Hippocampal maturity promotes memory distinctiveness in childhood and adolescence

Significance Children tend to extract schematic knowledge at the expense of learning and recollecting specific events. Our findings allow us to speculate that the heterogeneous development of subregions within the hippocampus—a brain region crucial for laying down novel memories—contributes to this developmental lag in memory. Specifically, we used in vivo high-resolution structural MRI and memory tests in a large sample of children aged 6–14 years and young adults to characterize hippocampal development. We show that hippocampal maturity as expressed in the multivariate pattern of age-related differences in hippocampal subregions is specifically related to the ability to lay down highly specific memories. Adaptive learning systems need to meet two complementary and partially conflicting goals: detecting regularities in the world versus remembering specific events. The hippocampus (HC) keeps a fine balance between computations that extract commonalities of incoming information (i.e., pattern completion) and computations that enable encoding of highly similar events into unique representations (i.e., pattern separation). Histological evidence from young rhesus monkeys suggests that HC development is characterized by the differential development of intrahippocampal subfields and associated networks. However, due to challenges in the in vivo investigation of such developmental organization, the ontogenetic timing of HC subfield maturation remains controversial. Delineating its course is important, as it directly influences the fine balance between pattern separation and pattern completion operations and, thus, developmental changes in learning and memory. Here, we relate in vivo, high-resolution structural magnetic resonance imaging data of HC subfields to behavioral memory performance in children aged 6–14 y and in young adults. We identify a multivariate profile of age-related differences in intrahippocampal structures and show that HC maturity as captured by this pattern is associated with age differences in the differential encoding of unique memory representations.

[1]  M. Moser,et al.  Stellate cells drive maturation of the entorhinal-hippocampal circuit , 2017, Science.

[2]  Valerie A. Carr,et al.  A harmonized segmentation protocol for hippocampal and parahippocampal subregions: Why do we need one and what are the key goals? , 2017, Hippocampus.

[3]  Nicholas B. Turk-Browne,et al.  Hippocampal Structure Predicts Statistical Learning and Associative Inference Abilities during Development , 2017, Journal of Cognitive Neuroscience.

[4]  Hauke R. Heekeren,et al.  Neural activation patterns of successful episodic encoding: Reorganization during childhood, maintenance in old age , 2016, Developmental Cognitive Neuroscience.

[5]  Andrew R. Bender,et al.  Changes in Search Path Complexity and Length During Learning of a Virtual Water Maze: Age Differences and Differential Associations with Hippocampal Subfield Volumes. , 2016, Cerebral cortex.

[6]  A. Morcom,et al.  Cortical pattern separation and item-specific memory encoding , 2016, Neuropsychologia.

[7]  Andrew R. Bender,et al.  Age differences in hippocampal subfield volumes from childhood to late adulthood , 2016, Hippocampus.

[8]  Carter Wendelken,et al.  Age- and performance-related differences in hippocampal contributions to episodic retrieval , 2016, Developmental Cognitive Neuroscience.

[9]  Carter Wendelken,et al.  A Time and Place for Everything: Developmental Differences in the Building Blocks of Episodic Memory. , 2016, Child development.

[10]  Simon Hanslmayr,et al.  Human Hippocampal Dynamics during Response Conflict , 2015, Current Biology.

[11]  Margaret L. Schlichting,et al.  Learning-related representational changes reveal dissociable integration and separation signatures in the hippocampus and prefrontal cortex , 2015, Nature Communications.

[12]  M. Mallar Chakravarty,et al.  Quantitative comparison of 21 protocols for labeling hippocampal subfields and parahippocampal subregions in in vivo MRI: Towards a harmonized segmentation protocol , 2015, NeuroImage.

[13]  Simona Ghetti,et al.  Structural development of the hippocampus and episodic memory: developmental differences along the anterior/posterior axis. , 2014, Cerebral cortex.

[14]  Craig E. L. Stark,et al.  Loss of pattern separation performance in schizophrenia suggests dentate gyrus dysfunction , 2014, Schizophrenia Research.

[15]  Zachariah M. Reagh,et al.  Object and spatial mnemonic interference differentially engage lateral and medial entorhinal cortex in humans , 2014, Proceedings of the National Academy of Sciences.

[16]  Arne D. Ekstrom,et al.  Volume of hippocampal subfields and episodic memory in childhood and adolescence , 2014, NeuroImage.

[17]  Pierre Lavenex,et al.  Building hippocampal circuits to learn and remember: Insights into the development of human memory , 2013, Behavioural Brain Research.

[18]  Shauna M. Stark,et al.  A task to assess behavioral pattern separation (BPS) in humans: Data from healthy aging and mild cognitive impairment , 2013, Neuropsychologia.

[19]  Ana M. Daugherty,et al.  Vascular Risk Moderates Associations between Hippocampal Subfield Volumes and Memory , 2013, Journal of Cognitive Neuroscience.

[20]  Vijay K. Venkatraman,et al.  Neuroanatomical Assessment of Biological Maturity , 2012, Current Biology.

[21]  John D E Gabrieli,et al.  The Development of Brain Systems Associated with Successful Memory Retrieval of Scenes , 2012, The Journal of Neuroscience.

[22]  James L. McClelland,et al.  Generalization Through the Recurrent Interaction of Episodic Memories , 2012, Psychological review.

[23]  S. Ghetti,et al.  The Development of Episodic Memory: Binding Processes, Controlled Processes, and Introspection on Memory States , 2012 .

[24]  Simona Ghetti,et al.  Origins and development of recollection : perspectives from psychology and neuroscience , 2012 .

