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Research Articles, Behavioral/Cognitive

Holistic Recollection via Pattern Completion Involves Hippocampal Subfield CA3

Xenia Grande, David Berron, Aidan J. Horner, James A. Bisby, Emrah Düzel and Neil Burgess
Journal of Neuroscience 9 October 2019, 39 (41) 8100-8111; DOI: https://doi.org/10.1523/JNEUROSCI.0722-19.2019
Xenia Grande
1German Center for Neurodegenerative Diseases, 39120 Magdeburg, Germany,
2Institute of Cognitive Neurology and Dementia Research, Otto-von-Guericke University Magdeburg, 39120 Magdeburg, Germany,
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David Berron
1German Center for Neurodegenerative Diseases, 39120 Magdeburg, Germany,
2Institute of Cognitive Neurology and Dementia Research, Otto-von-Guericke University Magdeburg, 39120 Magdeburg, Germany,
6Clinical Memory Research Unit, Department of Clinical Sciences Malmö, Lund University, 223 62 Lund, Sweden,
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Aidan J. Horner
7Department of Psychology, University of York YO10 5DD, United Kingdom, and
8York Biomedical Research Institute, University of York YO10 5DD, United Kingdom
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James A. Bisby
3Institute of Cognitive Neuroscience, University College London, London WC1N 3AZ, United Kingdom,
4UCL Queen Square Institute of Neurology, University College London, London WC1N 3BG, United Kingdom,
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Emrah Düzel
1German Center for Neurodegenerative Diseases, 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, London WC1N 3AZ, United Kingdom,
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Neil Burgess
3Institute of Cognitive Neuroscience, University College London, London WC1N 3AZ, United Kingdom,
4UCL Queen Square Institute of Neurology, University College London, London WC1N 3BG, United Kingdom,
5Wellcome Trust Centre for Human Neuroimaging, University College London, London WC1N 3AR, United Kingdom,
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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 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, although 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.

  • 7 T fMRI
  • hippocampal subfields
  • medial temporal lobe
  • memory
  • pattern completion
  • recollection

This is an open-access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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The Journal of Neuroscience: 39 (41)
Journal of Neuroscience
Vol. 39, Issue 41
9 Oct 2019
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Holistic Recollection via Pattern Completion Involves Hippocampal Subfield CA3
Xenia Grande, David Berron, Aidan J. Horner, James A. Bisby, Emrah Düzel, Neil Burgess
Journal of Neuroscience 9 October 2019, 39 (41) 8100-8111; DOI: 10.1523/JNEUROSCI.0722-19.2019

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Holistic Recollection via Pattern Completion Involves Hippocampal Subfield CA3
Xenia Grande, David Berron, Aidan J. Horner, James A. Bisby, Emrah Düzel, Neil Burgess
Journal of Neuroscience 9 October 2019, 39 (41) 8100-8111; DOI: 10.1523/JNEUROSCI.0722-19.2019
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Keywords

  • 7 T fMRI
  • hippocampal subfields
  • medial temporal lobe
  • memory
  • pattern completion
  • recollection

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