Alpha Traveling Waves during Working Memory: Disentangling Bottom-up Gating and Top-down Gain Control.

IF 4.4 2区 医学 Q1 NEUROSCIENCES
Yifan Zeng, Paul Sauseng, Andrea Alamia
{"title":"Alpha Traveling Waves during Working Memory: Disentangling Bottom-up Gating and Top-down Gain Control.","authors":"Yifan Zeng, Paul Sauseng, Andrea Alamia","doi":"10.1523/JNEUROSCI.0532-24.2024","DOIUrl":null,"url":null,"abstract":"<p><p>While previous works established the inhibitory role of alpha oscillations during working memory maintenance, it remains an open question whether such an inhibitory control is a top-down process. Here, we attempted to disentangle this issue by considering the spatio-temporal component of waves in the alpha band, i.e., alpha traveling waves. We reanalyzed two pre-existing and open-access EEG datasets (N = 180, 90 males, 80 females, 10 unknown) where participants performed lateralized, visual delayed match-to-sample working memory tasks. In the first dataset, the distractor load was manipulated (2, 4, or 6), whereas in the second dataset, the memory span varied between 1, 3, and 6 items. We focused on the propagation of alpha waves on the anterior-posterior axis during the retention period. Our results reveal an increase in alpha-band forward waves as the distractor load increased, but also an increase in forward waves and a decrease in backward waves as the memory set size increased. Our results also showed a lateralization effect: alpha forward waves exhibited a more pronounced increase in the hemisphere contralateral to the distractors, whereas the reduction in backward waves was stronger in the hemisphere contralateral to the targets. In short, the forward waves were regulated by distractors, whereas targets inversely modulated backward waves. Such a dissociation of goal-related and goal-irrelevant physiological signals suggests the co-existence of bottom-up and top-down inhibitory processes: alpha forward waves might convey a gating effect driven by distractor load, while backward waves may represent direct top-down gain control of downstream visual areas.<b>Significance Statement</b> When exploring the functional role of alpha band neural oscillations during working memory, mostly amplitude modulations have been considered so far, with relatively limited exploration of spatial-temporal dynamics of this rather global brain oscillatory signature. The present study seeks to address this gap by examining the directionality of alpha wave propagation during working memory retention. Our findings offer novel insights into the well-established inhibitory role of alpha waves, demonstrating that this function is manifested differently according to their propagation directions: forward waves seem to facilitate bottom-up gating, while backward waves might mediate top-down gain control.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.4000,"publicationDate":"2024-11-06","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.0532-24.2024","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

While previous works established the inhibitory role of alpha oscillations during working memory maintenance, it remains an open question whether such an inhibitory control is a top-down process. Here, we attempted to disentangle this issue by considering the spatio-temporal component of waves in the alpha band, i.e., alpha traveling waves. We reanalyzed two pre-existing and open-access EEG datasets (N = 180, 90 males, 80 females, 10 unknown) where participants performed lateralized, visual delayed match-to-sample working memory tasks. In the first dataset, the distractor load was manipulated (2, 4, or 6), whereas in the second dataset, the memory span varied between 1, 3, and 6 items. We focused on the propagation of alpha waves on the anterior-posterior axis during the retention period. Our results reveal an increase in alpha-band forward waves as the distractor load increased, but also an increase in forward waves and a decrease in backward waves as the memory set size increased. Our results also showed a lateralization effect: alpha forward waves exhibited a more pronounced increase in the hemisphere contralateral to the distractors, whereas the reduction in backward waves was stronger in the hemisphere contralateral to the targets. In short, the forward waves were regulated by distractors, whereas targets inversely modulated backward waves. Such a dissociation of goal-related and goal-irrelevant physiological signals suggests the co-existence of bottom-up and top-down inhibitory processes: alpha forward waves might convey a gating effect driven by distractor load, while backward waves may represent direct top-down gain control of downstream visual areas.Significance Statement When exploring the functional role of alpha band neural oscillations during working memory, mostly amplitude modulations have been considered so far, with relatively limited exploration of spatial-temporal dynamics of this rather global brain oscillatory signature. The present study seeks to address this gap by examining the directionality of alpha wave propagation during working memory retention. Our findings offer novel insights into the well-established inhibitory role of alpha waves, demonstrating that this function is manifested differently according to their propagation directions: forward waves seem to facilitate bottom-up gating, while backward waves might mediate top-down gain control.

工作记忆中的α游走波:区分自下而上的门控和自上而下的增益控制
虽然之前的研究证实了阿尔法振荡在工作记忆维持过程中的抑制作用,但这种抑制控制是否是一个自上而下的过程仍是一个未决问题。在这里,我们试图通过考虑α波段波的时空成分,即α行波,来厘清这一问题。我们重新分析了两个已有的、开放存取的脑电图数据集(N = 180,90 名男性,80 名女性,10 名未知者),在这两个数据集中,参与者进行了侧向、视觉延迟匹配到样本的工作记忆任务。在第一个数据集中,分散注意力的负荷是可调的(2、4 或 6),而在第二个数据集中,记忆跨度在 1、3 和 6 个项目之间变化。我们重点研究了保留期间α波在前后轴上的传播。我们的结果表明,随着分心负荷的增加,α波段的前向波也会增加,但随着记忆集大小的增加,前向波也会增加,而后向波则会减少。我们的结果还显示了侧化效应:α前向波在分心者对侧半球的增加更为明显,而后向波在目标对侧半球的减少更为强烈。简而言之,前向波受到干扰物的调节,而目标则反向调节后向波。这种目标相关和目标无关生理信号的分离表明,自下而上和自上而下的抑制过程是并存的:α前向波可能传达了由分心物负荷驱动的门控效应,而后向波可能代表了对下游视觉区域直接的自上而下的增益控制。 意义声明 在探索工作记忆过程中α波段神经振荡的功能作用时,迄今为止考虑的主要是振幅调制,而对这一相当全面的大脑振荡特征的时空动态的探索相对有限。本研究试图通过研究工作记忆保持过程中阿尔法波传播的方向性来填补这一空白。我们的研究结果为α波行之有效的抑制作用提供了新的见解,证明这一功能根据其传播方向的不同而有不同的表现:前向波似乎有助于自下而上的门控,而后向波可能介导自上而下的增益控制。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
求助全文
约1分钟内获得全文 求助全文
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
×
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
确定
请完成安全验证×
copy
已复制链接
快去分享给好友吧!
我知道了
右上角分享
点击右上角分享
0
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 布克学术 All rights reserved.
京ICP备2023020795号-1
ghs 京公网安备 11010802042870号
Book学术文献互助
Book学术文献互助群
群 号:481959085
Book学术官方微信