Abstract
Brain regions that are involved in memory formation, particularly medial temporal lobe (MTL) structures and lateral prefrontal cortex (PFC), have been identified in adults, but not in children. We investigated the development of brain regions involved in memory formation in 49 children and adults (ages 8–24), who studied scenes during functional magnetic resonance imaging. Recognition memory for vividly recollected scenes improved with age. There was greater activation for subsequently remembered scenes than there was for forgotten scenes in MTL and PFC regions. These activations increased with age in specific PFC, but not in MTL, regions. PFC, but not MTL, activations correlated with developmental gains in memory for details of experiences. Voxel-based morphometry indicated that gray matter volume in PFC, but not in MTL, regions reduced with age. These results suggest that PFC regions that are important for the formation of detailed memories for experiences have a prolonged maturational trajectory.
This is a preview of subscription content, access via your institution
Access options
Subscribe to this journal
Receive 12 print issues and online access
$209.00 per year
only $17.42 per issue
Rent or buy this article
Prices vary by article type
from$1.95
to$39.95
Prices may be subject to local taxes which are calculated during checkout
Similar content being viewed by others
References
Squire, L.R. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99, 195–231 (1992).
Scoville, W.B. & Milner, B. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 20, 11–21 (1957).
Janowsky, J.S., Shimamura, A.P. & Squire, L.R. Source memory impairment in patients with frontal lobe lesions. Neuropsychologia 27, 1043–1056 (1989).
Schacter, D.L., Harbluk, J.L. & Mclachlan, D.R. Retrieval without recollection: an experimental analysis of source amnesia. J. Verbal Learn. Verbal Behav. 23, 593–611 (1984).
Brewer, J.B., Zhao, Z., Desmond, J.E., Glover, G.H. & Gabrieli, J.D.E. Making memories: brain activity that predicts how well visual experience will be remembered. Science 281, 1185–1187 (1998).
Stern, C.E. et al. The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. Proc. Natl. Acad. Sci. USA 93, 8660–8665 (1996).
Davachi, L., Mitchell, J.P. & Wagner, A.D. Multiple routes to memory: distinct medial temporal lobe processes build item and source memories. Proc. Natl. Acad. Sci. USA 100, 2157–2162 (2003).
Buckner, R.L., Kelley, W.M. & Petersen, S.E. Frontal cortex contributes to human memory formation. Nat. Neurosci. 2, 311–314 (1999).
Wagner, A.D. et al. Building memories: remembering and forgetting of verbal experiences as predicted by brain activity. Science 281, 1188–1191 (1998).
Billingsley, R.L., Lou Smith, M. & Pat McAndrews, M. Developmental patterns in priming and familiarity in explicit recollection. J. Exp. Child Psychol. 82, 251–277 (2002).
Cycowicz, Y.M., Friedman, D., Snodgrass, J.G. & Duff, M. Recognition and source memory for pictures in children and adults. Neuropsychologia 39, 255–267 (2001).
Dirks, J. & Neisser, U. Memory for objects in real scenes: the development of recognition and recall. J. Exp. Child Psychol. 23, 315–328 (1977).
Mandler, J.M. & Robinson, C.A. Developmental changes in picture recognition. J. Exp. Child Psychol. 26, 122–136 (1978).
Drummey, A.B. & Newcombe, N.S. Developmental changes in source memory. Dev. Sci. 5, 502–513 (2002).
Cycowicz, Y.M., Friedman, D. & Duff, M. Pictures and their colors: what do children remember? J. Cogn. Neurosci. 15, 759–768 (2003).
Czernochowski, D., Mecklinger, A., Johansson, M. & Brinkmann, M. Age-related differences in familiarity and recollection: ERP evidence from a recognition memory study in children and young adults. Cogn. Affect. Behav. Neurosci. 5, 417–433 (2005).
Huttenlocher, P.R. Synaptic density in human frontal cortex - developmental changes and effects of aging. Brain Res. 163, 195–205 (1979).
