A temporoparietal and prefrontal network for retrieving the spatial context of lifelike events
Abstract
Virtual reality (VR) and event-related functional magnetic resonance imaging were used to study memory for the spatial context of controlled but lifelike events. Subjects received a set of objects from two different people in two different places within a VR environment. Memory for the objects, and for where and from whom they were received was tested by putting the subject back into a place in the company of a person and giving a paired forced choice of objects. In four conditions objects had to be chosen according to different criteria: which was received in that place, which was received from that person, which object was recognized, and which object was widest. Event-related functional magnetic resonance imaging was performed during testing to identify areas involved in retrieval of the spatial context of an event. A network of areas was identified consisting of a temporoparietal pathway running between the precuneus and parahippocampi via retrosplenial cortex and the parieto-occipital sulcus, left hippocampus, bilateral posterior parietal, dorsolateral, ventrolateral and anterior prefrontal cortices, and the anterior cingulate. Of these areas the parahippocampal, right posterior parietal, and posteriodorsal medial parietal areas were specifically involved in retrieval of spatial context compared to retrieval of nonspatial context. The posterior activations are consistent with a model of long-term storage of allocentric representations in medial temporal regions with translation to body-centered and head-centered representations computed in right posterior parietal cortex and buffered in the temporoparietal pathway so as to provide an imageable representation in the precuneus. Prefrontal activations are consistent with strategic retrieval processes, including those required to overcome the interference between the highly similar events.
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Prior neuropsychological research has consistently indicated the dominance of the right hemisphere in processing spatial information.
“Prior neuropsychological research has consistently indicated the dominance of the right hemisphere in processing spatial information (Spiers et al. 2001; Burgess et al. 2001, 2002)”
From Hippocampal and Retrosplenial Goal Distance Coding After Long-term Consolidation of a Real-World Environment (2019) · cites this paper as Burgess et al. 2001
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Brewin, C. R., Gregory, J. D., Lipton, M., & Burgess, N. (2010) · Psychological Review · doi:10.1037/a0018113 · Cited by 1,226 · see citing works
Self-citationMultisensory brain mechanisms of bodily self-consciousness.
Blanke, O. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3292 · Cited by 1,147 · see citing works
Remembering the past and imagining the future: A neural model of spatial memory and imagery.
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Self-citationPrefrontal and medial temporal lobe interactions in long-term memory
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Self-citationNeural systems for recognition of familiar faces
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Are spatial memories strengthened in the human hippocampus during slow wave sleep?
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Neural correlates of the first-person-perspective
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<i>Spatial Cognition and the Brain</i>
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Self-citationNeural Correlates of First-Person Perspective as One Constituent of Human Self-Consciousness
Vogeley, K., May, M., Ritzl, A., Falkai, P., Zilles, K., & Fink, G. R. (2004) · Journal of Cognitive Neuroscience · doi:10.1162/089892904970799 · Cited by 548 · see citing works
Neuroimaging studies of autobiographical event memory
Maguire, E. A. (2001) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2001.0944 · Cited by 513 · see citing works
Self-citationSpace in the brain: How the hippocampal formation supports spatial cognition
Hartley, T., Lever, C., Burgess, N., & O'Keefe, J. (2014) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2012.0510 · Cited by 495 · see citing works
Self-citationCytology and functionally correlated circuits of human posterior cingulate areas
Vogt, B. A., Vogt, L., & Laureys, S. (2006) · NeuroImage · doi:10.1016/j.neuroimage.2005.07.048 · Cited by 484 · see citing works
Recollective qualities modulate hippocampal activation during autobiographical memory retrieval
Addis, D. R., Moscovitch, M., Crawley, A. P., & McAndrews, M. P. (2004) · Hippocampus · doi:10.1002/hipo.10215 · Cited by 383 · see citing works
Memory for events and their spatial context: models and experiments
Burgess, N., Becker, S., King, J. A., & O'Keefe, J. (2001) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.2001.0948 · Cited by 377 · see citing works
Self-citationAutobiographical and episodic memory—one and the same?
