{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,12]],"date-time":"2026-10-12T16:46:20Z","timestamp":1791823580146,"version":"4.3.4"},"reference-count":53,"publisher":"Elsevier BV","issue":"7","license":[{"start":{"date-parts":[[2018,4,1]],"date-time":"2018-04-01T00:00:00Z","timestamp":1522540800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2018,2,20]],"date-time":"2018-02-20T00:00:00Z","timestamp":1519084800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100002347","name":"Bundesministerium f\u00fcr Bildung und Forschung","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100002347","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000781","name":"European Research Council","doi-asserted-by":"publisher","award":["335090"],"award-info":[{"award-number":["335090"]}],"id":[{"id":"10.13039\/501100000781","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["cell.com","elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Current Biology"],"published-print":{"date-parts":[[2018,4]]},"DOI":"10.1016\/j.cub.2018.02.038","type":"journal-article","created":{"date-parts":[[2018,3,18]],"date-time":"2018-03-18T21:00:23Z","timestamp":1521406823000},"page":"1108-1115.e6","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":141,"title":["Compromised Grid-Cell-like Representations in Old Age as a Key Mechanism to Explain Age-Related Navigational Deficits"],"prefix":"10.1016","volume":"28","author":[{"given":"Matthias","family":"Stangl","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Johannes","family":"Achtzehn","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Karin","family":"Huber","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Caroline","family":"Dietrich","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Claus","family":"Tempelmann","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thomas","family":"Wolbers","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.cub.2018.02.038_bib1","doi-asserted-by":"crossref","first-page":"1019","DOI":"10.1016\/j.neuron.2017.06.037","article-title":"The aging navigational system","volume":"95","author":"Lester","year":"2017","journal-title":"Neuron"},{"key":"10.1016\/j.cub.2018.02.038_bib2","doi-asserted-by":"crossref","first-page":"19","DOI":"10.1146\/annurev-neuro-070815-013824","article-title":"Ten years of grid cells","volume":"39","author":"Rowland","year":"2016","journal-title":"Annu. Rev. Neurosci."},{"key":"10.1016\/j.cub.2018.02.038_bib3","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1038\/nature03721","article-title":"Microstructure of a spatial map in the entorhinal cortex","volume":"436","author":"Hafting","year":"2005","journal-title":"Nature"},{"key":"10.1016\/j.cub.2018.02.038_bib4","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1038\/nrn1932","article-title":"Path integration and the neural basis of the \u2018cognitive map\u2019","volume":"7","author":"McNaughton","year":"2006","journal-title":"Nat. Rev. Neurosci."},{"key":"10.1016\/j.cub.2018.02.038_bib5","series-title":"Space, Time and Memory in the Hippocampal Formation","first-page":"373","article-title":"How does the brain solve the computational problems of spatial navigation?","author":"Widloski","year":"2014"},{"key":"10.1016\/j.cub.2018.02.038_bib6","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1038\/s41593-017-0039-3","article-title":"Impaired path integration in mice with disrupted grid cell firing","volume":"21","author":"Gil","year":"2018","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.cub.2018.02.038_bib7","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1007\/BF00308809","article-title":"Neuropathological stageing of Alzheimer-related changes","volume":"82","author":"Braak","year":"1991","journal-title":"Acta Neuropathol."},{"key":"10.1016\/j.cub.2018.02.038_bib8","doi-asserted-by":"crossref","first-page":"4491","DOI":"10.1523\/JNEUROSCI.16-14-04491.1996","article-title":"Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer\u2019s disease","volume":"16","author":"G\u00f3mez-Isla","year":"1996","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.cub.2018.02.038_bib9","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1136\/jnnp.71.4.441","article-title":"Magnetic resonance imaging of the entorhinal cortex and hippocampus in mild cognitive impairment and Alzheimer\u2019s disease","volume":"71","author":"Du","year":"2001","journal-title":"J.