Regional Hippocampal Volumes and Development Predict Learning and Memory

The hippocampus is an anatomically and functionally heterogeneous structure, but longitudinal studies of its regional development are scarce and it is not known whether protracted maturation of the hippocampus in adolescence is related to memory development. First, we investigated hippocampal subfield development using 170 longitudinally acquired brain magnetic resonance imaging scans from 85 participants aged 8-21 years. Hippocampal subfield volumes were estimated by the use of automated segmentation of 7 subfields, including the cornu ammonis (CA) sectors and the dentate gyrus (DG), while longitudinal subfield volumetric change was quantified using a nonlinear registration procedure. Second, associations between subfield volumes and change and verbal learning/memory across multiple retention intervals (5 min, 30 min and 1 week) were tested. It was hypothesized that short and intermediate memory would be more closely related to CA2-3/CA4-DG and extended, remote memory to CA1. Change rates were significantly different across hippocampal subfields, but nearly all subfields showed significant volume decreases over time throughout adolescence. Several subfield volumes were larger in the right hemisphere and in males, while for change rates there were no hemisphere or sex differences. Partly in support of the hypotheses, greater volume of CA1 and CA2-3 was related to recall and retention after an extended delay, while longitudinal reduction of CA2-3 and CA4-DG was related to learning. This suggests continued regional development of the hippocampus across adolescence and that volume and volume change in specific subfields differentially predict verbal learning and memory over different retention intervals, but future high-resolution studies are called for.

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

[2]  Anders M. Dale,et al.  Longitudinal Working Memory Development Is Related to Structural Maturation of Frontal and Parietal Cortices , 2013, Journal of Cognitive Neuroscience.

[3]  Eleanor A Maguire,et al.  Representations of recent and remote autobiographical memories in hippocampal subfields , 2013, Hippocampus.

[4]  A M Dale,et al.  Measuring the thickness of the human cerebral cortex from magnetic resonance images. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[5]  A. Dale,et al.  Age does not increase rate of forgetting over weeks—Neuroanatomical volumes and visual memory across the adult life-span , 2005, Journal of the International Neuropsychological Society.

[6]  Deanna Greenstein,et al.  Hippocampal volume development in healthy siblings of childhood-onset schizophrenia patients. , 2011, The American journal of psychiatry.

[7]  Kiralee M. Hayashi,et al.  Dynamic mapping of normal human hippocampal development , 2006, Hippocampus.

[8]  J. Rapoport,et al.  Structural MRI of Pediatric Brain Development: What Have We Learned and Where Are We Going? , 2010, Neuron.

[9]  F. Gage,et al.  Neurogenesis in the adult human hippocampus , 1998, Nature Medicine.

[10]  Yaakov Stern,et al.  Hippocampal subregions differentially associate with standardized memory tests , 2010, Hippocampus.

[11]  A. Dale,et al.  Unbiased comparison of sample size estimates from longitudinal structural measures in ADNI , 2012, Human brain mapping.

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

[13]  L. Tugan Muftuler,et al.  Cortical and subcortical changes in typically developing preadolescent children , 2011, Brain Research.

[14]  Torsten Rohlfing,et al.  Developmental change in regional brain structure over 7 months in early adolescence: Comparison of approaches for longitudinal atlas-based parcellation , 2011, NeuroImage.

[15]  Silvia A. Bunge,et al.  Developmental Cognitive Neuroscience Neural changes underlying the development of episodic memory during middle childhood , 2022 .

[16]  Alan C. Evans,et al.  A nonparametric method for automatic correction of intensity nonuniformity in MRI data , 1998, IEEE Transactions on Medical Imaging.

[17]  Anders M. Dale,et al.  Sequence-independent segmentation of magnetic resonance images , 2004, NeuroImage.

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

[19]  F. Gage,et al.  Mechanisms and Functional Implications of Adult Neurogenesis , 2008, Cell.

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

[21]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[22]  Anders M. Dale,et al.  When does brain aging accelerate? Dangers of quadratic fits in cross-sectional studies , 2010, NeuroImage.

