Subfields of the hippocampal formation at 7T MRI: In vivo volumetric assessment

Animal and human autopsy studies suggest that subfields of the hippocampal formation are differentially affected by neuropsychiatric diseases. Therefore, subfield volumes may be more sensitive to effects of disease processes. The few human studies that segmented subfields of the hippocampal formation in vivo either assessed the subfields only in the body of the hippocampus, assessed only three subfields, or did not take the differential angulation of the head of the hippocampus into account. We developed a protocol using 7 Tesla MRI with isotropic voxels to reliably delineate the entorhinal cortex (ERC), subiculum (SUB), CA1, CA2, CA3, dentate gyrus (DG)&CA4 along the full-length of the hippocampus. Fourteen subjects (aged 54-74 years, 2 men and 12 women) were scanned with a 3D turbo spin echo (TSE) sequence with isotropic voxels of 0.7 × 0.7 × 0.7 mm(3) on a 7 T MRI whole body scanner. Based on previous protocols and extensive anatomic atlases, a new protocol for segmentation of subfields of the hippocampal formation was formulated. ERC, SUB, CA1, CA2, CA3 and DG&CA4 were manually segmented twice by one rater from coronal MR images. Good-to-excellent consistency was found for all subfields (Intraclass Correlation Coefficient's (ICC) varying from 0.74 to 0.98). Accuracy as measured with the Dice Similarity Index (DSI) was above 0.82 for all subfields, with the exception of the smaller subfield CA3 (0.68-0.70). In conclusion, this study shows that it is possible to delineate the main subfields of the hippocampal formation along its full-length in vivo at 7 T MRI. Our data give evidence that this can be done in a reliable manner. Segmentation of subfields in the full-length of the hippocampus may bolster the study of the etiology neuropsychiatric diseases.

[1]  Brian B. Avants,et al.  A high-resolution computational atlas of the human hippocampus from postmortem magnetic resonance imaging at 9.4 T , 2009, NeuroImage.

[2]  K. Amunts,et al.  Cytoarchitectonic mapping of the human amygdala, hippocampal region and entorhinal cortex: intersubject variability and probability maps , 2005, Anatomy and Embryology.

[3]  Paul M. Thompson,et al.  In vivo neuropathology of the hippocampal formation in AD: A radial mapping MR-based study , 2006, NeuroImage.

[4]  J. Bremner,et al.  MR-based in vivo hippocampal volumetrics: 1. Review of methodologies currently employed , 2005, Molecular Psychiatry.

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

[6]  Emma R. Wood,et al.  The role of hippocampal subregions in memory for stimulus associations , 2010, Behavioural Brain Research.

[7]  N. Sousa,et al.  Ligand and subfield specificity of corticoid-induced neuronal loss in the rat hippocampal formation , 1999, Neuroscience.

[8]  C. Jack,et al.  MRI‐Based Hippocampal Volume Measurements in Epilepsy , 1994, Epilepsia.

[9]  H. Soininen,et al.  MR volumetric analysis of the human entorhinal, perirhinal, and temporopolar cortices. , 1998, AJNR. American journal of neuroradiology.

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

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

[12]  Michael W. L. Chee,et al.  Hippocampal region-specific contributions to memory performance in normal elderly , 2010, Brain and Cognition.

[13]  R. Marc Lebel,et al.  In vivo quantification of hippocampal subfields using 4.7 T fast spin echo imaging , 2010, NeuroImage.

[14]  H. Duvernoy,et al.  The Human Hippocampus: Functional Anatomy, Vascularization and Serial Sections with MRI , 1997 .

[15]  C. Jack,et al.  Medial temporal atrophy on MRI in normal aging and very mild Alzheimer's disease , 1997, Neurology.

[16]  D. Bowers,et al.  Entorhinal cortex volume in older adults: Reliability and validity considerations for three published measurement protocols , 2010, Journal of the International Neuropsychological Society.

[17]  Irwin Nazareth,et al.  The natural course and outcome of major depressive disorder in primary care: the PREDICT-NL study , 2010, Social Psychiatry and Psychiatric Epidemiology.