\u00a0Neurol. Neurosurg. Psychiatry"},{"key":"10.1016\/j.cub.2018.02.038_bib10","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1016\/S0197-4580(03)00084-8","article-title":"Hippocampus and entorhinal cortex in mild cognitive impairment and early AD","volume":"25","author":"Pennanen","year":"2004","journal-title":"Neurobiol. Aging"},{"key":"10.1016\/j.cub.2018.02.038_bib11","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/j.jns.2005.05.001","article-title":"Neuroimaging as a marker of the onset and progression of Alzheimer\u2019s disease","volume":"236","author":"Masdeu","year":"2005","journal-title":"J.\u00a0Neurol. Sci."},{"key":"10.1016\/j.cub.2018.02.038_bib12","doi-asserted-by":"crossref","first-page":"108190","DOI":"10.1155\/2010\/108190","article-title":"Selective vulnerability of neurons in layer II of the entorhinal cortex during aging and Alzheimer\u2019s disease","volume":"2010","author":"Stranahan","year":"2010","journal-title":"Neural Plast."},{"key":"10.1016\/j.cub.2018.02.038_bib13","doi-asserted-by":"crossref","first-page":"919","DOI":"10.1093\/cercor\/bhs379","article-title":"Accelerating cortical thinning: unique to dementia or universal in aging?","volume":"24","author":"Fjell","year":"2014","journal-title":"Cereb. Cortex"},{"key":"10.1016\/j.cub.2018.02.038_bib14","doi-asserted-by":"crossref","first-page":"304","DOI":"10.1038\/nn.3606","article-title":"Molecular drivers and cortical spread of lateral entorhinal cortex dysfunction in preclinical Alzheimer\u2019s disease","volume":"17","author":"Khan","year":"2014","journal-title":"Nat. Neurosci."},{"key":"10.1016\/j.cub.2018.02.038_bib15","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1038\/nature08704","article-title":"Evidence for grid cells in a human memory network","volume":"463","author":"Doeller","year":"2010","journal-title":"Nature"},{"key":"10.1016\/j.cub.2018.02.038_bib16","doi-asserted-by":"crossref","first-page":"430","DOI":"10.1126\/science.aac8128","article-title":"Reduced grid-cell-like representations in adults at genetic risk for Alzheimer\u2019s disease","volume":"350","author":"Kunz","year":"2015","journal-title":"Science"},{"key":"10.1016\/j.cub.2018.02.038_bib17","doi-asserted-by":"crossref","first-page":"842","DOI":"10.1016\/j.cub.2016.01.042","article-title":"Grid-like processing of imagined navigation","volume":"26","author":"Horner","year":"2016","journal-title":"Curr. Biol."},{"key":"10.1016\/j.cub.2018.02.038_bib18","doi-asserted-by":"crossref","first-page":"47","DOI":"10.3389\/fninf.2017.00047","article-title":"The GridCAT: a toolbox for automated analysis of human grid cell codes in fMRI","volume":"11","author":"Stangl","year":"2017","journal-title":"Front. Neuroinform."},{"key":"10.1016\/j.cub.2018.02.038_bib19","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1038\/40859","article-title":"Multistability of cognitive maps in the hippocampus of old rats","volume":"388","author":"Barnes","year":"1997","journal-title":"Nature"},{"key":"10.1016\/j.cub.2018.02.038_bib20","doi-asserted-by":"crossref","first-page":"3094","DOI":"10.1523\/JNEUROSCI.1348-12.2013","article-title":"Tracking the course of hippocampal representations during learning: when is the map required?","volume":"33","author":"Schimanski","year":"2013","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.cub.2018.02.038_bib21","doi-asserted-by":"crossref","first-page":"20120516","DOI":"10.1098\/rstb.2012.0516","article-title":"Functional connectivity of the entorhinal-hippocampal space circuit","volume":"369","author":"Zhang","year":"2013","journal-title":"Philos. Trans. R. Soc. Lond. B Biol. Sci."},{"key":"10.1016\/j.cub.2018.02.038_bib22","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1038\/nature05601","article-title":"Hippocampal remapping and grid realignment in entorhinal cortex","volume":"446","author":"Fyhn","year":"2007","journal-title":"Nature"},{"key":"10.1016\/j.cub.2018.02.038_bib23","series-title":"The Rat Nervous System, Second Edition","first-page":"443","article-title":"The hippocampus","author":"Amaral","year":"1995"},{"key":"10.1016\/j.cub.2018.02.038_bib24","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1152\/jn.1993.70.1.128","article-title":"Differential electroresponsiveness of\u00a0stellate and pyramidal-like cells of medial entorhinal cortex layer II","volume":"70","author":"Alonso","year":"1993","journal-title":"J.\u00a0Neurophysiol."},{"key":"10.1016\/j.cub.2018.02.038_bib25","doi-asserted-by":"crossref","first-page":"801","DOI":"10.1002\/hipo.20327","article-title":"An oscillatory interference model of grid cell firing","volume":"17","author":"Burgess","year":"2007","journal-title":"Hippocampus"},{"key":"10.1016\/j.cub.2018.02.038_bib26","doi-asserted-by":"crossref","first-page":"758","DOI":"10.1126\/science.1125572","article-title":"Conjunctive representation of position, direction, and velocity in entorhinal cortex","volume":"312","author":"Sargolini","year":"2006","journal-title":"Science"},{"key":"10.1016\/j.cub.2018.02.038_bib27","doi-asserted-by":"crossref","first-page":"88","DOI":"10.1016\/j.bbr.2009.08.001","article-title":"Age differences in visual path integration","volume":"205","author":"Mahmood","year":"2009","journal-title":"Behav. Brain Res."