Sowell, E.R. et al. Longitudinal mapping of cortical thickness and brain growth in normal children. J. Neurosci. 24, 8223–8231 (2004).
Giedd, J.N. et al. Brain development during childhood and adolescence: a longitudinal MRI study. Nat. Neurosci. 2, 861–863 (1999).
Gogtay, N. et al. Dynamic mapping of human cortical development during childhood through early adulthood. Proc. Natl. Acad. Sci. USA 101, 8174–8179 (2004).
Sowell, E.R., Trauner, D.A., Gamst, A. & Jernigan, T.L. Development of cortical and subcortical brain structures in childhood and adolescence: a structural MRI study. Dev. Med. Child Neurol. 44, 4–16 (2002).
Gogtay, N. et al. Dynamic mapping of normal human hippocampal development. Hippocampus 16, 664–672 (2006).
Sowell, E.R. & Jernigan, T.L. Further MRI evidence of late brain maturation: limbic volume increases and changing asymmetries during childhood and adolescence. Dev. Neuropsychol. 14, 599–617 (1998).
Giedd, J.N. et al. Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: ages 4–18 years. J. Comp. Neurol. 366, 223–230 (1996).
Menon, V., Boyett-Anderson, J.M. & Reiss, A.L. Maturation of medial temporal lobe response and connectivity during memory encoding. Brain Res. Cogn. Brain Res. 25, 379–385 (2005).
Chiu, C.Y.P., Schmithorst, V.J., Brown, R.D., Holland, S.K. & Dunn, S. Making memories: a crosssectional investigation of episodic memory encoding in childhood using fMRI. Dev. Neuropsychol. 29, 321–340 (2006).
Ranganath, C. et al. Dissociable correlates of recollection and familiarity within the medial temporal lobes. Neuropsychologia 42, 2–13 (2004).
Wig, G.S., Miller, M.B., Kingstone, A. & Kelley, W.M. Separable routes to human memory formation: dissociating task and material contributions in the prefrontal cortex. J. Cogn. Neurosci. 16, 139–148 (2004).
Casey, B.J., Galvan, A. & Hare, T.A. Changes in cerebral functional organization during cognitive development. Curr. Opin. Neurobiol. 15, 239–244 (2005).
Schlaggar, B.L. et al. Functional neuroanatomical differences between adults and school-age children in the processing of single words. Science 296, 1476–1479 (2002).
Brown, T.T. et al. Developmental changes in human cerebral functional organization for word generation. Cereb. Cortex 15, 275–290 (2005).
Wilke, M., Schmithorst, V.J. & Holland, S.K. Normative pediatric brain data for spatial normalization and segmentation differs from standard adult data. Magn. Reson. Med. 50, 749–757 (2003).
Burgund, E.D. et al. The feasibility of a common stereotactic space for children and adults in fMRI studies of development. Neuroimage 17, 184–200 (2002).
Davis, T.L., Kwong, K.K., Weisskoff, R.M. & Rosen, B.R. Calibrated functional MRI: mapping the dynamics of oxidative metabolism. Proc. Natl. Acad. Sci. USA 95, 1834–1839 (1998).
Aguirre, G.K., Zarahn, E. & D'Esposito, M. The variability of human, BOLD hemodynamic responses. Neuroimage 8, 360–369 (1998).
Miezin, F.M., Maccotta, L., Ollinger, J.M., Petersen, S.E. & Buckner, R.L. Characterizing the hemodynamic response: effects of presentation rate, sampling procedure and the possibility of ordering brain activity based on relative timing. Neuroimage 11, 735–759 (2000).
D'Esposito, M., Deouell, L.Y. & Gazzaley, A. Alterations in the BOLD fMRI signal with ageing and disease: a challenge for neuroimaging. Nat. Rev. Neurosci. 4, 863–872 (2003).