[25]  T. Riggins Building blocks of recollection , 2012 .

[26]  C. Stark,et al.  Pattern separation in the hippocampus , 2011, Trends in Neurosciences.

[27]  U. Lindenberger,et al.  Only time will tell: cross-sectional studies offer no solution to the age-brain-cognition triangle: comment on Salthouse (2011). , 2011, Psychological bulletin.

[28]  L. Squire,et al.  The cognitive neuroscience of human memory since H.M. , 2011, Annual review of neuroscience.

[29]  Anthony Randal McIntosh,et al.  Partial Least Squares (PLS) methods for neuroimaging: A tutorial and review , 2011, NeuroImage.

[30]  U. Lindenberger,et al.  Cross-sectional age variance extraction: what's change got to do with it? , 2011, Psychology and aging.

[31]  Yee Lee Shing,et al.  Aging Neuroscience , 2022 .

[32]  Shauna M. Stark,et al.  Distinct pattern separation related transfer functions in human CA3/dentate and CA1 revealed using high-resolution fMRI and variable mnemonic similarity. , 2010, Learning & memory.

[33]  Shauna M. Stark,et al.  Pattern separation deficits associated with increased hippocampal CA3 and dentate gyrus activity in nondemented older adults , 2010, Hippocampus.

[34]  Valerie A. Carr,et al.  Neural Activity in the Hippocampus and Perirhinal Cortex during Encoding Is Associated with the Durability of Episodic Memory , 2010, Journal of Cognitive Neuroscience.

[35]  Timothy F. Brady,et al.  Conceptual Distinctiveness Supports Detailed Visual Long-term Memory for Real-world Objects the Fidelity of Long-term Memory for Visual Information , 2022 .

[36]  Dana M. DeMaster,et al.  Developmental Differences in Medial Temporal Lobe Function during Memory Encoding , 2010, The Journal of Neuroscience.

[37]  Yee Lee Shing,et al.  Episodic memory across the lifespan: The contributions of associative and strategic components , 2010, Neuroscience & Biobehavioral Reviews.

[38]  David Friedman,et al.  Changes in familiarity and recollection across the lifespan: An ERP perspective , 2010, Brain Research.

[39]  Marcia K. Johnson,et al.  Source monitoring 15 years later: what have we learned from fMRI about the neural mechanisms of source memory? , 2009, Psychological bulletin.

[40]  C. Grady,et al.  Event-related fMRI studies of episodic encoding and retrieval: Meta-analyses using activation likelihood estimation , 2009, Neuropsychologia.

[41]  Yee Lee Shing,et al.  Adult age differences in memory for name–face associations: The effects of intentional and incidental learning , 2009, Memory.

[42]  Moser Edvard,et al.  Pattern Separation in the Dentate Gyrus , 2009 .

[43]  Norbert Schuff,et al.  Selective effect of Apo e4 on CA3 and dentate in normal aging and Alzheimer's disease using high resolution MRI at 4 T , 2008, NeuroImage.

[44]  Arthur W. Toga,et al.  Construction of a 3D probabilistic atlas of human cortical structures , 2008, NeuroImage.

[45]  John D E Gabrieli,et al.  Development of the declarative memory system in the human brain , 2007, Nature Neuroscience.

[46]  N. Schuff,et al.  Measurement of hippocampal subfields and age-related changes with high resolution MRI at 4T , 2007, Neurobiology of Aging.

[47]  S. Maxwell,et al.  Bias in cross-sectional analyses of longitudinal mediation. , 2007, Psychological methods.

[48]  M. Frotscher The Human Hippocampus, third ed., Henri M. Duvernoy (Ed.). Springer, Berlin, Heidelberg, New York (2005), (271 figures, 47 tables, VIII, 232pp., Hardcover, EURO169,95; SFR 287.50; GBP 130,50; US$ 199.00), ISBN: 3-540-23191-9 , 2005 .

[49]  Cheryl L. Dahle,et al.  Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. , 2005, Cerebral cortex.

[50]  B. Knowlton,et al.  A Dissociation of Encoding and Retrieval Processes in the Human Hippocampus , 2005, The Journal of Neuroscience.

[51]  Martin Lepage,et al.  Dorsolateral prefrontal cortex involvement in memory post-retrieval monitoring revealed in both item and associative recognition tests , 2005, NeuroImage.

[52]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[53]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[54]  Henri M. Duvernoy,et al.  The Human Hippocampus , 1998, Springer Berlin Heidelberg.

[55]  E. Tulving,et al.  Episodic and declarative memory: Role of the hippocampus , 1998, Hippocampus.

[56]  L. Squire,et al.  Episodic memory, semantic memory, and amnesia , 1998, Hippocampus.

[57]  J. V. Haxby,et al.  Spatial Pattern Analysis of Functional Brain Images Using Partial Least Squares , 1996, NeuroImage.

[58]  James L. McClelland,et al.  Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. , 1995, Psychological review.

[59]  V. Reyna,et al.  Fuzzy-trace theory: An interim synthesis , 1995 .

[60]  Xiao-Li Meng,et al.  Comparing correlated correlation coefficients , 1992 .

[61]  C. Jack,et al.  Anterior temporal lobes and hippocampal formations: normative volumetric measurements from MR images in young adults. , 1989, Radiology.

[62]  Michael Chapman,et al.  Constructive Evolution: Origins and Development of Piaget's Thought , 1988 .

[63]  Jean Piaget,et al.  Epistemology and Psychology of Functions , 1977 .

[64]  John R. Nesselroade,et al.  The developmental analysis of individual differences on multiple measures. , 1973 .