Mapping eye, arm, and reward information in frontal motor cortices using electrocorticography in non-human primates.

IF 4.4 2区 医学 Q1 NEUROSCIENCES Journal of Neuroscience Pub Date : 2025-01-31 DOI:10.1523/JNEUROSCI.1536-24.2025
Tomohiro Ouchi, Leo R Scholl, Pavithra Rajeswaran, Ryan A Canfield, Lydia I Smith, Amy L Orsborn
{"title":"Mapping eye, arm, and reward information in frontal motor cortices using electrocorticography in non-human primates.","authors":"Tomohiro Ouchi, Leo R Scholl, Pavithra Rajeswaran, Ryan A Canfield, Lydia I Smith, Amy L Orsborn","doi":"10.1523/JNEUROSCI.1536-24.2025","DOIUrl":null,"url":null,"abstract":"<p><p>Goal-directed reaches give rise to dynamic neural activity across the brain as we move our eyes and arms, and process outcomes. High spatiotemporal resolution mapping of multiple cortical areas will improve our understanding of how these neural computations are spatially and temporally distributed across the brain. In this study, we used micro-electrocorticography (µECoG) recordings in two male monkeys performing visually guided reaches to map information related to eye movements, arm movements, and receiving rewards over primary motor cortex, premotor cortex, frontal eye field, and dorsolateral pre-frontal cortex. Time-frequency and decoding analyses revealed that eye and arm movement information shifts across brain regions during a reach, likely reflecting shifts from planning to execution. Although eye and arm movement temporally overlapped, phase clustering analyses enabled us to resolve differences in eye and arm information across brain regions. This analysis revealed that eye and arm information spatially overlapped in motor cortex, which we further confirmed by demonstrating that arm movement decoding performance from motor cortex activity was impacted by task-irrelevant eye movements. Phase clustering analyses also identified reward-related activity in the pre-frontal and premotor cortex. Our results demonstrate µECoG's strengths for functional mapping and provide further detail on the spatial distribution of eye, arm, and reward information processing distributed across frontal cortices during reaching. These insights advance our understanding of the overlapping neural computations underlying coordinated movements and reveal opportunities to leverage these signals to enhance future brain-computer interfaces.<b>Significance statement</b> Picking up your coffee mug requires coordinating movements of your eyes and hand and processing the outcomes of those movements. Mapping how neural activity relates to different functions helps us understand how the brain performs these computations. Many mapping techniques have limited spatial or temporal resolution, restricting our ability to dissect computations that overlap closely in space and time. We used micro-electrocorticography recordings to map neural activity across multiple cortical areas while monkeys made goal-directed reaches. These measurements revealed high spatial and temporal resolution maps of neural activity related to eye, arm, and reward information processing. These maps reveal overlapping neural computations underlying movement and open opportunities to use eye and reward information to improve therapies to restore motor function.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.4000,"publicationDate":"2025-01-31","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Neuroscience","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1523/JNEUROSCI.1536-24.2025","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
引用次数: 0

Abstract

Goal-directed reaches give rise to dynamic neural activity across the brain as we move our eyes and arms, and process outcomes. High spatiotemporal resolution mapping of multiple cortical areas will improve our understanding of how these neural computations are spatially and temporally distributed across the brain. In this study, we used micro-electrocorticography (µECoG) recordings in two male monkeys performing visually guided reaches to map information related to eye movements, arm movements, and receiving rewards over primary motor cortex, premotor cortex, frontal eye field, and dorsolateral pre-frontal cortex. Time-frequency and decoding analyses revealed that eye and arm movement information shifts across brain regions during a reach, likely reflecting shifts from planning to execution. Although eye and arm movement temporally overlapped, phase clustering analyses enabled us to resolve differences in eye and arm information across brain regions. This analysis revealed that eye and arm information spatially overlapped in motor cortex, which we further confirmed by demonstrating that arm movement decoding performance from motor cortex activity was impacted by task-irrelevant eye movements. Phase clustering analyses also identified reward-related activity in the pre-frontal and premotor cortex. Our results demonstrate µECoG's strengths for functional mapping and provide further detail on the spatial distribution of eye, arm, and reward information processing distributed across frontal cortices during reaching. These insights advance our understanding of the overlapping neural computations underlying coordinated movements and reveal opportunities to leverage these signals to enhance future brain-computer interfaces.Significance statement Picking up your coffee mug requires coordinating movements of your eyes and hand and processing the outcomes of those movements. Mapping how neural activity relates to different functions helps us understand how the brain performs these computations. Many mapping techniques have limited spatial or temporal resolution, restricting our ability to dissect computations that overlap closely in space and time. We used micro-electrocorticography recordings to map neural activity across multiple cortical areas while monkeys made goal-directed reaches. These measurements revealed high spatial and temporal resolution maps of neural activity related to eye, arm, and reward information processing. These maps reveal overlapping neural computations underlying movement and open opportunities to use eye and reward information to improve therapies to restore motor function.

查看原文
分享 分享
微信好友 朋友圈 QQ好友 复制链接
本刊更多论文
求助全文
约1分钟内获得全文 去求助
来源期刊
Journal of Neuroscience
Journal of Neuroscience 医学-神经科学
CiteScore
9.30
自引率
3.80%
发文量
1164
审稿时长
12 months
期刊介绍: JNeurosci (ISSN 0270-6474) is an official journal of the Society for Neuroscience. It is published weekly by the Society, fifty weeks a year, one volume a year. JNeurosci publishes papers on a broad range of topics of general interest to those working on the nervous system. Authors now have an Open Choice option for their published articles
期刊最新文献
Characterizing Brain-Cardiovascular Aging Using Multiorgan Imaging and Machine Learning Distinct patterns of PV and SST GABAergic neuronal activity in the basal forebrain during olfactory-guided behavior in mice. Neurofibromin deficiency alters the patterning and prioritization of motor behaviors in a state-dependent manner. Rab27b promotes lysosomal function and alpha-synuclein clearance in neurons. Sleep modulates neural timescales and spatiotemporal integration in the human cortex.
×
引用
GB/T 7714-2015
复制
MLA
复制
APA
复制
导出至
BibTeX EndNote RefMan NoteFirst NoteExpress
×
×
提示
您的信息不完整,为了账户安全,请先补充。
现在去补充
×
提示
您因"违规操作"
具体请查看互助需知
我知道了
×
提示
现在去查看 取消
×
提示
确定
0
微信
客服QQ
Book学术公众号 扫码关注我们
反馈
×
意见反馈
请填写您的意见或建议
请填写您的手机或邮箱
已复制链接
已复制链接
快去分享给好友吧!
我知道了
×
扫码分享
扫码分享
Book学术官方微信
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术
文献互助 智能选刊 最新文献 互助须知 联系我们:info@booksci.cn
Book学术提供免费学术资源搜索服务,方便国内外学者检索中英文文献。致力于提供最便捷和优质的服务体验。
Copyright © 2023 Book学术 All rights reserved.
ghs 京公网安备 11010802042870号 京ICP备2023020795号-1