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Atypical functional connectivity of temporal cortex with precuneus and visual regions may be an early-age signature of ASD
Molecular Autism ( IF 6.2 ) Pub Date : 2023-03-10 , DOI: 10.1186/s13229-023-00543-8
Yaqiong Xiao 1, 2 , Teresa H Wen 2 , Lauren Kupis 3 , Lisa T Eyler 4, 5 , Vani Taluja 2 , Jaden Troxel 2 , Disha Goel 2 , Michael V Lombardo 6 , Karen Pierce 2 , Eric Courchesne 2
Affiliation  

Social and language abilities are closely intertwined during early typical development. In autism spectrum disorder (ASD), however, deficits in social and language development are early-age core symptoms. We previously reported that superior temporal cortex, a well-established social and language region, shows reduced activation to social affective speech in ASD toddlers; however, the atypical cortical connectivity that accompanies this deviance remains unknown. We collected clinical, eye tracking, and resting-state fMRI data from 86 ASD and non-ASD subjects (mean age 2.3 ± 0.7 years). Functional connectivity of left and right superior temporal regions with other cortical regions and correlations between this connectivity and each child’s social and language abilities were examined. While there was no group difference in functional connectivity, the connectivity between superior temporal cortex and frontal and parietal regions was significantly correlated with language, communication, and social abilities in non-ASD subjects, but these effects were absent in ASD subjects. Instead, ASD subjects, regardless of different social or nonsocial visual preferences, showed atypical correlations between temporal–visual region connectivity and communication ability (r(49) = 0.55, p < 0.001) and between temporal–precuneus connectivity and expressive language ability (r(49) = 0.58, p < 0.001). The distinct connectivity–behavior correlation patterns may be related to different developmental stages in ASD and non-ASD subjects. The use of a prior 2-year-old template for spatial normalization may not be optimal for a few subjects beyond this age range. Superior temporal cortex is known to have reduced activation to social affective speech in ASD at early ages, and here we find in ASD toddlers that it also has atypical connectivity with visual and precuneus cortices that is correlated with communication and language ability, a pattern not seen in non-ASD toddlers. This atypicality may be an early-age signature of ASD that also explains why the disorder has deviant early language and social development. Given that these atypical connectivity patterns are also present in older individuals with ASD, we conclude these atypical connectivity patterns persist across age and may explain why successful interventions targeting language and social skills at all ages in ASD are so difficult to achieve.

中文翻译:

颞叶皮层与楔前叶和视觉区域的非典型功能连接可能是 ASD 的早期特征

在早期典型发展过程中,社交和语言能力密切相关。然而,在自闭症谱系障碍 (ASD) 中,社交和语言发育缺陷是早期的核心症状。我们之前曾报道,颞上皮层是一个完善的社交和语言区域,显示 ASD 幼儿对社交情感言语的激活减少;然而,伴随这种异常的非典型皮层连接仍然未知。我们收集了 86 名 ASD 和非 ASD 受试者(平均年龄 2.3 ± 0.7 岁)的临床、眼动追踪和静息态 fMRI 数据。检查了左右颞上区与其他皮层区域的功能连接,以及这种连接与每个孩子的社交和语言能力之间的相关性。虽然在功能连接方面没有组别差异,上颞叶皮层与额叶和顶叶区域之间的连通性与非 ASD 受试者的语言、沟通和社交能力显着相关,但 ASD 受试者不存在这些影响。相反,ASD 受试者,无论社会或非社会视觉偏好不同,都显示出时间-视觉区域连通性和沟通能力之间的非典型相关性 (r(49) = 0.55,p < 0.001) 以及时间-楔前叶连通性和语言表达能力之间的非典型相关性 (r (49) = 0.58,p < 0.001)。不同的连通性-行为相关模式可能与 ASD 和非 ASD 受试者的不同发育阶段有关。对于超出此年龄范围的一些受试者,使用之前 2 岁的模板进行空间归一化可能不是最佳选择。众所周知,上颞叶皮层在早期 ASD 中减少了对社交情感言语的激活,在这里我们在 ASD 幼儿中发现它还与视觉和楔前叶皮层具有非典型连接性,这与沟通和语言能力相关,这是一种未见的模式在非 ASD 幼儿中。这种非典型性可能是 ASD 的早期特征,这也解释了为什么这种疾病具有异常的早期语言和社会发展。鉴于这些非典型连接模式也存在于患有 ASD 的老年人中,我们得出结论,这些非典型连接模式在整个年龄段都存在,并且可以解释为什么针对所有年龄段的 ASD 患者的语言和社交技能的成功干预如此难以实现。在这里,我们在 ASD 幼儿中发现它还与视觉和楔前叶皮质具有非典型连接,这与沟通和语言能力相关,这种模式在非 ASD 幼儿中是看不到的。这种非典型性可能是 ASD 的早期特征,这也解释了为什么这种疾病具有异常的早期语言和社会发展。鉴于这些非典型连接模式也存在于患有 ASD 的老年人中,我们得出结论,这些非典型连接模式在整个年龄段都存在,并且可以解释为什么针对所有年龄段的 ASD 患者的语言和社交技能的成功干预如此难以实现。在这里,我们在 ASD 幼儿中发现它还与视觉和楔前叶皮质具有非典型连接,这与沟通和语言能力相关,这种模式在非 ASD 幼儿中是看不到的。这种非典型性可能是 ASD 的早期特征,这也解释了为什么这种疾病具有异常的早期语言和社会发展。鉴于这些非典型连接模式也存在于患有 ASD 的老年人中,我们得出结论,这些非典型连接模式在整个年龄段都存在,并且可以解释为什么针对所有年龄段的 ASD 患者的语言和社交技能的成功干预如此难以实现。这种非典型性可能是 ASD 的早期特征,这也解释了为什么这种疾病具有异常的早期语言和社会发展。鉴于这些非典型连接模式也存在于患有 ASD 的老年人中,我们得出结论,这些非典型连接模式在整个年龄段都存在,并且可以解释为什么针对所有年龄段的 ASD 患者的语言和社交技能的成功干预如此难以实现。这种非典型性可能是 ASD 的早期特征,这也解释了为什么这种疾病具有异常的早期语言和社会发展。鉴于这些非典型连接模式也存在于患有 ASD 的老年人中,我们得出结论,这些非典型连接模式在整个年龄段都存在,并且可以解释为什么针对所有年龄段的 ASD 患者的语言和社交技能的成功干预如此难以实现。
更新日期:2023-03-11
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