Hotspot of human verbal memory encoding in the left anterior prefrontal cortex.


Journal

EBioMedicine
ISSN: 2352-3964
Titre abrégé: EBioMedicine
Pays: Netherlands
ID NLM: 101647039

Informations de publication

Date de publication:
Aug 2022
Historique:
received: 13 08 2021
revised: 31 05 2022
accepted: 14 06 2022
pubmed: 6 7 2022
medline: 17 8 2022
entrez: 5 7 2022
Statut: ppublish

Résumé

Treating memory and cognitive deficits requires knowledge about anatomical sites and neural activities to be targeted with particular therapies. Emerging technologies for local brain stimulation offer attractive therapeutic options but need to be applied to target specific neural activities, at distinct times, and in specific brain regions that are critical for memory formation. The areas that are critical for successful encoding of verbal memory as well as the underlying neural activities were determined directly in the human brain with intracranial electrophysiological recordings in epilepsy patients. We recorded a broad range of spectral activities across the cortex of 135 patients as they memorised word lists for subsequent free recall. The greatest differences in the spectral power between encoding subsequently recalled and forgotten words were found in low theta frequency (3-5 Hz) activities of the left anterior prefrontal cortex. This subsequent memory effect was proportionally greater in the lower frequency bands and in the more anterior cortical regions. We found the peak of this memory signal in a distinct part of the prefrontal cortex at the junction between the Broca's area and the frontal pole. The memory effect in this confined area was significantly higher (Tukey-Kramer test, p<0.05) than in other anatomically distinct areas. Our results suggest a focal hotspot of human verbal memory encoding located in the higher-order processing region of the prefrontal cortex, which presents a prospective target for modulating cognitive functions in the human patients. The memory effect provides an electrophysiological biomarker of low frequency neural activities, at distinct times of memory encoding, and in one hotspot location in the human brain. Open-access datasets were originally collected as part of a BRAIN Initiative project called Restoring Active Memory (RAM) funded by the Defence Advanced Research Project Agency (DARPA). CT, ML, MTK and this research were supported from the First Team grant of the Foundation for Polish Science co-financed by the European Union under the European Regional Development Fund.

Sections du résumé

BACKGROUND BACKGROUND
Treating memory and cognitive deficits requires knowledge about anatomical sites and neural activities to be targeted with particular therapies. Emerging technologies for local brain stimulation offer attractive therapeutic options but need to be applied to target specific neural activities, at distinct times, and in specific brain regions that are critical for memory formation.
METHODS METHODS
The areas that are critical for successful encoding of verbal memory as well as the underlying neural activities were determined directly in the human brain with intracranial electrophysiological recordings in epilepsy patients. We recorded a broad range of spectral activities across the cortex of 135 patients as they memorised word lists for subsequent free recall.
FINDINGS RESULTS
The greatest differences in the spectral power between encoding subsequently recalled and forgotten words were found in low theta frequency (3-5 Hz) activities of the left anterior prefrontal cortex. This subsequent memory effect was proportionally greater in the lower frequency bands and in the more anterior cortical regions. We found the peak of this memory signal in a distinct part of the prefrontal cortex at the junction between the Broca's area and the frontal pole. The memory effect in this confined area was significantly higher (Tukey-Kramer test, p<0.05) than in other anatomically distinct areas.
INTERPRETATION CONCLUSIONS
Our results suggest a focal hotspot of human verbal memory encoding located in the higher-order processing region of the prefrontal cortex, which presents a prospective target for modulating cognitive functions in the human patients. The memory effect provides an electrophysiological biomarker of low frequency neural activities, at distinct times of memory encoding, and in one hotspot location in the human brain.
FUNDING BACKGROUND
Open-access datasets were originally collected as part of a BRAIN Initiative project called Restoring Active Memory (RAM) funded by the Defence Advanced Research Project Agency (DARPA). CT, ML, MTK and this research were supported from the First Team grant of the Foundation for Polish Science co-financed by the European Union under the European Regional Development Fund.

Identifiants

pubmed: 35785617
pii: S2352-3964(22)00316-4
doi: 10.1016/j.ebiom.2022.104135
pmc: PMC9254338
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

104135

Informations de copyright

Copyright © 2022 The Authors. Published by Elsevier B.V. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare that they have no competing interests.

Auteurs

Çağdaş Topçu (Ç)

Gdansk University of Technology, Faculty of Electronics, Telecommunications and Informatics, Multimedia Systems Department, BioTechMed Center, Gdansk, Poland; Department of Neurology, Mayo Clinic, Rochester, MN, USA; Laboratory of Neuroinformatics, Nencki Institute of Experimental Biology of the Polish Academy of Sciences, Warsaw, Poland.

Victoria S Marks (VS)

Graduate School of Biomedical Sciences, Mayo Clinic, USA.

Krishnakant V Saboo (KV)

University of Illinois, Department of Electrical and Computer Engineering, Urbana-Champaign IL, USA.

Michał Lech (M)

Gdansk University of Technology, Faculty of Electronics, Telecommunications and Informatics, Multimedia Systems Department, BioTechMed Center, Gdansk, Poland; Department of Neurology, Mayo Clinic, Rochester, MN, USA.

Petr Nejedly (P)

Department of Neurology, Mayo Clinic, Rochester, MN, USA.

Vaclav Kremen (V)

Department of Neurology, Mayo Clinic, Rochester, MN, USA; Czech Institute of Informatics, Robotics, and Cybernetics, Czech Technical University in Prague, Prague, Czech Republic.

Gregory A Worrell (GA)

Department of Neurology, Mayo Clinic, Rochester, MN, USA; Department of Physiology and Biomedical Engineering, Mayo Clinic, USA.

Michal T Kucewicz (MT)

Gdansk University of Technology, Faculty of Electronics, Telecommunications and Informatics, Multimedia Systems Department, BioTechMed Center, Gdansk, Poland; Department of Neurology, Mayo Clinic, Rochester, MN, USA; Department of Physiology and Biomedical Engineering, Mayo Clinic, USA. Electronic address: michal.kucewicz@pg.edu.pl.

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