFS, inferior frontal sulcus; IFG, inferior frontal gyrus; In, insula; PCG, postcentral gyrus; FG, fusiform gyrus; MTG, middle temporal gyrus. L, left; R, right.

Supplementary Figure 8 Interproblem multivoxel pattern stability analysis with comparable number of correctly solved problems across groups.

(a-b) Increases in inter-problem pattern stability for those problems correctly solved in the anatomically-defined left and right hippocampus in adolescents and adults compared to children at Time-1 (T1) or Time-2 (T2). Mean and standard deviation of the number of correctly solved problems was matched across groups (see Table S10). (c-d) Results of whole-brain analysis showing significant increases in pattern stability in the bilateral hippocampus in childhood compared to adolescence and adulthood. Notes: * P < 0.05; **, P < 0.01; m.s., marginally significant (P value, 0.08; two-tailed); L, left; R, right.

Supplementary Figure 9 Task-related activation in the hippocampus using AAL masks versus manually drawn ROIs (based on a pediatric brain template).

Pediatric brain template images are derived from twelve 8.5 year-old children2 and adult automated anatomical labelling (AAL) masks of the hippocampus. Left panel: Results using hippocampal AAL masks are reported in the main text. Right panel: Results from hand-drawn hippocampal ROIs (see online Methods for details). Notes: * P < 0.05; **, P < 0.01; L, left; R, right.

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Supplementary Figures 1–9, Supplementary Results and Supplementary Tables 1–9 (PDF 6802 kb)

Supplementary Methods Checklist (PDF 183 kb)

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Qin, S., Cho, S., Chen, T. et al. Hippocampal-neocortical functional reorganization underlies children's cognitive development. Nat Neurosci 17, 1263–1269 (2014). https://doi.org/10.1038/nn.3788

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