{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2024,11,19]],"date-time":"2024-11-19T18:59:39Z","timestamp":1732042779791},"reference-count":64,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,6,15]],"date-time":"2023-06-15T00:00:00Z","timestamp":1686787200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100004431","name":"Fondation de France","doi-asserted-by":"publisher","award":["00070721"],"id":[{"id":"10.13039\/501100004431","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Neuroinform."],"abstract":"The hippocampal subfields, pivotal to episodic memory, are distinct both in terms of cyto- and myeloarchitectony. Studying the structure of hippocampal subfields in vivo<\/jats:italic> is crucial to understand volumetric trajectories across the lifespan, from the emergence of episodic memory during early childhood to memory impairments found in older adults. However, segmenting hippocampal subfields on conventional MRI sequences is challenging because of their small size. Furthermore, there is to date no unified segmentation protocol for the hippocampal subfields, which limits comparisons between studies. Therefore, we introduced a novel segmentation tool called HSF short for hippocampal segmentation factory, which leverages an end-to-end deep learning pipeline. First, we validated HSF against currently used tools (ASHS, HIPS, and HippUnfold). Then, we used HSF on 3,750 subjects from the HCP development, young adults, and aging datasets to study the effect of age and sex on hippocampal subfields volumes. Firstly, we showed HSF to be closer to manual segmentation than other currently used tools (p<\/jats:italic> < 0.001), regarding the Dice Coefficient, Hausdorff Distance, and Volumetric Similarity. Then, we showed differential maturation and aging across subfields, with the dentate gyrus being the most affected by age. We also found faster growth and decay in men than in women for most hippocampal subfields. Thus, while we introduced a new, fast and robust end-to-end segmentation tool, our neuroanatomical results concerning the lifespan trajectories of the hippocampal subfields reconcile previous conflicting results.<\/jats:p>","DOI":"10.3389\/fninf.2023.1130845","type":"journal-article","created":{"date-parts":[[2023,6,15]],"date-time":"2023-06-15T04:47:06Z","timestamp":1686804426000},"update-policy":"http:\/\/dx.doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":4,"title":["A fast and robust hippocampal subfields segmentation: HSF revealing lifespan volumetric dynamics"],"prefix":"10.3389","volume":"17","author":[{"given":"Clement","family":"Poiret","sequence":"first","affiliation":[]},{"given":"Antoine","family":"Bouyeure","sequence":"additional","affiliation":[]},{"given":"Sandesh","family":"Patil","sequence":"additional","affiliation":[]},{"given":"Antoine","family":"Grigis","sequence":"additional","affiliation":[]},{"given":"Edouard","family":"Duchesnay","sequence":"additional","affiliation":[]},{"given":"Matthieu","family":"Faillot","sequence":"additional","affiliation":[]},{"given":"Michel","family":"Bottlaender","sequence":"additional","affiliation":[]},{"given":"Frederic","family":"Lemaitre","sequence":"additional","affiliation":[]},{"given":"Marion","family":"Noulhiane","sequence":"additional","affiliation":[]}],"member":"1965","published-online":{"date-parts":[[2023,6,15]]},"reference":[{"key":"B1","doi-asserted-by":"crossref","first-page":"p. 109","DOI":"10.1002\/9781118597705.ch6","article-title":"The development of memory from a neurocognitive and comparative perspective","volume-title":"The Wiley Handbook on the Development of Children's