Holistic recollection via pattern completion involves hippocampal subfield CA3
- Xenia Grande1,2,
- David Berron1,2,6,
- Aidan J. Horner7,8,
- James A. Bisby3,4,
- Emrah Düzel1,2,3, and
- Neil Burgess3,4,5
- 1German Center for Neurodegenerative Diseases (DZNE), 39120 Magdeburg, Germany
- 2Institute of Cognitive Neurology and Dementia Research, Otto-von-Guericke University Magdeburg, 39120 Magdeburg, Germany
- 3Institute of Cognitive Neuroscience, University College London, 17 Queen Square, London WC1N 3AZ, UK
- 4UCL Queen Square Institute of Neurology, University College London, Queen Square, London WC1N 3BG, UK
- 5Wellcome Trust Centre for Human Neuroimaging, University College London, 12 Queen Square, London WC1N 3AR, UK
- 6Clinical Memory Research Unit, Department of Clinical Sciences Malmö, Lund University, 223 62 Lund, Sweden
- 7Department of Psychology, University of York YO10 5DD, UK
- 8York Biomedical Research Institute, University of York YO10 5DD, UK
- Corresponding author: Xenia Grande (xenia.grande{at}dzne.de)
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Author contributions: X.G., D.B., A.H., J.A.B., and E.D. designed research; X.G. and N.B. performed research; X.G. analyzed data; X.G. wrote the first draft of the paper; X.G., D.B., A.H., J.A.B., E.D., and N.B. edited the paper; X.G. wrote the paper; D.B. and A.H. contributed unpublished reagents/analytic tools.
Abstract
Episodic memories typically comprise multiple elements. A defining characteristic of episodic retrieval is holistic recollection, i.e. comprehensive recall of the elements a memorized event encompasses. A recent study implicated activity in the human hippocampus with holistic recollection of multi-element events based on cues (Horner, Bisby, Bush, Lin, & Burgess et al., 2015). Here, we obtained ultra-high resolution functional neuroimaging data at 7 Tesla in 30 younger adults (12 female) using the same paradigm. In accordance with anatomically inspired computational models and animal research, we found that metabolic activity in hippocampal subfield CA3 (but less pronounced in dentate gyrus) correlated with this form of mnemonic pattern completion across participants. Our study provides the first evidence in humans for a strong involvement of hippocampal subfield CA3 in holistic recollection via pattern completion.
SIGNIFICANCE STATEMENT
Memories of daily events usually involve multiple elements, while a single element can be sufficient to prompt recollection of the whole event. Such holistic recollection is thought to require reactivation of brain activity representing the full event from one event element (‘pattern completion’). Computational and animal models suggest that mnemonic pattern completion is accomplished in a specific subregion of the hippocampus called CA3, but empirical evidence in humans was lacking. Here, we leverage the ultra-high resolution of 7 Tesla neuroimaging to provide first evidence for a strong involvement of the human CA3 in holistic recollection of multi-element events via pattern completion.
Footnotes
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The authors declare no competing financial interests.
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We thank the Leibniz Institute for Neurobiology in Magdeburg for providing access to the 7 Tesla MR Scanner. This project has received funding from the European Union's Horizon 2020 Research and Innovation Programme under Grant Agreement No. 720270 (HBP SGA1) and Grant Agreement No. 785907 (HBP SGA2). Additional funding was received from the Wellcome Trust (for NB 202805/Z/16/Z and for AJH 204277/Z/16/Z). AJH was moreover supported by ESRC (ES/R007454/1).
- Received March 29, 2019.
- Revision received July 11, 2019.
- Accepted July 14, 2019.
- Copyright © 2019 Grande et al.
This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