[23]  Yasuhiro Kawasaki,et al.  Male-specific volume expansion of the human hippocampus during adolescence. , 2004, Cerebral cortex.

[24]  András Vincze,et al.  Myelination in the human hippocampal formation from midgestation to adulthood , 2010, International Journal of Developmental Neuroscience.

[25]  Hisao Nishijo,et al.  Developmental Trajectories of Amygdala and Hippocampus from Infancy to Early Adulthood in Healthy Individuals , 2012, PloS one.

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

[27]  M. Moser,et al.  Functional differentiation in the hippocampus , 1998, Hippocampus.

[28]  Susan L. Andersen,et al.  Developmental trajectories during adolescence in males and females: A cross-species understanding of underlying brain changes , 2011, Neuroscience & Biobehavioral Reviews.

[29]  Susanna Sallstroem,et al.  Functional Differentiation , 2009, Modern Condensed Matter Physics.

[30]  Polina Golland,et al.  Automated segmentation of hippocampal subfields from ultra‐high resolution in vivo MRI , 2009, Hippocampus.

[31]  Indira Tendolkar,et al.  Amygdala and hippocampus enlargement during adolescence in autism. , 2010, Journal of the American Academy of Child and Adolescent Psychiatry.

[32]  Sebastien Ourselin,et al.  Cerebral atrophy in mild cognitive impairment and Alzheimer disease , 2013, Neurology.

[33]  Anders M. Dale,et al.  Reliability in multi-site structural MRI studies: Effects of gradient non-linearity correction on phantom and human data , 2006, NeuroImage.

[34]  George Richardson,et al.  Brain development and aging: Overlapping and unique patterns of change , 2013, NeuroImage.

[35]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[36]  Craig E. L. Stark,et al.  High-resolution structural and functional MRI of hippocampal CA3 and dentate gyrus in patients with amnestic Mild Cognitive Impairment , 2010, NeuroImage.

[37]  Deborah A Yurgelun-Todd,et al.  Cognitive Correlates of Medial Temporal Lobe Development across Adolescence: A Magnetic Resonance Imaging Study , 2003, Perceptual and motor skills.

[38]  S. Ghetti,et al.  Developmental differences in hippocampal and cortical contributions to episodic retrieval , 2013, Cortex.

[39]  P. Rutecki,et al.  Brain structure and aging in chronic temporal lobe epilepsy , 2012, Epilepsia.

[40]  Morris Moscovitch,et al.  A Hippocampal Marker of Recollection Memory Ability among Healthy Young Adults: Contributions of Posterior and Anterior Segments , 2011, Neuron.

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

[42]  C. Lebel,et al.  Longitudinal Development of Human Brain Wiring Continues from Childhood into Adulthood , 2011, The Journal of Neuroscience.

[43]  Ricardo Insausti,et al.  Postnatal development of the human hippocampal formation. , 2009, Advances in anatomy, embryology, and cell biology.

[44]  N. Burgess,et al.  The hippocampus and memory: insights from spatial processing , 2008, Nature Reviews Neuroscience.

[45]  J. Rapoport,et al.  Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: Ages 4–18 years , 1995, The Journal of comparative neurology.

[46]  Michael Weiner,et al.  Nearly automatic segmentation of hippocampal subfields in in vivo focal T2-weighted MRI , 2010, NeuroImage.

[47]  L. Westlye,et al.  Brain maturation in adolescence and young adulthood: regional age-related changes in cortical thickness and white matter volume and microstructure. , 2010, Cerebral cortex.

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

[49]  Michael Weiner,et al.  Evidence for functional specialization of hippocampal subfields detected by MR subfield volumetry on high resolution images at 4T , 2011, NeuroImage.

[50]  Richard S. J. Frackowiak,et al.  Navigation-related structural change in the hippocampi of taxi drivers. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Simona Ghetti,et al.  Development of memory for spatial context: Hippocampal and cortical contributions , 2013, Neuropsychologia.

[52]  E. Maguire,et al.  London taxi drivers and bus drivers: A structural MRI and neuropsychological analysis , 2006, Hippocampus.

