Dissociable neural circuits for encoding and retrieval of object locations during active navigation in humans
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.
References (61)
- et al.
Magnetic resonance imaging of cerebellar–prefrontal and cerebellar–parietal functional connectivity
Neuroimage
(2005) - et al.
The human hippocampus and spatial and episodic memory
Neuron
(2002) - et al.
Neural activity in the human brain relating to uncertainty and arousal during anticipation
Neuron
(2001) Parahippocampal and retrosplenial contributions to human spatial navigation
Trends Cogn. Sci.
(2008)- et al.
Pure topographical disorientation: a definition and anatomical basis
Cortex
(1987) - et al.
The well-worn route and the path less travelled: distinct neural bases of route following and wayfinding in humans
Neuron
(2003) - et al.
Involvement of basal ganglia and orbitofrontal cortex in goal-directed behavior
Prog. Brain Res.
(2000) - et al.
Effects of ventrolateral–ventromedial thalamic lesions on motor coordination and spatial orientation in rats
Neurosci. Res.
(2003) - et al.
The cerebellum's involvement in the judgment of spatial orientation: a functional magnetic resonance imaging study
Neuropsychologia
(2005) - et al.
Cognitive maps and the hippocampus
Trends Cogn. Sci.
(2003)
Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning
Neurobiol. Learn. Mem.
The cerebellum in the spatial problem solving: a co-star or a guest star?
Progr. Neurobiol.
Evidence for a cerebellar role in reduced exploration and stereotyped behavior in autism
Biol. Psychiatry
Competition among multiple memory systems: converging evidence from animal and human brain studies
Neuropsychologia
Neural correlates of working memory for sign language
Cognit. Brain Res.
Effects of prenatal marijuana on visuospatial working memory: an fMRI study in young adults
Neurotoxicol. Teratol.
Functional magnetic resonance imaging of mental rotation and memory scanning: a multidimensional scaling analysis of brain activation patterns
Brain Res. Rev.
Gender differences in post-temporal lobectomy verbal memory and relationships between MRI hippocampal volumes and preoperative verbal memory
Epilepsy Res.
Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single subject brain
NeuroImage
Why am I unsure? Internal and external attributions of uncertainty dissociated by fMRI
NeuroImage
Optimal EPI parameters for reduction of susceptibility-induced BOLD sensitivity losses: a wholebrain analysis at 3 T and 1.5 T
Neuroimage
The parahippocampus subserves topographical learning in man
Cereb. Cortex
Intentional maps in posterior parietal cortex
Annu. Rev. Neurosci.
The parahippocampal cortex mediates spatial and nonspatial associations
Cereb. Cortex
From visual affordances in monkey parietal cortex to hippocampo-parietal interactions underlying rat navigation
Philos. Trans. R. Soc. Lond., B. Biol. Sci.
Hippocampal function and spatial memory: evidence from functional neuroimaging in healthy participants and performance of patients with medial temporal lobe resections
Neuropsychology
Predictions derived from modelling the hippocampal role in navigation
Biol. Cybern.
The inferior parietal lobule is the target of output from the superior colliculus, hippocampus, and cerebellum
J. Neurosci.
Transient and sustained activity in a distributed neural system for human working memory
Nature
Distinct error-correcting and incidental learning of location relative to landmarks and boundaries
Proc. Natl. Acad. Sci. U. S. A.
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