Anatomically distinct regions in the inferior frontal cortex are modulated by task and reading skill.

IF 4 2区 医学 Q1 NEUROSCIENCES Journal of Neuroscience Pub Date : 2025-03-24 DOI:10.1523/JNEUROSCI.1767-24.2025
Hannah L Stone, Jamie L Mitchell, Mia Fuentes-Jimenez, Jasmine E Tran, Jason D Yeatman, Maya Yablonski
{"title":"Anatomically distinct regions in the inferior frontal cortex are modulated by task and reading skill.","authors":"Hannah L Stone, Jamie L Mitchell, Mia Fuentes-Jimenez, Jasmine E Tran, Jason D Yeatman, Maya Yablonski","doi":"10.1523/JNEUROSCI.1767-24.2025","DOIUrl":null,"url":null,"abstract":"<p><p>Inferior frontal cortex (IFC) is a critical region for reading and language. This part of the cortex is highly heterogeneous in its structural and functional organization and shows high variability across individuals. Despite decades of research, the relationship between specific IFC regions and reading skill remains unclear. To shed light on the function of IFC in reading, we aim to (1) characterize the functional landscape of text-selective responses in IFC, while accounting for interindividual variability; and (2) examine how text-selective regions in the IFC relate to reading proficiency. To this end, children with a wide range of reading ability (N=66; age 7-14 years, 34 female, 32 male) completed functional MRI scans while performing two tasks on text and non-text visual stimuli. Importantly, both tasks do not explicitly require reading, and can be performed on all visual stimuli. This design allows us to tease apart stimulus-driven responses from task-driven responses and examine where in IFC task and stimulus interact. We were able to identify three anatomically-distinct, text-selective clusters of activation in IFC, in the inferior frontal sulcus (IFS), and dorsal and ventral precentral gyrus (PrG). ​​These three regions showed a strong task effect that was highly specific to text. Furthermore, text-selectivity in the IFS and dorsal PrG was associated with reading proficiency, such that better readers showed higher selectivity to text. These findings suggest that text-selective regions in the IFC are sensitive to both stimulus and task, and highlight the importance of this region for proficient reading.<b>Significance statement</b> The inferior frontal cortex (IFC) is a critical region for language processing, yet despite decades of research, its relationship with reading skill remains unclear. In a group of children with a wide range of reading skills, we were able to identify three anatomically distinct text-selective clusters of activation in the IFC. ​​These regions showed a strong task effect that was highly selective to text. Text-selectivity was positively correlated with reading proficiency, such that better readers showed higher selectivity to text, even in tasks that did not require reading. These findings suggest that multiple text-selective regions within IFC are sensitive to both stimulus and task, and highlight the critical role of IFC for reading proficiency.</p>","PeriodicalId":50114,"journal":{"name":"Journal of Neuroscience","volume":" ","pages":""},"PeriodicalIF":4.0000,"publicationDate":"2025-03-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12060616/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of Neuroscience","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1523/JNEUROSCI.1767-24.2025","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

Inferior frontal cortex (IFC) is a critical region for reading and language. This part of the cortex is highly heterogeneous in its structural and functional organization and shows high variability across individuals. Despite decades of research, the relationship between specific IFC regions and reading skill remains unclear. To shed light on the function of IFC in reading, we aim to (1) characterize the functional landscape of text-selective responses in IFC, while accounting for interindividual variability; and (2) examine how text-selective regions in the IFC relate to reading proficiency. To this end, children with a wide range of reading ability (N=66; age 7-14 years, 34 female, 32 male) completed functional MRI scans while performing two tasks on text and non-text visual stimuli. Importantly, both tasks do not explicitly require reading, and can be performed on all visual stimuli. This design allows us to tease apart stimulus-driven responses from task-driven responses and examine where in IFC task and stimulus interact. We were able to identify three anatomically-distinct, text-selective clusters of activation in IFC, in the inferior frontal sulcus (IFS), and dorsal and ventral precentral gyrus (PrG). ​​These three regions showed a strong task effect that was highly specific to text. Furthermore, text-selectivity in the IFS and dorsal PrG was associated with reading proficiency, such that better readers showed higher selectivity to text. These findings suggest that text-selective regions in the IFC are sensitive to both stimulus and task, and highlight the importance of this region for proficient reading.Significance statement The inferior frontal cortex (IFC) is a critical region for language processing, yet despite decades of research, its relationship with reading skill remains unclear. In a group of children with a wide range of reading skills, we were able to identify three anatomically distinct text-selective clusters of activation in the IFC. ​​These regions showed a strong task effect that was highly selective to text. Text-selectivity was positively correlated with reading proficiency, such that better readers showed higher selectivity to text, even in tasks that did not require reading. These findings suggest that multiple text-selective regions within IFC are sensitive to both stimulus and task, and highlight the critical role of IFC for reading proficiency.

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
下额叶皮层中解剖学上不同的区域受任务和阅读技能的调节。
下额叶皮质(IFC)是阅读和语言的关键区域。这部分皮层在结构和功能组织上是高度异质的,并且在个体之间表现出高度的可变性。尽管经过数十年的研究,特定IFC区域与阅读技能之间的关系仍不清楚。为了阐明IFC在阅读中的功能,我们的目标是(1)描述IFC中文本选择反应的功能格局,同时考虑个体间的差异;(2)研究IFC中的文本选择区域与阅读能力的关系。为此,具有广泛阅读能力的儿童(N=66;年龄7-14岁,34名女性,32名男性)在执行文本和非文本视觉刺激两项任务时完成了功能性MRI扫描。重要的是,这两项任务都不明确要求阅读,并且可以在所有视觉刺激下执行。这种设计使我们能够区分刺激驱动的反应和任务驱动的反应,并检查IFC中任务和刺激在哪里相互作用。我们能够在IFC、额下沟(IFS)和中央前回背侧和腹侧(PrG)中识别出三个解剖学上不同的、文本选择性的激活簇。这三个区域显示出强烈的任务效应,这是高度特定于文本的。此外,前颞叶和背侧PrG的文本选择性与阅读能力有关,因此,更好的读者对文本表现出更高的选择性。这些发现表明,IFC中的文本选择区域对刺激和任务都很敏感,并强调了该区域对熟练阅读的重要性。下额叶皮层(IFC)是语言处理的关键区域,然而,尽管几十年的研究,它与阅读技能的关系尚不清楚。在一组具有广泛阅读技能的儿童中,我们能够在IFC中识别出三个解剖学上不同的文本选择激活簇。这些区域显示出强烈的任务效应,对文本具有高度选择性。文本选择性与阅读熟练程度正相关,因此,更好的读者对文本的选择性更高,即使在不需要阅读的任务中也是如此。这些研究结果表明,IFC内的多个文本选择区域对刺激和任务都很敏感,并强调了IFC对阅读能力的关键作用。
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 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
Increased and coupled ERP and fMRI responses towards positive social evaluative feedback: An EEG-fMRI study. Anesthetic State-Dependent Bidirectional Control of States of Consciousness via Heterogeneous Medial Septum to Ventral Tegmental Area Circuits under Sevoflurane in Mice. Temporally coordinated activity among motor cortex, thalamus, and thalamic reticular nucleus neurons during rat forelimb movements. Corticotropin-releasing factor and somatostatin neurons in the central amygdala mediate dynamic defensive behaviors during fear extinction. The Parafascicular Role in Updating Action from a Spatial to a Visual Strategy is Driven by its Glutamatergic Mesencephalic Locomotor Region inputs.
×
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:604180095
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