Memory","author":"Bachevalier","year":"2013"},{"key":"B2","doi-asserted-by":"publisher","first-page":"466","DOI":"10.1016\/j.nicl.2017.05.022","article-title":"A protocol for manual segmentation of medial temporal lobe subregions in 7 Tesla MRI","volume":"15","author":"Berron","year":"2017","journal-title":"NeuroImage Clin"},{"key":"B3","doi-asserted-by":"publisher","first-page":"335","DOI":"10.1016\/j.neuroimage.2018.10.009","article-title":"The lifespan human connectome project in aging: an overview","volume":"185","author":"Bookheimer","year":"2019","journal-title":"Neuroimage"},{"key":"B4","doi-asserted-by":"crossref","unstructured":"p. 51727\n BouyeureA.\n NoulhianeM.\n ElsevierEpisodic memory development in normal and adverse environments. In: Factors Affecting Neurodevelopment2021","DOI":"10.1016\/B978-0-12-817986-4.00044-4"},{"key":"B5","doi-asserted-by":"publisher","first-page":"1202","DOI":"10.1002\/hipo.23385","article-title":"Hippocampal subfield volumes and memory discrimination in the developing brain","volume":"31","author":"Bouyeure","year":"2021","journal-title":"Hippocampus"},{"key":"B6","doi-asserted-by":"publisher","first-page":"117931","DOI":"10.1016\/j.neuroimage.2021.117931","article-title":"Hippocampal subfield volumes across the healthy lifespan and the effects of MR sequence on estimates","volume":"233","author":"Bussy","year":"2021","journal-title":"Neuroimage"},{"key":"B7","unstructured":"CanadaK. L.\n Examining the Co-Development of Episodic Memory and Hippocampal Subfields \u2013 A Longitudinal Study. Digital Repository at the University of Maryland2020"},{"key":"B8","doi-asserted-by":"publisher","first-page":"105877","DOI":"10.1016\/j.bandc.2022.105877","article-title":"Age-related volumetric alterations in hippocampal subiculum region are associated with reduced retention of the \u201cwhen\u201d memory component","volume":"160","author":"Chi","year":"2022","journal-title":"Brain Cogn"},{"key":"B9","doi-asserted-by":"publisher","first-page":"239821281770144","DOI":"10.1177\/2398212817701448","article-title":"Segmenting subregions of the human hippocampus on structural magnetic resonance image scans: an illustrated tutorial","volume":"1","author":"Dalton","year":"2017","journal-title":"Brain Neurosci. Adv."},{"key":"B10","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1016\/j.neuroscience.2015.08.033","article-title":"Structural imaging of hippocampal subfields in healthy aging and Alzheimer's disease","volume":"309","author":"de Flores","year":"2015","journal-title":"Neuroscience"},{"key":"B11","unstructured":"DeKrakerJ.\n HaastR. A.\n YousifM. D.\n KaratB.\n K\u00f6hlerS.\n KhanA. R.\n 36519725HippUnfold: Automated Hippocampal Unfolding, Morphometry, and Subfield Segmentation. Neuroscience2021"},{"key":"B12","doi-asserted-by":"publisher","first-page":"e77945","DOI":"10.7554\/eLife.77945","article-title":"Automated hippocampal unfolding for morphometry and subfield segmentation with HippUnfold","volume":"11","author":"DeKraker","year":"2022","journal-title":"Elife"},{"key":"B13","doi-asserted-by":"publisher","first-page":"68","DOI":"10.1186\/s12874-022-01542-8","article-title":"Using linear and natural cubic splines, SITAR, and latent trajectory models to characterise nonlinear longitudinal growth trajectories in cohort studies","volume":"22","author":"Elhakeem","year":"2022","journal-title":"BMC Med. Res. Methodol"},{"key":"B14","doi-asserted-by":"publisher","first-page":"3358","DOI":"10.1016\/j.cub.2021.04.072","article-title":"Evidence of hippocampal learning in human infants","volume":"31","author":"Ellis","year":"2021","journal-title":"Curr. Biol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"545","DOI":"10.1002\/hipo.23172","article-title":"Characterization of hippocampal subfields using