Buckner, R.L., Snyder, A.Z., Sanders, A.L., Raichle, M.E. & Morris, J.C. Functional brain imaging of young, nondemented and demented older adults. J. Cogn. Neurosci. 12, 24–34 (2000).
Kang, H.C., Burgund, E.D., Lugar, H.M., Petersen, S.E. & Schlaggar, B.L. Comparison of functional activation foci in children and adults using a common stereotactic space. Neuroimage 19, 16–28 (2003).
Shaw, P. et al. Intellectual ability and cortical development in children and adolescents. Nature 440, 676–679 (2006).
Durston, S. et al. A shift from diffuse to focal cortical activity with development. Dev. Sci. 9, 1–8 (2006).
Knowlton, B.J. & Squire, L.R. Remembering and knowing: two different expressions of declarative memory. J. Exp. Psychol. Learn. Mem. Cogn. 21, 699–710 (1995).
Sowell, E.R., Delis, D., Stiles, J. & Jernigan, T.L. Improved memory functioning and frontal lobe maturation between childhood and adolescence: a structural MRI study. J. Int. Neuropsychol. Soc. 7, 312–322 (2001).
Bunge, S.A., Dudukovic, N.M., Thomason, M.E., Vaidya, C.J. & Gabrieli, J.D.E. Immature frontal lobe contributions to cognitive control in children: evidence from fMRI. Neuron 33, 301–311 (2002).
Goswami, U. Neuroscience and education: from research to practice? Nat. Rev. Neurosci. 7, 406–413 (2006).
Yonelinas, A.P. & Jacoby, L.L. Dissociating automatic and controlled processes in a memory-search task: beyond implicit memory. Psychol. Res. 57, 156–165 (1995).
Glover, G.H. & Law, C.S. Spiral-in/out BOLD fMRI for increased SNR and reduced susceptibility artifacts. Magn. Reson. Med. 46, 515–522 (2001).
Good, C.D. et al. A voxel-based morphometric study of ageing in 465 normal adult human brains. Neuroimage 14, 21–36 (2001).
Ashburner, J. & Friston, K.J. Voxel-based morphometry—the methods. Neuroimage 11, 805–821 (2000).
Snodgrass, J.G. & Vanderwart, M. A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity and visual complexity. J. Exp. Psychol. [Hum Learn] 6, 174–215 (1980).
Acknowledgements
We thank N. Gaab, T. Hedden, D. Palti and S. Corkin for helpful discussions, J. Motsinger and N. Rubinstein for help with data collection and analysis, and three anonymous reviewers for helpful comments on earlier versions of the manuscript. This work was supported by the US National Institute of Mental Health (J.D.E.G).
Author information
Authors and Affiliations
Contributions
N.O., Y.-C.K. and J.D.E.G. designed the experiments. N.O., Y.-C.K., P.S.-H., H.K. and S.W.-G. collected and analyzed the data. N.O., S.W.-G. and J.D.E.G. wrote the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing financial interests.
Supplementary information
Supplementary Text and Figures
Supplementary Table 1 (PDF 88 kb)
Rights and permissions
About this article
Cite this article
Ofen, N., Kao, YC., Sokol-Hessner, P. et al. Development of the declarative memory system in the human brain. Nat Neurosci 10, 1198–1205 (2007). https://doi.org/10.1038/nn1950
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1038/nn1950
This article is cited by
-
Goal-directed learning in adolescence: neurocognitive development and contextual influences
Nature Reviews Neuroscience (2024)
-
Cognitive mechanisms underlying free recall in episodic memory performance across the lifespan: testing the control/representation model
Psychological Research (2023)
-
Children’s altruism after recalling recent and distant morally-valenced behavior and the mediating role of guilt
Current Psychology (2023)
-
Verbal learning impairment in adolescents with methamphetamine use disorder: a cross-sectional study
BMC Psychiatry (2021)
-
Developmental differences in memory reactivation relate to encoding and inference in the human brain
Nature Human Behaviour (2021)