Developing a hippocampal neural prosthetic to facilitate human memory encoding and recall of stimulus features and categories.

CA1 CA3 cognition neurophysiology nonlinear prosthetic

Journal

Frontiers in computational neuroscience
ISSN: 1662-5188
Titre abrégé: Front Comput Neurosci
Pays: Switzerland
ID NLM: 101477956

Informations de publication

Date de publication:
2024
Historique:
received: 19 07 2023
accepted: 19 01 2024
medline: 23 2 2024
pubmed: 23 2 2024
entrez: 23 2 2024
Statut: epublish

Résumé

Here, we demonstrate the first successful use of static neural stimulation patterns for specific information content. These static patterns were derived by a model that was applied to a subject's own hippocampal spatiotemporal neural codes for memory. We constructed a new model of processes by which the hippocampus encodes specific memory items via spatiotemporal firing of neural ensembles that underlie the successful encoding of targeted content into short-term memory. A memory decoding model (MDM) of hippocampal CA3 and CA1 neural firing was computed which derives a stimulation pattern for CA1 and CA3 neurons to be applied during the encoding (sample) phase of a delayed match-to-sample (DMS) human short-term memory task. MDM electrical stimulation delivered to the CA1 and CA3 locations in the hippocampus during the sample phase of DMS trials facilitated memory of images from the DMS task during a delayed recognition (DR) task that also included control images that were not from the DMS task. Across all subjects, the stimulated trials exhibited significant changes in performance in 22.4% of patient and category combinations. Changes in performance were a combination of both increased memory performance and decreased memory performance, with increases in performance occurring at almost 2 to 1 relative to decreases in performance. Across patients with impaired memory that received bilateral stimulation, significant changes in over 37.9% of patient and category combinations was seen with the changes in memory performance show a ratio of increased to decreased performance of over 4 to 1. Modification of memory performance was dependent on whether memory function was intact or impaired, and if stimulation was applied bilaterally or unilaterally, with nearly all increase in performance seen in subjects with impaired memory receiving bilateral stimulation. These results demonstrate that memory encoding in patients with impaired memory function can be facilitated for specific memory content, which offers a stimulation method for a future implantable neural prosthetic to improve human memory.

Identifiants

pubmed: 38390007
doi: 10.3389/fncom.2024.1263311
pmc: PMC10881797
doi:

Types de publication

Journal Article

Langues

eng

Pagination

1263311

Informations de copyright

Copyright © 2024 Roeder, She, Dakos, Moore, Wicks, Witcher, Couture, Laxton, Clary, Popli, Liu, Lee, Heck, Nune, Gong, Shaw, Marmarelis, Berger, Deadwyler, Song and Hampson.

Déclaration de conflit d'intérêts

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The reviewer SS declared a shared affiliation with the author XS to the handling editor at the time of review.

Auteurs

Brent M Roeder (BM)

Wake Forest Baptist Medical Center, Winston-Salem, NC, United States.

Xiwei She (X)

Department of Biomedical Engineering, University of Southern California, Los Angeles, CA, United States.

Alexander S Dakos (AS)

Wake Forest Baptist Medical Center, Winston-Salem, NC, United States.

Bryan Moore (B)

Department of Biomedical Engineering, University of Southern California, Los Angeles, CA, United States.

Robert T Wicks (RT)

Wake Forest Baptist Medical Center, Winston-Salem, NC, United States.
Johns Hopkins Children's Center, Baltimore, MD, United States.

Mark R Witcher (MR)

Wake Forest Baptist Medical Center, Winston-Salem, NC, United States.
Virginia Tech Carilion School of Medicine and Research Institute, Roanoke, VA, United States.

Daniel E Couture (DE)

Wake Forest Baptist Medical Center, Winston-Salem, NC, United States.

Adrian W Laxton (AW)

Wake Forest Baptist Medical Center, Winston-Salem, NC, United States.

Heidi Munger Clary (HM)

Wake Forest Baptist Medical Center, Winston-Salem, NC, United States.

Gautam Popli (G)

Wake Forest Baptist Medical Center, Winston-Salem, NC, United States.

Charles Liu (C)

Department of Biomedical Engineering, University of Southern California, Los Angeles, CA, United States.
USC Keck Memorial Hospital, Los Angeles, CA, United States.

Brian Lee (B)

USC Keck Memorial Hospital, Los Angeles, CA, United States.

Christianne Heck (C)

Department of Biomedical Engineering, University of Southern California, Los Angeles, CA, United States.
USC Keck Memorial Hospital, Los Angeles, CA, United States.

George Nune (G)

USC Keck Memorial Hospital, Los Angeles, CA, United States.

Hui Gong (H)

Rancho Los Amigos National Rehabilitation Hospital, Los Angeles, CA, United States.

Susan Shaw (S)

Rancho Los Amigos National Rehabilitation Hospital, Los Angeles, CA, United States.

Vasilis Z Marmarelis (VZ)

Department of Biomedical Engineering, University of Southern California, Los Angeles, CA, United States.

Theodore W Berger (TW)

Department of Biomedical Engineering, University of Southern California, Los Angeles, CA, United States.

Sam A Deadwyler (SA)

Wake Forest Baptist Medical Center, Winston-Salem, NC, United States.

Dong Song (D)

Department of Biomedical Engineering, University of Southern California, Los Angeles, CA, United States.

Robert E Hampson (RE)

Wake Forest Baptist Medical Center, Winston-Salem, NC, United States.

Classifications MeSH