{"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":null,"pages":null},"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.
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