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The hippocampus as the switchboard between perception and memory

Matthias S. Treder, Ian Charest, Sebastian Michelmann, View ORCID ProfileMaría Carmen Martín-Buro, Frédéric Roux, Fernando Carceller-Benito, Arturo Ugalde-Canitrot, David T. Rollings, Vijay Sawlani, Ramesh Chelvarajah, Maria Wimber, Simon Hanslmayr, View ORCID ProfileBernhard P. Staresina
doi: https://doi.org/10.1101/2020.05.20.104539
Matthias S. Treder
1School of Computer Science and Informatics, Cardiff University, UK
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Ian Charest
2School of Psychology and Centre for Human Brain Health, University of Birmingham, Birmingham, UK
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Sebastian Michelmann
3Princeton Neuroscience Institute and Department of Psychology, Princeton University, Princeton, USA
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María Carmen Martín-Buro
4Laboratory of Cognitive and Computational Neuroscience, Center for Biomedical Technology, Madrid, Spain
5Faculty of Health Sciences, King Juan Carlos University, Madrid, Spain
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  • ORCID record for María Carmen Martín-Buro
Frédéric Roux
2School of Psychology and Centre for Human Brain Health, University of Birmingham, Birmingham, UK
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Fernando Carceller-Benito
6Neurosurgery Service, Hospital Universitario La Paz, Madrid, Spain
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Arturo Ugalde-Canitrot
7Epilepsy Monitoring Unit, Neurology and Clinical Neurophysiology Service, Hospital Universitario La Paz, Madrid, Spain
8School of Medicine, Universidad Francisco de Vitoria, Madrid, Spain
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David T. Rollings
2School of Psychology and Centre for Human Brain Health, University of Birmingham, Birmingham, UK
9Complex Epilepsy and Surgery Service, Neurophysiology Department, Queen Elizabeth Hospital, Birmingham, UK
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Vijay Sawlani
2School of Psychology and Centre for Human Brain Health, University of Birmingham, Birmingham, UK
10Complex Epilepsy and Surgery Service, Neuroradiology Department, Queen Elizabeth Hospital, Birmingham,UK
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Ramesh Chelvarajah
2School of Psychology and Centre for Human Brain Health, University of Birmingham, Birmingham, UK
11Complex Epilepsy and Surgery Service, Neurosurgery Department, Queen Elizabeth Hospital, Birmingham, UK
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Maria Wimber
12Institute of Neuroscience and Psychology, University of Glasgow, UK
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Simon Hanslmayr
12Institute of Neuroscience and Psychology, University of Glasgow, UK
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Bernhard P. Staresina
2School of Psychology and Centre for Human Brain Health, University of Birmingham, Birmingham, UK
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  • ORCID record for Bernhard P. Staresina
  • For correspondence: b.staresina@bham.ac.uk
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Abstract

Adaptive memory recall requires a rapid and flexible switch from external perceptual reminders to internal mnemonic representations. However, owing to the limited temporal or spatial resolution of brain imaging modalities used in isolation, the hippocampal-cortical dynamics supporting this process remain unknown. We thus employed an object-scene cued recall paradigm across two studies, including intracranial Electroencephalography (iEEG) and high-density scalp EEG. First, a sustained increase in hippocampal high gamma power (60-110 Hz) emerged 500 ms after cue onset and distinguished successful vs. unsuccessful recall. This increase in gamma power for successful recall was followed by a decrease in hippocampal alpha power (8-12 Hz). Intriguingly, the hippocampal gamma power increase marked the moment at which extrahippocampal activation patterns shifted from perceptual cue towards mnemonic target representations. In parallel, source-localised EEG alpha power revealed that the recall signal progresses from hippocampus to posterior parietal cortex and then to medial prefrontal cortex. Together, these results identify the hippocampus as the switchboard between perception and memory and elucidate the ensuing hippocampal-cortical dynamics supporting the recall process.

Significance How do we adaptively switch from perceiving the external world to retrieving goal-relevant internal memories? To tackle this question, we used – in a cued-recall paradigm - direct intracranial recordings from the human hippocampus complemented by high-density scalp Electroencephalography (EEG). We found that a hippocampal signal ~500 ms after a perceptual cue marks the conversion from external (perceptual) to internal (mnemonic) representations. This sets in motion a recall cascade involving posterior parietal and medial prefrontal cortex, revealed via source-localised and time-resolved EEG alpha power. Together, these results unveil the hippocampal-cortical dynamics supporting rapid and flexible memory recall.

Competing Interest Statement

The authors have declared no competing interest.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted April 06, 2021.
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The hippocampus as the switchboard between perception and memory
Matthias S. Treder, Ian Charest, Sebastian Michelmann, María Carmen Martín-Buro, Frédéric Roux, Fernando Carceller-Benito, Arturo Ugalde-Canitrot, David T. Rollings, Vijay Sawlani, Ramesh Chelvarajah, Maria Wimber, Simon Hanslmayr, Bernhard P. Staresina
bioRxiv 2020.05.20.104539; doi: https://doi.org/10.1101/2020.05.20.104539
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The hippocampus as the switchboard between perception and memory
Matthias S. Treder, Ian Charest, Sebastian Michelmann, María Carmen Martín-Buro, Frédéric Roux, Fernando Carceller-Benito, Arturo Ugalde-Canitrot, David T. Rollings, Vijay Sawlani, Ramesh Chelvarajah, Maria Wimber, Simon Hanslmayr, Bernhard P. Staresina
bioRxiv 2020.05.20.104539; doi: https://doi.org/10.1101/2020.05.20.104539

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