ex vivo MRI and histology data: Lessons for in vivo segmentation","volume":"30","author":"Flores","year":"2020","journal-title":"Hippocampus"},{"key":"B16","doi-asserted-by":"publisher","first-page":"S102","DOI":"10.1016\/S1053-8119(09)70884-5","article-title":"Unbiased nonlinear average age-appropriate brain templates from birth to adulthood","volume":"47","author":"Fonov","year":"2009","journal-title":"Neuroimage"},{"key":"B17","doi-asserted-by":"publisher","first-page":"1206","DOI":"10.1002\/hipo.23133","article-title":"The role of hippocampal subfield volume and fornix microstructure in episodic memory across the lifespan","volume":"29","author":"Foster","year":"2019","journal-title":"Hippocampus"},{"key":"B18","doi-asserted-by":"publisher","first-page":"225","DOI":"10.1002\/hipo.20154","article-title":"Gonadal hormone modulation of hippocampal neurogenesis in the adult","volume":"16","author":"Galea","year":"2006","journal-title":"Hippocampus"},{"key":"B19","doi-asserted-by":"publisher","first-page":"664","DOI":"10.1002\/hipo.20193","article-title":"Dynamic mapping of normal human hippocampal development","volume":"16","author":"Gogtay","year":"2006","journal-title":"Hippocampus"},{"key":"B20","doi-asserted-by":"publisher","first-page":"450","DOI":"10.1097\/00001648-199507000-00025","article-title":"Avoiding power loss associated with categorization and ordinal scores in dose-response and trend analysis: Epidemiology","volume":"6","author":"Greenland","year":"1995"},{"key":"B21","doi-asserted-by":"publisher","first-page":"77","DOI":"10.1186\/s13195-020-00642-1","article-title":"Imaging the aging brain: study design and baseline findings of the SENIOR cohort","volume":"12","author":"Haeger","year":"2020","journal-title":"Alz Res Therapy"},{"key":"B22","doi-asserted-by":"publisher","first-page":"3294","DOI":"10.1210\/en.2013-1129","article-title":"Androgens increase survival of adult-born neurons in the dentate gyrus by an androgen receptor-dependent mechanism in male rats","volume":"154","author":"Hamson","year":"2013","journal-title":"Endocrinology"},{"key":"B23","doi-asserted-by":"publisher","first-page":"665","DOI":"10.1038\/nn.4284","article-title":"Linking pattern completion in the hippocampus to predictive coding in visual cortex","volume":"19","author":"Hindy","year":"2016","journal-title":"Nat. Neurosci"},{"key":"B24","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1016\/j.neuroimage.2015.04.042","article-title":"A computational atlas of the hippocampal formation using ex vivo, ultra-high resolution MRI: Application to adaptive segmentation of in vivo MRI","volume":"115","author":"Iglesias","year":"2015","journal-title":"Neuroimage"},{"key":"B25","doi-asserted-by":"publisher","first-page":"15","DOI":"10.1016\/j.neuroscience.2020.05.025","article-title":"Androgen affects the dynamics of intrinsic plasticity of pyramidal neurons in the CA1 hippocampal subfield in adolescent male rats","volume":"440","author":"Islam","year":"2020","journal-title":"Neuroscience"},{"key":"B26","doi-asserted-by":"publisher","first-page":"150059","DOI":"10.1038\/sdata.2015.59","article-title":"Multi-contrast submillimetric 3 Tesla hippocampal subfield segmentation protocol and dataset","volume":"2","author":"Kulaga-Yoskovitz","year":"2015","journal-title":"Sci Data"},{"key":"B27","doi-asserted-by":"publisher","first-page":"498","DOI":"10.1038\/s41398-021-01628-9","article-title":"Distinct amyloid and tau PET signatures are associated with diverging clinical and imaging trajectories in patients with amnestic syndrome of the hippocampal type","volume":"11","author":"Lagarde","year":"2021","journal-title":"Transl