},{"key":"10.1016\/j.cub.2018.02.038_bib28","doi-asserted-by":"crossref","first-page":"26","DOI":"10.3389\/fnagi.2012.00026","article-title":"Age differences in virtual environment and real world path integration","volume":"4","author":"Adamo","year":"2012","journal-title":"Front. Aging Neurosci."},{"key":"10.1016\/j.cub.2018.02.038_bib29","doi-asserted-by":"crossref","first-page":"1770","DOI":"10.1002\/hipo.22011","article-title":"Ageing effects on path integration and landmark navigation","volume":"22","author":"Harris","year":"2012","journal-title":"Hippocampus"},{"key":"10.1016\/j.cub.2018.02.038_bib30","doi-asserted-by":"crossref","first-page":"2761","DOI":"10.1016\/j.neurobiolaging.2014.04.003","article-title":"How cognitive aging affects multisensory integration of navigational cues","volume":"35","author":"Bates","year":"2014","journal-title":"Neurobiol. Aging"},{"key":"10.1016\/j.cub.2018.02.038_bib31","doi-asserted-by":"crossref","first-page":"4266","DOI":"10.1523\/JNEUROSCI.4353-05.2006","article-title":"A spin glass model of path integration in rat medial entorhinal cortex","volume":"26","author":"Fuhs","year":"2006","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.cub.2018.02.038_bib32","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1142\/S0129065707001093","article-title":"A model of grid cells based on a twisted torus topology","volume":"17","author":"Guanella","year":"2007","journal-title":"Int. J. Neural Syst."},{"key":"10.1016\/j.cub.2018.02.038_bib33","doi-asserted-by":"crossref","first-page":"1213","DOI":"10.1002\/hipo.20512","article-title":"Grid cell mechanisms and function: contributions of entorhinal persistent spiking and phase resetting","volume":"18","author":"Hasselmo","year":"2008","journal-title":"Hippocampus"},{"key":"10.1016\/j.cub.2018.02.038_bib34","doi-asserted-by":"crossref","first-page":"e1000291","DOI":"10.1371\/journal.pcbi.1000291","article-title":"Accurate path integration in continuous attractor network models of grid cells","volume":"5","author":"Burak","year":"2009","journal-title":"PLoS Comput. Biol."},{"key":"10.1016\/j.cub.2018.02.038_bib35","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1016\/j.neuron.2011.07.023","article-title":"Computational models of grid cells","volume":"71","author":"Giocomo","year":"2011","journal-title":"Neuron"},{"key":"10.1016\/j.cub.2018.02.038_bib36","doi-asserted-by":"crossref","first-page":"16","DOI":"10.3389\/fncir.2012.00016","article-title":"Models of grid cell spatial firing published 2005-2011","volume":"6","author":"Zilli","year":"2012","journal-title":"Front. Neural Circuits"},{"key":"10.1016\/j.cub.2018.02.038_bib37","doi-asserted-by":"crossref","first-page":"9408","DOI":"10.1523\/JNEUROSCI.2146-07.2007","article-title":"Differential recruitment of the hippocampus, medial prefrontal cortex, and the human motion complex during path integration in humans","volume":"27","author":"Wolbers","year":"2007","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.cub.2018.02.038_bib38","doi-asserted-by":"crossref","first-page":"19304","DOI":"10.1523\/JNEUROSCI.1825-13.2013","article-title":"Hippocampus and retrosplenial cortex combine path integration signals for successful navigation","volume":"33","author":"Sherrill","year":"2013","journal-title":"J.\u00a0Neurosci."},{"key":"10.1016\/j.cub.2018.02.038_bib39","doi-asserted-by":"crossref","DOI":"10.1523\/ENEURO.0346-16.2017","article-title":"Individual differences in human path integration abilities correlate with gray matter volume in retrosplenial cortex, hippocampus, and medial prefrontal cortex","volume":"4","author":"Chrastil","year":"2017","journal-title":"eNeuro"},{"key":"10.1016\/j.cub.2018.02.038_bib40","doi-asserted-by":"crossref","first-page":"4042","DOI":"10.1073\/pnas.0611314104","article-title":"Spatial navigation deficit in amnestic mild cognitive impairment","volume":"104","author":"Hort","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.cub.2018.02.038_bib41","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1159\/000289226","article-title":"Human analogue of the morris water maze for testing subjects at risk of Alzheimer\u2019s disease","volume":"7","author":"Lacz\u00f3","year":"2010","journal-title":"Neurodegener. Dis."