[53]  Hallvard Røe Evensmoen,et al.  Long-axis specialization of the human hippocampus , 2013, Trends in Cognitive Sciences.

[54]  Alan C. Evans,et al.  Total and regional brain volumes in a population-based normative sample from 4 to 18 years: the NIH MRI Study of Normal Brain Development. , 2012, Cerebral cortex.

[55]  Paul M. Thompson,et al.  Sexual dimorphism of brain developmental trajectories during childhood and adolescence , 2007, NeuroImage.

[56]  Mieke Verfaellie,et al.  Distinct hippocampal regions make unique contributions to relational memory , 2009, Hippocampus.

[57]  M. Styner,et al.  Longitudinal development of cortical and subcortical gray matter from birth to 2 years. , 2012, Cerebral cortex.

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

[59]  Hong-wei Dong,et al.  Are the Dorsal and Ventral Hippocampus Functionally Distinct Structures? , 2010, Neuron.

[60]  Anders M. Fjell,et al.  Heterogeneity in Subcortical Brain Development: A Structural Magnetic Resonance Imaging Study of Brain Maturation from 8 to 30 Years , 2009, The Journal of Neuroscience.

[61]  Andreas Engvig,et al.  Hippocampal subfield volumes correlate with memory training benefit in subjective memory impairment , 2012, NeuroImage.

[62]  G. Doerner Sexual dimorphism of the brain , 1979 .

[63]  D. Louis Collins,et al.  Volumetric analysis of medial temporal lobe structures in brain development from childhood to adolescence , 2013, NeuroImage.

[64]  Koenraad Van Leemput,et al.  Model-Based Segmentation of Hippocampal Subfields in Ultra-High Resolution In Vivo MRI , 2008, MICCAI.

[65]  E. Crone,et al.  Sex differences and structural brain maturation from childhood to early adulthood , 2013, Developmental Cognitive Neuroscience.

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

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

[68]  Arne D. Ekstrom,et al.  Advances in high-resolution imaging and computational unfolding of the human hippocampus , 2009, NeuroImage.

[69]  F. Benes,et al.  Myelination of cortical-hippocampal relays during late adolescence. , 1989, Schizophrenia bulletin.

[70]  Menno P. Witter,et al.  A pathophysiological framework of hippocampal dysfunction in ageing and disease , 2011, Nature Reviews Neuroscience.

[71]  Brian B. Avants,et al.  Histology-derived volumetric annotation of the human hippocampal subfields in postmortem MRI , 2014, NeuroImage.

[72]  M. Yücel,et al.  Mapping subcortical brain maturation during adolescence: evidence of hemisphere- and sex-specific longitudinal changes. , 2013, Developmental science.

[73]  P. Seres,et al.  High field structural MRI reveals specific episodic memory correlates in the subfields of the hippocampus , 2014, Neuropsychologia.

[74]  Torbjørn Elvsåshagen,et al.  Evidence for reduced dentate gyrus and fimbria volume in bipolar II disorder , 2013, Bipolar disorders.

[75]  X Seron,et al.  Mild cognitive impairment: Differential atrophy in the hippocampal subfields , 2011, Alzheimer's & Dementia.

[76]  F. Benes,et al.  Myelination of a key relay zone in the hippocampal formation occurs in the human brain during childhood, adolescence, and adulthood. , 1994, Archives of general psychiatry.

[77]  Raymond P. Kesner,et al.  The temporal attributes of episodic memory , 2010, Behavioural Brain Research.

[78]  D. Bowers,et al.  Asymmetry of the hippocampus and amygdala in MRI volumetric measurements of normal adults , 2004, Journal of the International Neuropsychological Society.

[79]  Anders M. Dale,et al.  Nonlinear registration of longitudinal images and measurement of change in regions of interest , 2011, Medical Image Anal..

[80]  Ylva Østby,et al.  Dissociating memory processes in the developing brain: the role of hippocampal volume and cortical thickness in recall after minutes versus days. , 2012, Cerebral cortex.

[81]  G. Ming,et al.  Adult Neurogenesis in the Mammalian Brain: Significant Answers and Significant Questions , 2011, Neuron.