Buckley, Matthew, McGregor, Anthony, Ihssen, Niklas, Austen, Joseph, Thurlbeck, Simon, Smith, Shamus P., Heinecke, Armin and Lew, Adina Raquel (2024). The well‐worn route revisited: Striatal and hippocampal system contributions to familiar route navigation. Hippocampus, 34 (7), pp. 310-326.
Abstract
Classic research has shown a division in the neuroanatomical structures that support flexible (e.g., short‐cutting) and habitual (e.g., familiar route following) navigational behavior, with hippocampal–caudate systems associated with the former and putamen systems with the latter. There is, however, disagreement about whether the neural structures involved in navigation process particular forms of spatial information, such as associations between constellations of cues forming a cognitive map, versus single landmark‐action associations, or alternatively, perform particular reinforcement learning algorithms that allow the use of different spatial strategies, so‐called model‐based (flexible) or model‐free (habitual) forms of learning. We sought to test these theories by asking participants (N = 24) to navigate within a virtual environment through a previously learned, 9‐junction route with distinctive landmarks at each junction while undergoing functional magnetic resonance imaging (fMRI). In a series of probe trials, we distinguished knowledge of individual landmark‐action associations along the route versus knowledge of the correct sequence of landmark‐action associations, either by having absent landmarks, or “out‐of‐sequence” landmarks. Under a map‐based perspective, sequence knowledge would not require hippocampal systems, because there are no constellations of cues available for cognitive map formation. Within a learning‐based model, however, responding based on knowledge of sequence would require hippocampal systems because prior context has to be utilized. We found that hippocampal–caudate systems were more active in probes requiring sequence knowledge, supporting the learning‐based model. However, we also found greater putamen activation in probes where navigation based purely on sequence memory could be planned, supporting models of putamen function that emphasize its role in action sequencing.
Publication DOI: | https://doi.org/10.1002/hipo.23607 |
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Divisions: | College of Health & Life Sciences College of Health & Life Sciences > School of Psychology College of Health & Life Sciences > Aston Institute of Health & Neurodevelopment (AIHN) Aston University (General) |
Funding Information: | This research was funded by ESRC grant ES/M01066X/1, awarded to AM, ARL, NI, and SPS. We thank Dr. Mushfa Yousuf for advice on the BASCO toolbox for beta series connectivity analysis and Prof. Chris Plack for feedback on an earlier version of the manuscri |
Additional Information: | Copyright © 2024 The Authors. Hippocampus published by Wiley Periodicals LLC. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. |
Uncontrolled Keywords: | caudate,cognitive map,hippocampus,model-based learning,model-free learning,putamen,sequential-egocentric navigation,Cognitive Neuroscience |
Publication ISSN: | 1098-1063 |
Data Access Statement: | Raw data can be accessed at https://reshare.ukdataservice.ac.uk/<br/>855171/. Processed data linked to tables and figures reported can be<br/>accessed at https://osf.io/mz63e/. |
Last Modified: | 02 Dec 2024 09:06 |
Date Deposited: | 29 May 2024 14:35 |
Full Text Link: | |
Related URLs: |
https://onlinel ... 1002/hipo.23607
(Publisher URL) http://www.scop ... tnerID=8YFLogxK (Scopus URL) https://reshare ... .ac.uk/ 855171/ (Related URL) https://osf.io/mz63e/ (Related URL) |
PURE Output Type: | Article |
Published Date: | 2024-05-09 |
Published Online Date: | 2024-05-09 |
Accepted Date: | 2024-02-20 |
Authors: |
Buckley, Matthew
(
0000-0002-6879-9408)
McGregor, Anthony Ihssen, Niklas Austen, Joseph Thurlbeck, Simon Smith, Shamus P. Heinecke, Armin Lew, Adina Raquel |