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Long-term consolidation switches goal proximity coding from hippocampus to retrosplenial cortex

E. Zita Patai, Amir-Homayoun Javadi, Jason D. Ozubko, Andrew O’Callaghan, Shuman Ji, Jessica Robin, Cheryl Grady, Gordon Winocur, Shayna R. Rosenbaum, Morris Moscovitch, Hugo J. Spiers
doi: https://doi.org/10.1101/167882
E. Zita Patai
1Institute of Behavioural Neuroscience, University College London, London, UK
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Amir-Homayoun Javadi
1Institute of Behavioural Neuroscience, University College London, London, UK
2School of Psychology, University of Kent, Canterbury, UK
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Jason D. Ozubko
3Department of Psychology, SUNY Geneseo, Geneseo New York, USA
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Andrew O’Callaghan
1Institute of Behavioural Neuroscience, University College London, London, UK
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Shuman Ji
4Institute of Cognitive Neuroscience, University College London, London, UK
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Jessica Robin
5Department of Psychology, University of Toronto, Toronto, Canada
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Cheryl Grady
5Department of Psychology, University of Toronto, Toronto, Canada
6Rotman Research Institute, Baycrest Centre, University of Toronto, Toronto, Canada
8Department of Psychology, Trent University, Peterborough, Canada
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Gordon Winocur
5Department of Psychology, University of Toronto, Toronto, Canada
6Rotman Research Institute, Baycrest Centre, University of Toronto, Toronto, Canada
8Department of Psychology, Trent University, Peterborough, Canada
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Shayna R. Rosenbaum
7Department of Psychology, York University, Toronto, Canada
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Morris Moscovitch
5Department of Psychology, University of Toronto, Toronto, Canada
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Hugo J. Spiers
1Institute of Behavioural Neuroscience, University College London, London, UK
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  • For correspondence: h.spiers@ucl.ac.uk
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Abstract

Recent research indicates the hippocampus may code the distance to the goal during navigation of newly learned environments. It is unclear however, whether this also pertains to highly familiar environments where extensive systems-level consolidation is thought to have transformed mnemonic representations. Here we recorded fMRI while University College London and Imperial College London students navigated virtual simulations of their own familiar campus (> 2 years of exposure) and the other campus learned days before scanning. Posterior hippocampal activity tracked the proximity to the goal in the newly learned campus, but not in the familiar campus. By contrast retrosplenial cortex tracked the distance to the goal in the familiar campus, but not in the recently learned campus. These responses were abolished when participants were guided to their goal by external cues. These results open new avenues of research on navigation and consolidation of spatial information and help advance models of how neural circuits support navigation in novel and highly familiar environments.

Significance Statement Historically, research on the hippocampal formation has focused on its role in long-term memory and navigation – often in isolation. No study to date has directly compared realistic navigation within familiar with recently learned environments, nor has it been explored how the neural substrates, along with computational codes, may change. In this study, we show for the first time, a shift from hippocampal to cortical coding of distance to a goal during active navigation. This study bridges the gap between memory consolidation and navigation, and paves the way for more functional and realistic understanding of the hippocampus.

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Posted July 25, 2017.
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Long-term consolidation switches goal proximity coding from hippocampus to retrosplenial cortex
E. Zita Patai, Amir-Homayoun Javadi, Jason D. Ozubko, Andrew O’Callaghan, Shuman Ji, Jessica Robin, Cheryl Grady, Gordon Winocur, Shayna R. Rosenbaum, Morris Moscovitch, Hugo J. Spiers
bioRxiv 167882; doi: https://doi.org/10.1101/167882
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Long-term consolidation switches goal proximity coding from hippocampus to retrosplenial cortex
E. Zita Patai, Amir-Homayoun Javadi, Jason D. Ozubko, Andrew O’Callaghan, Shuman Ji, Jessica Robin, Cheryl Grady, Gordon Winocur, Shayna R. Rosenbaum, Morris Moscovitch, Hugo J. Spiers
bioRxiv 167882; doi: https://doi.org/10.1101/167882

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