Combining Patient-lesion and Big Data Approaches to Reveal Hippocampal Contributions to Spatial Memory and Navigation

Overview

Journal iScience

Publisher Cell Press

Date 2024 Jul 1

PMID 38947515

Authors

Sara Pishdadian

Antoine Coutrot

Lauren Webber

Michael Hornberger

Hugo Spiers

R Shayna Rosenbaum

Affiliations

Soon will be listed here.

Abstract

Classic findings of impaired allocentric spatial learning and memory following hippocampal lesions indicate that the hippocampus supports cognitive maps of one's environment. Many studies assess navigation in vista space virtual reality environments and compare hippocampal-lesioned individuals' performance to that of small control samples, potentially stifling detection of preserved and impaired performance. Using the mobile app we examined navigation in diverse complex environments in two individuals with hippocampal lesions relative to demographically matched controls ( = 17,734). We found surprisingly accurate navigation in several environments, particularly those containing a constrained set of sub-goals, paths, and/or turns. Areas of impaired performance may reflect a role for the hippocampus in anterograde memory and more flexible and/or precise spatial representations, even when the need for allocentric processing is minimal. The results emphasize the value of combining single cases with big data and illustrate navigation performance profiles in individuals with hippocampal compromise.

Citing Articles

Predicting real-world navigation performance from a virtual navigation task in older adults.

Goodroe S, Fernandez Velasco P, Gahnstrom C, Wiener J, Coutrot A, Hornberger M PLoS One. 2025; 20(1):e0317026.

PMID: 39869655 PMC: 11771902. DOI: 10.1371/journal.pone.0317026.

References

Shrager Y, Kirwan C, Squire L . Neural basis of the cognitive map: path integration does not require hippocampus or entorhinal cortex. Proc Natl Acad Sci U S A. 2008; 105(33):12034-8. PMC: 2575247. DOI: 10.1073/pnas.0805414105. View

Coughlan G, Coutrot A, Khondoker M, Minihane A, Spiers H, Hornberger M . Toward personalized cognitive diagnostics of at-genetic-risk Alzheimer's disease. Proc Natl Acad Sci U S A. 2019; 116(19):9285-9292. PMC: 6511014. DOI: 10.1073/pnas.1901600116. View

Farzanfar D, Spiers H, Moscovitch M, Rosenbaum R . From cognitive maps to spatial schemas. Nat Rev Neurosci. 2022; 24(2):63-79. DOI: 10.1038/s41583-022-00655-9. View

Rosenbaum R, Priselac S, Kohler S, Black S, Gao F, Nadel L . Remote spatial memory in an amnesic person with extensive bilateral hippocampal lesions. Nat Neurosci. 2000; 3(10):1044-8. DOI: 10.1038/79867. View

Kessels R, de Haan E, Kappelle L, Postma A . Varieties of human spatial memory: a meta-analysis on the effects of hippocampal lesions. Brain Res Brain Res Rev. 2001; 35(3):295-303. DOI: 10.1016/s0165-0173(01)00058-3. View

Coughlan G, Laczo J, Hort J, Minihane A, Hornberger M . Spatial navigation deficits - overlooked cognitive marker for preclinical Alzheimer disease?. Nat Rev Neurol. 2018; 14(8):496-506. DOI: 10.1038/s41582-018-0031-x. View

Maguire E, Nannery R, Spiers H . Navigation around London by a taxi driver with bilateral hippocampal lesions. Brain. 2006; 129(Pt 11):2894-907. DOI: 10.1093/brain/awl286. View

Guilmette T, Sweet J, Hebben N, Koltai D, Mahone E, Spiegler B . American Academy of Clinical Neuropsychology consensus conference statement on uniform labeling of performance test scores. Clin Neuropsychol. 2020; 34(3):437-453. DOI: 10.1080/13854046.2020.1722244. View

Epstein R . Parahippocampal and retrosplenial contributions to human spatial navigation. Trends Cogn Sci. 2008; 12(10):388-96. PMC: 2858632. DOI: 10.1016/j.tics.2008.07.004. View

10.

Seton C, Coutrot A, Hornberger M, Spiers H, Knight R, Whyatt C . Wayfinding and path integration deficits detected using a virtual reality mobile app in patients with traumatic brain injury. PLoS One. 2023; 18(3):e0282255. PMC: 9997943. DOI: 10.1371/journal.pone.0282255. View

11.

Rosenbaum R, Cassidy B, Herdman K . Patterns of preserved and impaired spatial memory in a case of developmental amnesia. Front Hum Neurosci. 2015; 9:196. PMC: 4426723. DOI: 10.3389/fnhum.2015.00196. View

12.

Rosenbaum R, Gilboa A, Moscovitch M . Case studies continue to illuminate the cognitive neuroscience of memory. Ann N Y Acad Sci. 2014; 1316:105-33. DOI: 10.1111/nyas.12467. View

13.

Coutrot A, Schmidt S, Coutrot L, Pittman J, Hong L, Wiener J . Virtual navigation tested on a mobile app is predictive of real-world wayfinding navigation performance. PLoS One. 2019; 14(3):e0213272. PMC: 6422266. DOI: 10.1371/journal.pone.0213272. View

14.

Goodrich-Hunsaker N, Hopkins R . Spatial memory deficits in a virtual radial arm maze in amnesic participants with hippocampal damage. Behav Neurosci. 2010; 124(3):405-13. DOI: 10.1037/a0019193. View

15.

Patai E, Javadi A, Ozubko J, OCallaghan A, Ji S, Robin J . Hippocampal and Retrosplenial Goal Distance Coding After Long-term Consolidation of a Real-World Environment. Cereb Cortex. 2019; 29(6):2748-2758. PMC: 6519689. DOI: 10.1093/cercor/bhz044. View

16.

Urgolites Z, Kim S, Hopkins R, Squire L . Map reading, navigating from maps, and the medial temporal lobe. Proc Natl Acad Sci U S A. 2016; 113(50):14289-14293. PMC: 5167206. DOI: 10.1073/pnas.1617786113. View

17.

Hamre C, Fure B, Helbostad J, Wyller T, Ihle-Hansen H, Vlachos G . Impairments in spatial navigation during walking in patients 70 years or younger with mild stroke. Top Stroke Rehabil. 2020; 27(8):601-609. DOI: 10.1080/10749357.2020.1755814. View

18.

Bohbot V, Corkin S . Posterior parahippocampal place learning in H.M. Hippocampus. 2007; 17(9):863-72. DOI: 10.1002/hipo.20313. View

19.

Vann S, Aggleton J, Maguire E . What does the retrosplenial cortex do?. Nat Rev Neurosci. 2009; 10(11):792-802. DOI: 10.1038/nrn2733. View

20.

Corkin S . What's new with the amnesic patient H.M.?. Nat Rev Neurosci. 2002; 3(2):153-60. DOI: 10.1038/nrn726. View