Brent M. Roeder, Xiwei She, Alexander S. Dakos, Bryan Moore, Robert T. Wicks, Mark R. Witcher, Daniel E. Couture, Adrian W. Laxton, Heidi Munger Clary, Gautam Popli, Charles Liu, Brian Lee, Christianne Heck, George Nune, Hui Gong, Susan Shaw, Vasilis Z. Marmarelis, Theodore W. Berger, Sam A. Deadwyler, Dong Song, Robert E. Hampson
{"title":"Developing a hippocampal neural prosthetic to facilitate human memory encoding and recall of stimulus features and categories","authors":"Brent M. Roeder, Xiwei She, Alexander S. Dakos, Bryan Moore, Robert T. Wicks, Mark R. Witcher, Daniel E. Couture, Adrian W. Laxton, Heidi Munger Clary, Gautam Popli, Charles Liu, Brian Lee, Christianne Heck, George Nune, Hui Gong, Susan Shaw, Vasilis Z. Marmarelis, Theodore W. Berger, Sam A. Deadwyler, Dong Song, Robert E. Hampson","doi":"10.3389/fncom.2024.1263311","DOIUrl":null,"url":null,"abstract":"ObjectiveHere, 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.ApproachWe 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.Main resultsMDM 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.SignificanceThese 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.","PeriodicalId":12363,"journal":{"name":"Frontiers in Computational Neuroscience","volume":"20 1","pages":""},"PeriodicalIF":2.1000,"publicationDate":"2024-02-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Frontiers in Computational Neuroscience","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.3389/fncom.2024.1263311","RegionNum":4,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"MATHEMATICAL & COMPUTATIONAL BIOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
ObjectiveHere, 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.ApproachWe 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.Main resultsMDM 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.SignificanceThese 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.
期刊介绍:
Frontiers in Computational Neuroscience is a first-tier electronic journal devoted to promoting theoretical modeling of brain function and fostering interdisciplinary interactions between theoretical and experimental neuroscience. Progress in understanding the amazing capabilities of the brain is still limited, and we believe that it will only come with deep theoretical thinking and mutually stimulating cooperation between different disciplines and approaches. We therefore invite original contributions on a wide range of topics that present the fruits of such cooperation, or provide stimuli for future alliances. We aim to provide an interactive forum for cutting-edge theoretical studies of the nervous system, and for promulgating the best theoretical research to the broader neuroscience community. Models of all styles and at all levels are welcome, from biophysically motivated realistic simulations of neurons and synapses to high-level abstract models of inference and decision making. While the journal is primarily focused on theoretically based and driven research, we welcome experimental studies that validate and test theoretical conclusions.
Also: comp neuro