Psychiatry"},{"key":"B28","doi-asserted-by":"publisher","first-page":"8","DOI":"10.1016\/j.bbr.2013.02.007","article-title":"Building hippocampal circuits to learn and remember: Insights into the development of human memory","volume":"254","author":"Lavenex","year":"2013","journal-title":"Behav Brain Res"},{"key":"B29","doi-asserted-by":"publisher","first-page":"162","DOI":"10.1016\/j.neuroimage.2014.03.019","article-title":"Volume of hippocampal subfields and episodic memory in childhood and adolescence","volume":"94","author":"Lee","year":"2014","journal-title":"Neuroimage"},{"key":"B30","doi-asserted-by":"publisher","first-page":"495","DOI":"10.1523\/JNEUROSCI.4516-03.2004","article-title":"Androgens increase spine synapse density in the CA1 hippocampal subfield of ovariectomized female rats","volume":"24","author":"Leranth","year":"2004","journal-title":"J. Neurosci"},{"key":"B31","unstructured":"LuoP.\n RenJ.\n PengZ.\n ZhangR.\n LiJ.\n Differentiable Learning-to-Normalize via Switchable Normalization. arXiv: 1806107792019"},{"key":"B32","doi-asserted-by":"publisher","first-page":"3651","DOI":"10.1093\/cercor\/bhy244","article-title":"Hippocampal shape maturation in childhood and adolescence","volume":"29","author":"Lynch","year":"2019","journal-title":"Cereb. Cortex"},{"key":"B33","doi-asserted-by":"publisher","first-page":"237","DOI":"10.1038\/s41597-020-0557-9","article-title":"CerebrA, registration and manual label correction of Mindboggle-101 atlas for MNI-ICBM152 template","volume":"7","author":"Manera","year":"2020","journal-title":"Sci Data"},{"key":"B34","doi-asserted-by":"publisher","first-page":"719","DOI":"10.1016\/j.neurobiolaging.2006.03.007","article-title":"Measurement of hippocampal subfields and age-related changes with high resolution MRI at 4T","volume":"28","author":"Mueller","year":"2007","journal-title":"Neurobiol Aging"},{"key":"B35","unstructured":"OktayO.\n SchlemperJ.\n FolgocL. L.\n LeeM.\n HeinrichM.\n MisawaK.\n Attention U-Net: Learning Where to Look for the Pancreas. arXiv:1804039992018"},{"key":"B36","first-page":"128","article-title":"Deep learning vs. traditional computer vision","author":"O'Mahony","year":"2020","journal-title":"Advances in Computer Vision"},{"key":"B37","doi-asserted-by":"publisher","first-page":"169","DOI":"10.1613\/jair.614","article-title":"Popular ensemble methods: an empirical study","volume":"11","author":"Opitz","year":"1999","journal-title":"jair"},{"key":"B38","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1002\/hipo.22818","article-title":"Episodic autobiographical memory is associated with variation in the size of hippocampal subregions","volume":"28","author":"Palombo","year":"2018","journal-title":"Hippocampus"},{"key":"B39","doi-asserted-by":"publisher","first-page":"E137","DOI":"10.1016\/j.ijrobp.2019.06.2177","article-title":"Feasibility of Automatic Segmentation of Hippocampus Based on Deep Learning in Hippocampus-Sparing Radiotherapy","volume":"105","author":"Qiu","year":"2019","journal-title":"Int. J. Radiat. Oncol. Biol. Phy"},{"key":"B40","doi-asserted-by":"publisher","first-page":"286","DOI":"10.1016\/j.neuroimage.2017.09.049","article-title":"HIPS. A new hippocampus subfield segmentation method","volume":"163","author":"Romero","year":"2017","journal-title":"Neuroimage"},{"key":"B41","doi-asserted-by":"crossref","first-page":"p. 166","DOI":"10.1109\/ICDCSW.2011.20","article-title":"Finding a \u201cKneedle\u201d in a haystack: detecting knee points in system behavior","author":"Satopaa","year":"2011","journal-title":"2011 31st International Conference on Distributed Computing Systems Workshops"},{"key":"B42","doi-asserted-by":"publisher","first-page":"2500","DOI":"10.1002\/hbm.24017","article-title":"A comparison of manual