The well‐worn route revisited: Striatal and hippocampal system contributions to familiar route navigation

Matthew Buckley, Anthony McGregor, Niklas Ihssen, Joseph Austen, Simon Thurlbeck, Shamus P. Smith, Armin Heinecke, Adina Raquel Lew

Research output: Contribution to journalArticlepeer-review

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.
Original languageEnglish
Pages (from-to)310-326
Number of pages17
JournalHippocampus
Volume34
Issue number7
Early online date9 May 2024
DOIs
Publication statusE-pub ahead of print - 9 May 2024

Bibliographical note

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.

Data Access Statement

Raw data can be accessed at https://reshare.ukdataservice.ac.uk/
855171/. Processed data linked to tables and figures reported can be
accessed at https://osf.io/mz63e/.

Keywords

  • caudate
  • cognitive map
  • hippocampus
  • model-based learning
  • model-free learning
  • putamen
  • sequential-egocentric navigation

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