Top-down and bottom-up interactions rely on nested brain oscillations to shape rhythmic visual attention sampling.

IF 9.8 1区 生物学 Q1 Agricultural and Biological Sciences
PLoS Biology Pub Date : 2025-04-10 eCollection Date: 2025-04-01 DOI:10.1371/journal.pbio.3002688
Jelena Trajkovic, Domenica Veniero, Simon Hanslmayr, Satu Palva, Gabriela Cruz, Vincenzo Romei, Gregor Thut
{"title":"Top-down and bottom-up interactions rely on nested brain oscillations to shape rhythmic visual attention sampling.","authors":"Jelena Trajkovic, Domenica Veniero, Simon Hanslmayr, Satu Palva, Gabriela Cruz, Vincenzo Romei, Gregor Thut","doi":"10.1371/journal.pbio.3002688","DOIUrl":null,"url":null,"abstract":"<p><p>Adaptive visual processing is enabled through the dynamic interplay between top-down and bottom-up (feedback/feedforward) information exchange, presumably propagated through brain oscillations. Here, we causally tested for the oscillatory mechanisms governing this interaction in the human visual system. Using concurrent transcranial magnetic stimulation-electroencephalography (TMS-EEG), we emulated top-down signals by a single TMS pulse over the frontal eye field (right FEF), while manipulating the strength of sensory input through the presentation of moving concentric gratings (compared to a control-TMS site). FEF-TMS without sensory input led to a top-down modulated occipital phase realignment, alongside higher fronto-occipital phase connectivity, in the alpha/beta band. Sensory input in the absence of FEF-TMS increased occipital gamma activity. Crucially, testing the interaction between top-down and bottom-up processes (FEF-TMS during sensory input) revealed an increased nesting of the bottom-up gamma activity in the alpha/beta-band cycles. This establishes a causal link between phase-to-power coupling and top-down modulation of feedforward signals, providing novel mechanistic insights into how attention interacts with sensory input at the neural level, shaping rhythmic sampling.</p>","PeriodicalId":49001,"journal":{"name":"PLoS Biology","volume":"23 4","pages":"e3002688"},"PeriodicalIF":9.8000,"publicationDate":"2025-04-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12037075/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"PLoS Biology","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1371/journal.pbio.3002688","RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2025/4/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"Agricultural and Biological Sciences","Score":null,"Total":0}
引用次数: 0

Abstract

Adaptive visual processing is enabled through the dynamic interplay between top-down and bottom-up (feedback/feedforward) information exchange, presumably propagated through brain oscillations. Here, we causally tested for the oscillatory mechanisms governing this interaction in the human visual system. Using concurrent transcranial magnetic stimulation-electroencephalography (TMS-EEG), we emulated top-down signals by a single TMS pulse over the frontal eye field (right FEF), while manipulating the strength of sensory input through the presentation of moving concentric gratings (compared to a control-TMS site). FEF-TMS without sensory input led to a top-down modulated occipital phase realignment, alongside higher fronto-occipital phase connectivity, in the alpha/beta band. Sensory input in the absence of FEF-TMS increased occipital gamma activity. Crucially, testing the interaction between top-down and bottom-up processes (FEF-TMS during sensory input) revealed an increased nesting of the bottom-up gamma activity in the alpha/beta-band cycles. This establishes a causal link between phase-to-power coupling and top-down modulation of feedforward signals, providing novel mechanistic insights into how attention interacts with sensory input at the neural level, shaping rhythmic sampling.

自上而下和自下而上的相互作用依赖于嵌套的大脑振荡来形成有节奏的视觉注意采样。
自适应视觉处理是通过自上而下和自下而上(反馈/前馈)信息交换之间的动态相互作用实现的,可能是通过大脑振荡传播的。在这里,我们对人类视觉系统中控制这种相互作用的振荡机制进行了因果测试。使用并发经颅磁刺激-脑电图(TMS- eeg),我们通过在前额眼场(右侧FEF)上的单个TMS脉冲来模拟自上而下的信号,同时通过呈现移动的同心光栅来操纵感觉输入的强度(与对照TMS部位相比)。在没有感觉输入的情况下,FEF-TMS导致了自上而下调制的枕相调整,同时在α / β波段有更高的额枕相连通性。在没有FEF-TMS的情况下,感觉输入增加了枕部伽马活动。至关重要的是,测试自上而下和自下而上过程之间的相互作用(感官输入期间的FEF-TMS)显示,在α / β波段周期中,自下而上的伽马活动的嵌套增加。这建立了相位-功率耦合和前馈信号自上而下调制之间的因果关系,为注意如何在神经水平上与感觉输入相互作用,形成有节奏的采样提供了新的机制见解。
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
PLoS Biology
PLoS Biology BIOCHEMISTRY & MOLECULAR BIOLOGY-BIOLOGY
CiteScore
15.40
自引率
2.00%
发文量
359
审稿时长
3-8 weeks
期刊介绍: PLOS Biology is the flagship journal of the Public Library of Science (PLOS) and focuses on publishing groundbreaking and relevant research in all areas of biological science. The journal features works at various scales, ranging from molecules to ecosystems, and also encourages interdisciplinary studies. PLOS Biology publishes articles that demonstrate exceptional significance, originality, and relevance, with a high standard of scientific rigor in methodology, reporting, and conclusions. The journal aims to advance science and serve the research community by transforming research communication to align with the research process. It offers evolving article types and policies that empower authors to share the complete story behind their scientific findings with a diverse global audience of researchers, educators, policymakers, patient advocacy groups, and the general public. PLOS Biology, along with other PLOS journals, is widely indexed by major services such as Crossref, Dimensions, DOAJ, Google Scholar, PubMed, PubMed Central, Scopus, and Web of Science. Additionally, PLOS Biology is indexed by various other services including AGRICOLA, Biological Abstracts, BIOSYS Previews, CABI CAB Abstracts, CABI Global Health, CAPES, CAS, CNKI, Embase, Journal Guide, MEDLINE, and Zoological Record, ensuring that the research content is easily accessible and discoverable by a wide range of audiences.
×
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