tracing and FreeSurfer for estimating hippocampal volume over the adult lifespan","volume":"39","author":"Schmidt","year":"2018","journal-title":"Hum Brain Mapp"},{"key":"B43","doi-asserted-by":"publisher","first-page":"106043","DOI":"10.1016\/j.dib.2020.106043","article-title":"Towards optimising MRI characterisation of tissue (TOMCAT) dataset including all longitudinal automatic segmentation of hippocampal subfields (LASHiS) data","volume":"32","author":"Shaw","year":"2020","journal-title":"Data Brief"},{"key":"B44","doi-asserted-by":"publisher","first-page":"456","DOI":"10.1016\/j.neuroimage.2018.08.050","article-title":"The lifespan human connectome project in development: a large-scale study of brain connectivity development in 5\u201321 year olds","volume":"183","author":"Somerville","year":"2018","journal-title":"Neuroimage"},{"key":"B45","doi-asserted-by":"publisher","DOI":"10.1002\/dneu.20457","article-title":"Testosterone and dihydrotestosterone, but not estradiol, enhance survival of new hippocampal neurons in adult male rats","author":"Spritzer","year":"2007","journal-title":"Devel Neurobio"},{"key":"B46","doi-asserted-by":"publisher","first-page":"1093","DOI":"10.1016\/j.neurobiolaging.2004.09.015","article-title":"Preservation of hippocampal volume throughout adulthood in healthy men and women","volume":"26","author":"Sullivan","year":"2005","journal-title":"Neurobiol Aging"},{"key":"B47","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1093\/cercor\/bhh121","article-title":"Male-specific volume expansion of the human hippocampus during adolescence","volume":"15","author":"Suzuki","year":"2004","journal-title":"Cereb Cortex."},{"key":"B48","doi-asserted-by":"publisher","first-page":"e46970","DOI":"10.1371\/journal.pone.0046970","article-title":"Devel-opmental trajectories of amygdala and hippocampus from infancy to early adulthood in healthy individuals. Krueger F, editor","volume":"7","author":"Uematsu","year":"2012","journal-title":"PLoS ONE"},{"key":"B49","doi-asserted-by":"publisher","first-page":"3020","DOI":"10.1002\/hbm.22825","article-title":"Hippocampal (subfield) volume and shape in relation to cognitive performance across the adult lifespan: hippocampal volume, shape, and age-related cognitive performance","volume":"36","author":"Voineskos","year":"2015","journal-title":"Hum. Brain Mapp"},{"key":"B50","doi-asserted-by":"publisher","first-page":"10154","DOI":"10.1073\/pnas.1803667115","article-title":"Anatomical and microstructural determinants of hippocampal subfield functional connectome embedding","volume":"115","author":"Vos de Wael","year":"2018","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"B51","doi-asserted-by":"publisher","first-page":"34","DOI":"10.1016\/j.neucom.2019.01.103","article-title":"Aleatoric uncertainty estimation with test-time augmentation for medical image segmentation with convolutional neural networks","volume":"338","author":"Wang","year":"2019","journal-title":"Neurocomputing"},{"key":"B52","doi-asserted-by":"publisher","first-page":"254","DOI":"10.1016\/j.neuroimage.2013.02.003","article-title":"A novel in vivo atlas of human hippocampal subfields using high-resolution 3T magnetic resonance imaging","volume":"74","author":"Winterburn","year":"2013","journal-title":"Neuroimage"},{"key":"B53","doi-asserted-by":"publisher","first-page":"261","DOI":"10.3389\/fnagi.2014.00261","article-title":"Critical appraisal of the hippocampal subfield segmentation package in freesurfer","volume":"6","author":"Wisse","year":"2014","journal-title":"Front Aging Neurosci."