},{"key":"10.1016\/j.cub.2018.02.038_bib42","doi-asserted-by":"crossref","first-page":"150","DOI":"10.1016\/j.bbr.2016.03.052","article-title":"Real-space path integration is impaired in Alzheimer\u2019s disease and mild cognitive impairment","volume":"307","author":"Mokrisova","year":"2016","journal-title":"Behav. Brain Res."},{"key":"10.1016\/j.cub.2018.02.038_bib43","doi-asserted-by":"crossref","first-page":"1464","DOI":"10.1126\/science.aaf0941","article-title":"Organizing conceptual knowledge in humans with a gridlike code","volume":"352","author":"Constantinescu","year":"2016","journal-title":"Science"},{"key":"10.1016\/j.cub.2018.02.038_bib44","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1038\/nature21692","article-title":"Mapping of a non-spatial\u00a0dimension by the hippocampal-entorhinal circuit","volume":"543","author":"Aronov","year":"2017","journal-title":"Nature"},{"key":"10.1016\/j.cub.2018.02.038_bib45","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1111\/j.1532-5415.2005.53221.x","article-title":"The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment","volume":"53","author":"Nasreddine","year":"2005","journal-title":"J.\u00a0Am. Geriatr. Soc."},{"key":"10.1016\/j.cub.2018.02.038_bib46","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1002\/gps.2101","article-title":"Cross validation of the Montreal Cognitive Assessment in community dwelling older adults residing in the Southeastern US","volume":"24","author":"Luis","year":"2009","journal-title":"Int. J. Geriatr. Psychiatry"},{"key":"10.1016\/j.cub.2018.02.038_bib47","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1080\/01449299508914630","article-title":"Issues in training older adults to use computers","volume":"14","author":"Kelley","year":"1995","journal-title":"Behav. Inf. Technol."},{"key":"10.1016\/j.cub.2018.02.038_bib48","doi-asserted-by":"crossref","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":"10.1016\/j.cub.2018.02.038_bib49","doi-asserted-by":"crossref","first-page":"22552","DOI":"10.1073\/pnas.0908238106","article-title":"Performance level modulates adult age differences in brain activation during spatial working memory","volume":"106","author":"Nagel","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.cub.2018.02.038_bib50","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1111\/j.1538-4632.1993.tb00300.x","article-title":"The encoding-error model of pathway completion without vision","volume":"25","author":"Fujita","year":"1993","journal-title":"Geogr. Anal."},{"key":"10.1016\/j.cub.2018.02.038_bib51","doi-asserted-by":"crossref","first-page":"1152","DOI":"10.1073\/pnas.1011843108","article-title":"Visual influence on\u00a0path integration in darkness indicates a multimodal representation of large-scale space","volume":"108","author":"Tcheang","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"10.1016\/j.cub.2018.02.038_bib52","doi-asserted-by":"crossref","first-page":"425","DOI":"10.1016\/S0160-2896(02)00116-2","article-title":"Development of a self-report measure of environmental spatial ability","volume":"30","author":"Hegarty","year":"2002","journal-title":"Intelligence"},{"key":"10.1016\/j.cub.2018.02.038_bib53","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1207\/S15324826AN0704_8","article-title":"The Corsi block-tapping task: standardization and normative data","volume":"7","author":"Kessels","year":"2000","journal-title":"Appl. Neuropsychol."}],"container-title":["Current Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0960982218302239?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0960982218302239?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2022,7,6]],"date-time":"2022-07-06T00:52:00Z","timestamp":1657068720000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0960982218302239"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,4]]},"references-count":53,"journal-issue":{"issue":"7","published-print":{"date-parts":[[2018,4]]}},"alternative-id":["S0960982218302239"],"URL":"https:\/\/doi.org\/10.1016\/j.cub.2018.02.038","relation":{},"ISSN":["0960-9822"],"issn-type":[{"value":"0960-9822","type":"print"}],"subject":[],"published":{"date-parts":[[2018,4]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"Compromised Grid-Cell-like Representations in Old Age as a Key Mechanism to Explain Age-Related Navigational Deficits","name":"articletitle","label":"Article Title"},{"value":"Current Biology","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.cub.2018.02.038","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"\u00a9 2018 The Author(s). Published by Elsevier Ltd.","name":"copyright","label":"Copyright"}]}}