Atypical oscillatory and aperiodic signatures of visual sampling in developmental dyslexia

IF 3.4 2区 医学 Q2 NEUROIMAGING Neuroimage-Clinical Pub Date : 2025-01-01 DOI:10.1016/j.nicl.2024.103720
Alessia Santoni , Giuseppe Di Dona , David Melcher , Laura Franchin , Luca Ronconi
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Abstract

Temporal processing deficits in Developmental Dyslexia (DD) have been documented extensively at the behavioral level, leading to the formulation of neural theories positing that such anomalies in parsing multisensory input rely on aberrant synchronization of neural oscillations or to an excessive level of neural noise. Despite reading being primarily supported by visual functions, experimental evidence supporting these theories remains scarce. Here, we tested 26 adults with DD (9 females) and 31 neurotypical controls (16 females) with a temporal segregation/integration task that required participants to either integrate or segregate two rapidly presented displays while their EEG activity was recorded. We confirmed a temporal sampling deficit in DD, which specifically affected the rapid segregation of visual input. While the ongoing alpha frequency and the excitation/inhibition (E/I) ratio (i.e., an index of neural noise quantified by the aperiodic exponent) were differently modulated based on task demands in typical readers, DD participants exhibited an impairment in alpha speed modulation and an altered E/I ratio that affected their rapid visual sampling. Nonetheless, an association between visual temporal sampling accuracy and both alpha frequency and the E/I ratio measured at rest were evident in the DD group, further confirming an anomalous interplay between alpha synchronization, the E/I ratio and active visual sampling. These results provide evidence that both trait- and state-like differences in alpha-band synchronization and neural noise levels coexist in the dyslexic brain and are synergistically responsible for cascade effects on visual sampling and reading.
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发展性阅读障碍中视觉抽样的非典型振荡和非周期性特征。
发展性阅读障碍(DD)的时间处理缺陷已经在行为层面得到了广泛的记录,导致神经理论的形成,假设分析多感觉输入的这种异常依赖于神经振荡的异常同步或过度的神经噪声。尽管阅读主要是由视觉功能支持的,但支持这些理论的实验证据仍然很少。在这里,我们测试了26名成年DD患者(9名女性)和31名神经正常对照组(16名女性),并进行了时间分离/整合任务,该任务要求参与者在记录脑电图活动的同时整合或分离两个快速呈现的画面。我们证实了DD的时间采样缺陷,这特别影响了视觉输入的快速分离。在典型阅读者中,持续α频率和兴奋/抑制(E/I)比(即由非周期指数量化的神经噪声指数)根据任务需求被不同地调制,DD参与者表现出α速度调制的损伤和E/I比的改变,影响了他们的快速视觉采样。尽管如此,视觉时间采样精度与α频率和静止时测量的E/I比之间的关联在DD组中是明显的,进一步证实了α同步、E/I比和主动视觉采样之间的异常相互作用。这些结果提供了证据,证明在阅读困难的大脑中,α波段同步和神经噪声水平的特征和状态样差异共存,并协同负责视觉采样和阅读的级联效应。
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来源期刊
Neuroimage-Clinical
Neuroimage-Clinical NEUROIMAGING-
CiteScore
7.50
自引率
4.80%
发文量
368
审稿时长
52 days
期刊介绍: NeuroImage: Clinical, a journal of diseases, disorders and syndromes involving the Nervous System, provides a vehicle for communicating important advances in the study of abnormal structure-function relationships of the human nervous system based on imaging. The focus of NeuroImage: Clinical is on defining changes to the brain associated with primary neurologic and psychiatric diseases and disorders of the nervous system as well as behavioral syndromes and developmental conditions. The main criterion for judging papers is the extent of scientific advancement in the understanding of the pathophysiologic mechanisms of diseases and disorders, in identification of functional models that link clinical signs and symptoms with brain function and in the creation of image based tools applicable to a broad range of clinical needs including diagnosis, monitoring and tracking of illness, predicting therapeutic response and development of new treatments. Papers dealing with structure and function in animal models will also be considered if they reveal mechanisms that can be readily translated to human conditions.
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