},{"key":"B54","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1002\/hipo.22671","article-title":"A harmonized segmentation protocol for hippocampal and parahippocampal subregions: Why do we need one and what are the key goals?: A harmonized hippocampal subfield protocol: key goals and impact","volume":"27","author":"Wisse","year":"2017","journal-title":"Hippocampus"},{"key":"B55","doi-asserted-by":"publisher","first-page":"1050","DOI":"10.3174\/ajnr.A4659","article-title":"Automated Hippocampal Subfield Segmentation at 7T MRI","volume":"37","author":"Wisse","year":"2016","journal-title":"AJNR. Am. J. Neuroradiol"},{"key":"B56","doi-asserted-by":"publisher","first-page":"3075","DOI":"10.1002\/hbm.22125","article-title":"Evolution of hippocampal shapes across the human lifespan: hippocampal shapes in aging","volume":"34","author":"Yang","year":"2013","journal-title":"Hum. Brain Mapp"},{"key":"B57","doi-asserted-by":"publisher","first-page":"116947","DOI":"10.1016\/j.neuroimage.2020.116947","article-title":"CAST. A multi-scale convolutional neural network based automated hippocampal subfield segmentation toolbox","volume":"218","author":"Yang","year":"2020","journal-title":"Neuroimage"},{"key":"B58","doi-asserted-by":"publisher","first-page":"515","DOI":"10.1016\/j.tins.2011.06.006","article-title":"Pattern separation in the hippocampus","volume":"34","author":"Yassa","year":"2011","journal-title":"Trends Neurosci"},{"key":"B59","doi-asserted-by":"publisher","first-page":"526","DOI":"10.1016\/j.neuroimage.2015.01.004","article-title":"Quantitative comparison of 21 protocols for labeling hippocampal subfields and parahippocampal subregions in in vivo MRI: towards a harmonized segmentation protocol","volume":"111","author":"Yushkevich","year":"","journal-title":"Neuroimage"},{"key":"B60","doi-asserted-by":"publisher","first-page":"258","DOI":"10.1002\/hbm.22627","article-title":"Automated volumetry and regional thickness analysis of hippocampal subfields and medial temporal cortical structures in mild cognitive impairment: automatic morphometry of MTL subfields in MCI","volume":"36","author":"Yushkevich","year":"","journal-title":"Hum. Brain Mapp"},{"key":"B61","doi-asserted-by":"publisher","first-page":"1208","DOI":"10.1016\/j.neuroimage.2010.06.040","article-title":"Nearly automatic segmentation of hippocampal subfields in in vivo focal T2-weighted MRI","volume":"53","author":"Yushkevich","year":"2010","journal-title":"Neuroimage"},{"key":"B62","doi-asserted-by":"publisher","first-page":"749","DOI":"10.1109\/LGRS.2018.2802944","article-title":"Road extraction by deep residual U-net","volume":"15","author":"Zhang","year":"2018","journal-title":"IEEE Geosci Remote Sensing Lett"},{"key":"B63","doi-asserted-by":"publisher","first-page":"30","DOI":"10.3389\/fninf.2019.00030","article-title":"Dilated dense U-Net for infant hippocampus subfield segmentation","volume":"13","author":"Zhu","year":"2019","journal-title":"Front Neuroinform"},{"key":"B64","doi-asserted-by":"publisher","first-page":"2377","DOI":"10.1002\/hbm.21374","article-title":"Brain structural trajectories over the adult lifespan","volume":"33","author":"Ziegler","year":"2012","journal-title":"Hum Brain Mapp"}],"container-title":["Frontiers in Neuroinformatics"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fninf.2023.1130845\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,6,15]],"date-time":"2023-06-15T04:47:11Z","timestamp":1686804431000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fninf.2023.1130845\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,6,15]]},"references-count":64,"alternative-id":["10.3389\/fninf.2023.1130845"],"URL":"https:\/\/doi.org\/10.3389\/fninf.2023.1130845","relation":{},"ISSN":["1662-5196"],"issn-type":[{"value":"1662-5196","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,6,15]]}}}