Gilboa, A. (2004) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2004.02.014 · Cited by 367 · see citing works
Viewpoint-Specific Scene Representations in Human Parahippocampal Cortex
Epstein, R., Graham, K. S., & Downing, P. E. (2003) · Neuron · doi:10.1016/s0896-6273(03)00117-x · Cited by 360 · see citing works
Where am I now? Distinct roles for parahippocampal and retrosplenial cortices in place recognition
Epstein, R. A., Parker, W. E., & Feiler, A. M. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.0799-07.2007 · Cited by 331 · see citing works
Howard, M. W., Fotedar, M. S., Datey, A. V., & Hasselmo, M. E. (2005) · Psychological Review · doi:10.1037/0033-295x.112.1.75 · Cited by 283 · see citing works
van Reekum, C. M., Johnstone, T., Urry, H. L., Thurow, M. E., Schaefer, H. S., Alexander, A. L., & Davidson, R. J. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.03.052 · Cited by 271 · see citing works
Ekstrom, A. D., Arnold, A. E. G. F., & Iaria, G. (2014) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2014.00803 · Cited by 263 · see citing works
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A neural-level model of spatial memory and imagery
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Self-citationWeniger, G., Ruhleder, M., Lange, C., Wolf, S., & Irle, E. (2011) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2010.12.031 · Cited by 204 · see citing works
The role of visual experience for the neural basis of spatial cognition
Pasqualotto, A., & Proulx, M. J. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.01.008 · Cited by 192 · see citing works
Neuronal vector coding in spatial cognition
Bicanski, A., & Burgess, N. (2020) · Nature Reviews Neuroscience · doi:10.1038/s41583-020-0336-9 · Cited by 172 · see citing works
Self-citationLevine, B. (2004) · Brain and Cognition · doi:10.1016/s0278-2626(03)00280-x · Cited by 189 · see citing works
Sugiura, M., Shah, N. J., Zilles, K., & Fink, G. R. (2005) · Journal of Cognitive Neuroscience · doi:10.1162/0898929053124956 · Cited by 167 · see citing works
Two distinct scene processing networks connecting vision and memory
Baldassano, C., Esteva, A., Fei-Fei, L., & Beck, D. M. (2016) · eneuro · doi:10.1523/eneuro.0178-16.2016 · Cited by 144 · see citing works
Visual Scene Processing in Familiar and Unfamiliar Environments
Epstein, R. A., Higgins, J. S., Jablonski, K., & Feiler, A. M. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00003.2007 · Cited by 153 · see citing works
Self-awareness and the left inferior frontal gyrus: Inner speech use during self-related processing
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Anterior hippocampus and goal-directed spatial decision making
Viard, A., Doeller, C. F., Hartley, T., Bird, C. M., & Burgess, N. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.4640-10.2011 · Cited by 144 · see citing works
Self-citationNeural correlates of social cognition in naturalistic settings: a model-free analysis approach
Wolf, I., Dziobek, I., & Heekeren, H. R. (2010) · NeuroImage · doi:10.1016/j.neuroimage.2009.08.060 · Cited by 137 · see citing works
Dissociable networks involved in spatial and temporal order source retrieval
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Imagining Being Somewhere Else: Neural Basis of Changing Perspective in Space
Lambrey, S., Doeller, C., Berthoz, A., & Burgess, N. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhr101 · Cited by 130 · see citing works
Self-citationMultiple interacting brain areas underlie successful spatiotemporal memory retrieval in humans
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Self-citationNeural correlates of automatic mood regulation in girls at high risk for depression.
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The Use of Virtual Reality for Episodic Memory Assessment: Effects of Active Navigation
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First-person view of one’s body in immersive virtual reality: Influence on episodic memory
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Impaired allocentric spatial memory underlying topographical disorientation
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Hippocampal volume reduction and autobiographical memory deficits in chronic schizophrenia
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Identifying with fictive characters: structural brain correlates of the personality trait ‘fantasy’
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Decoding episodic autobiographical memory in naturalistic virtual reality
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- Authors
- Burgess, N., Maguire, E. A., Spiers, H. J., & O'Keefe, J.
- Affiliations
- University College London (GB)
- UCL Queen Square Institute of Neurology (GB)
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2001-08
- Volume
- 14
- Issue
- 2
- Pages
- 439-453
- ISSN
- 1053-8119 (ISSN-L)
- OpenAlex
- W2101418508
- Cited by
- 502
- References
- 105
- Citations by year
- 2026: 4 · 2025: 9 · 2024: 14 · 2023: 14 · 2022: 9 · 2021: 10 · 2020: 16 · 2019: 15 · 2018: 25 · 2017: 16 · 2016: 20 · 2015: 21 · 2014: 18 · 2013: 23 · 2012: 26
- FWCI
- 12.40
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- NeuroImage (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Royal Society
- Medical Research Council
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
- Keywords
- event memory, virtual reality, precuneus, parahippocampal cortex, posterior parietal cortex, hippocampus, prefrontal cortex, anterior cingulate cortex, allocentric spatial representation, strategic retrieval
- MeSH terms
- Adult, Brain Mapping, Dominance, Cerebral, Female, Gyrus Cinguli, Humans, Magnetic Resonance Imaging, Male, Nerve Net, Orientation, Parietal Lobe, Pattern Recognition, Visual, Mental Recall, Reference Values, Retention, Psychology, Temporal Lobe, User-Computer Interface, Visual Perception, Prefrontal Cortex, Parahippocampal Gyrus
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