Elsevier

NeuroImage

Volume 49, Issue 3, 1 February 2010, Pages 2816-2825
NeuroImage

Dissociable neural circuits for encoding and retrieval of object locations during active navigation in humans

https://doi.org/10.1016/j.neuroimage.2009.10.021Get rights and content

Abstract

Several cortical and subcortical circuits have been implicated in object location memory and navigation. Uncertainty remains, however, about which neural circuits are involved in the distinct processes of encoding and retrieval during active navigation through three-dimensional space. We used functional magnetic resonance imaging (fMRI) to measure neural responses as participants learned the location of a single target object relative to a small set of landmarks. Following a delay, the target was removed and participants were required to navigate back to its original position. The relative and absolute locations of landmarks and the target object were changed on every trial, so that participants had to learn a novel arrangement for each spatial scene. At encoding, greater activity within the right hippocampus and the parahippocampal gyrus bilaterally predicted more accurate navigation to the hidden target object in the retrieval phase. By contrast, during the retrieval phase, more accurate performance was associated with increased activity in the left hippocampus and the striatum bilaterally. Dividing participants into good and poor navigators, based upon behavioural performance, revealed greater striatal activity in good navigators during retrieval, perhaps reflecting superior procedural learning in these individuals. By contrast, the poor navigators showed stronger left hippocampal activity, suggesting reliance on a less effective verbal or symbolic code by this group. Our findings suggest separate neural substrates for the encoding and retrieval stages of object location memory during active navigation, which are further modulated by participants' overall navigational ability.

Introduction

As humans navigate, they acquire knowledge about their environment, such as the spatial layout of salient landmarks based upon visual, proprioceptive, and kinaesthetic inputs. This information is encoded and stored in memory, allowing us to find our way back to a desired location within the same environment. In humans, three brain regions have been proposed to play a key role in the process of learning the layout of large-scale environments through navigational experience: the hippocampus (e.g., Doeller et al., 2008, Ekstrom et al., 2003, Ekstrom and Bookheimer, 2007, Grön et al., 2000, Wolbers et al., 2007), the parahippocampus (e.g., Ekstrom and Bookheimer, 2007, Epstein, 2008, Janzen and van Tourennout, 2004), and the striatum (e.g., Bohbot et al., 2004, Doeller et al., 2008, Orban et al., 2006). Although all three regions have been implicated in spatial navigation, it remains unclear how each contributes to the distinct processes of encoding and retrieval during the learning of novel spatial arrays. Several previous fMRI studies have investigated memory retrieval of object locations, while others have sought to identify the functional anatomy of three-dimensional spatial memory as a whole, without distinguishing between the distinct stages of encoding and retrieval. The neural bases of these processes have received considerable attention in cognitive domains such as verbal working memory and episodic memory (e.g., Ludowig et al., 2008, Schacter and Wagner, 1999). In the area of human spatial navigation, however, no previous fMRI study has examined patterns of neural activity associated with encoding and retrieval processes within the context of a single behavioural task.

In the present study, we sought to identify the neural circuits that underlie the distinct processes of encoding and retrieval during landmark-based navigation. We used event-related fMRI to measure neural responses as participants navigated a virtual environment. It has been shown that cognitive maps built up in virtual environments are comparable to those acquired in the real environment (Ruddle et al., 1997) and that spatial knowledge acquired in virtual environments can be transferred to the real world (Richardson et al., 1999). The principal limitation of studies that have used realistic virtual environments, such as towns or cities, is that the number, location, and relative salience of paths and landmarks cannot be adequately quantified or controlled. To overcome this problem, we employed a sparse virtual environment that consisted of an infinite, textured plain containing three cylindrical landmarks and a distinctive, pyramid-shaped target object. In the initial encoding phase of each trial, participants were required to navigate to and encode the location of the target object. After a short delay, participants re-entered the arena from one of four different positions and were required to navigate back to the remembered location of the target, which had been removed from the display. We sought to identify brain regions whose activity patterns predicted navigation performance, with the aim of determining the neural circuits underlying the formation and retrieval of landmark-based spatial representations. We also divided participants into ‘good’ and ‘poor’ navigators, based upon their behavioural performance, to determine whether activity in specific brain regions predicts participants' overall navigational ability.

Section snippets

Participants

Seventeen right-handed, healthy male volunteers (mean age = 31.6 years, SD = 7.4) with normal or corrected-to-normal vision gave written informed consent to participate in the study, which was approved by the University of Queensland Ethics Committee.

Task and stimuli

We used the Blender open source 3D content creation suite (The Blender Foundation, Amsterdam, the Netherlands) to create a virtual environment and administer the navigation task. Participants moved through the virtual arena by means of a joystick held

Behavioural data

The average duration, movement speed and extent of rotational movement for the encoding and retrieval phases, and the equivalent variables for the baseline condition, are shown in Fig. 2. Participants were significantly faster in the retrieval condition than in the corresponding baseline condition (paired t-test, P < 0.05). There were no significant differences between the experimental and the corresponding baseline conditions for the other behavioural parameters. None of these behavioural

Discussion

We measured brain activity with fMRI during object location learning, in which the encoding and retrieval stages of the task required participants to actively navigate within a virtual environment. Successful encoding of purely landmark-related knowledge, within a single trial and without reinforcement, was tightly linked to activity within the right hippocampus and the parahippocampus bilaterally. By contrast, the retrieval of relevant spatial representations during navigation to a remembered

Summary

Our findings indicate that the right hippocampus and the parahippocampal gyrus bilaterally underlie successful memory encoding of object locations during active navigation, while the striatum bilaterally and the left hippocampus are important for memory retrieval. Stronger striatal activity in good navigators might reflect a procedural component of the learning and retrieval process that is predominantly active in good navigators, whereas stronger left hippocampal activity in less successful

Acknowledgments

This work was supported by an Australian Research Council (ARC) and National Health and Medical Research Council (NHMRC) Thinking Systems Grant. We gratefully acknowledge the Thinking Systems Team for their support, and in particular Mark Wakabayashi for programming the virtual environment used in the study.

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