[18]  R. Busse,et al.  Fast spin echo sequences with very long echo trains: Design of variable refocusing flip angle schedules and generation of clinical T2 contrast , 2006, Magnetic resonance in medicine.

[19]  Pierre Lavenex,et al.  Postmortem changes in the neuroanatomical characteristics of the primate brain: Hippocampal formation , 2009, The Journal of comparative neurology.

[20]  Charles D. Smith,et al.  Evidence that volume of anterior medial temporal lobe is reduced in seniors destined for mild cognitive impairment , 2010, Neurobiology of Aging.

[21]  Carlo Caltagirone,et al.  Hippocampal Volume Reduction in First-Episode and Chronic Schizophrenia , 2012, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[22]  Patrick Royston,et al.  Development and validation of an international risk prediction algorithm for episodes of major depression in general practice attendees: the PredictD study. , 2008, Archives of general psychiatry.

[23]  F Andermann,et al.  Anatomic basis of amygdaloid and hippocampal volume measurement by magnetic resonance imaging , 1992, Neurology.

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

[25]  B. Dickerson,et al.  MRI of human entorhinal cortex: a reliable protocol for volumetric measurement , 2001, Neurobiology of Aging.

[26]  Nick C. Fox,et al.  Improved reliability of hippocampal atrophy rate measurement in mild cognitive impairment using fluid registration , 2007, NeuroImage.

[27]  C R Jack,et al.  Volumetric magnetic resonance imaging. Clinical applications and contributions to the understanding of temporal lobe epilepsy. , 1997, Archives of neurology.

[28]  N. Schuff,et al.  Hippocampal atrophy patterns in mild cognitive impairment and Alzheimer's disease , 2010, Human brain mapping.

[29]  Lotte Gerritsen,et al.  Basal Hypothalamic Pituitary Adrenal Axis Activity and Hippocampal Volumes: The SMART-Medea Study , 2010, Biological Psychiatry.

[30]  Hannie C. Comijs,et al.  Depression, Hypothalamic Pituitary Adrenal Axis, and Hippocampal and Entorhinal Cortex Volumes—The SMART Medea Study , 2011, Biological Psychiatry.

[31]  A. Nappi,et al.  Alzheimer ' s Disease : Cell-Specific Pathology Isolates the Hippocampal Formation , 2022 .

[32]  R. Sapolsky,et al.  Glucocorticoids and hippocampal atrophy in neuropsychiatric disorders. , 2000, Archives of general psychiatry.

[33]  Olivier Colliot,et al.  Three-dimensional Segmentation of the Internal Structures of the Human Hippocampus at 7 Tesla , 2009 .

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

[35]  Truman R Brown,et al.  Linking hippocampal structure and function to memory performance in an aging population. , 2009, Archives of neurology.

[36]  Nick C. Fox,et al.  A meta-analysis of hippocampal atrophy rates in Alzheimer's disease , 2009, Neurobiology of Aging.

[37]  G. V. Van Hoesen,et al.  Alzheimer's disease: cell-specific pathology isolates the hippocampal formation. , 1984, Science.

[38]  J. Bohl,et al.  Stage-dependent and sector-specific neuronal loss in hippocampus during Alzheimer's disease , 2002, Acta Neuropathologica.

[39]  H. Soininen,et al.  Comparative MR analysis of the entorhinal cortex and hippocampus in diagnosing Alzheimer disease. , 1999, AJNR. American journal of neuroradiology.

[40]  P. Brambilla,et al.  Stress and hippocampal abnormalities in psychiatric disorders , 2004, European Neuropsychopharmacology.

[41]  Nigel J. Cairns,et al.  Neurons, intracellular and extracellular neurofibrillary tangles in subdivisions of the hippocampal cortex in normal ageing and Alzheimer's disease , 1995, Neuroscience Letters.

[42]  A. Convit,et al.  Specific Hippocampal Volume Reductions in Individuals at Risk for Alzheimer’s Disease , 1997, Neurobiology of Aging.

[43]  G. Kerchner,et al.  Hippocampal CA1 apical neuropil atrophy in mild Alzheimer disease visualized with 7-T MRI , 2010, Neurology.

[44]  G. Paxinos,et al.  Atlas of the Human Brain , 2000 .