Yicheng Zhang , Layla Banihashemi , Amelia Versace , Alyssa Samolyk , Megan Taylor , Gabrielle English , Vanessa J. Schmithorst , Vincent K. Lee , Richelle Stiffler , Haris Aslam , Ashok Panigrahy , Alison E. Hipwell , Mary L. Phillips
{"title":"婴儿早期前额叶皮质微结构可预测现在和未来的情绪性","authors":"Yicheng Zhang , Layla Banihashemi , Amelia Versace , Alyssa Samolyk , Megan Taylor , Gabrielle English , Vanessa J. Schmithorst , Vincent K. Lee , Richelle Stiffler , Haris Aslam , Ashok Panigrahy , Alison E. Hipwell , Mary L. Phillips","doi":"10.1016/j.biopsych.2024.04.001","DOIUrl":null,"url":null,"abstract":"<div><h3>Background</h3><div><span><span>High levels of infant negative emotionality<span> (NE) and low positive emotionality (PE) predict future emotional and behavioral problems. The </span></span>prefrontal cortex<span> (PFC) supports emotional<span> regulation, with each PFC subregion specializing in specific emotional processes. Neurite orientation dispersion and density imaging estimates microstructural integrity and </span></span></span>myelination via the neurite density index (NDI) and dispersion via the orientation dispersion index (ODI), with potential to more accurately evaluate microstructural alterations in the developing brain. Yet, no study has used these indices to examine associations between PFC microstructure and concurrent or developing infant emotionality.</div></div><div><h3>Methods</h3><div>We modeled PFC subregional NDI and ODI at 3 months with caregiver-reported infant NE and PE at 3 months (<em>n</em> = 61) and at 9 months (<em>n</em> = 50), using multivariable and subsequent bivariate regression models.</div></div><div><h3>Results</h3><div>The most robust statistically significant findings were positive associations among 3-month rostral anterior cingulate cortex<span><span> (ACC) ODI and caudal ACC NDI and concurrent NE, a positive association between 3-month lateral orbitofrontal cortex ODI and prospective NE, and a negative association between 3-month </span>dorsolateral PFC<span> ODI and concurrent PE. Multivariate models also revealed that other PFC subregional microstructure measures, as well as infant and caregiver sociodemographic and clinical factors, predicted infant 3- and 9-month NE and PE.</span></span></div></div><div><h3>Conclusions</h3><div>Greater NDI and ODI, reflecting greater microstructural complexity, in PFC regions supporting salience perception (rostral ACC), decision making<span> (lateral orbitofrontal cortex), action selection (caudal ACC), and attentional processes (dorsolateral PFC) might result in greater integration of these subregions with other neural networks and greater attention to salient negative external cues, thus higher NE and/or lower PE. These findings provide potential infant cortical markers of future psychopathology risk.</span></div></div>","PeriodicalId":8918,"journal":{"name":"Biological Psychiatry","volume":"96 12","pages":"Pages 959-970"},"PeriodicalIF":9.6000,"publicationDate":"2024-04-09","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Early Infant Prefrontal Cortical Microstructure Predicts Present and Future Emotionality\",\"authors\":\"Yicheng Zhang , Layla Banihashemi , Amelia Versace , Alyssa Samolyk , Megan Taylor , Gabrielle English , Vanessa J. Schmithorst , Vincent K. Lee , Richelle Stiffler , Haris Aslam , Ashok Panigrahy , Alison E. Hipwell , Mary L. Phillips\",\"doi\":\"10.1016/j.biopsych.2024.04.001\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<div><h3>Background</h3><div><span><span>High levels of infant negative emotionality<span> (NE) and low positive emotionality (PE) predict future emotional and behavioral problems. The </span></span>prefrontal cortex<span> (PFC) supports emotional<span> regulation, with each PFC subregion specializing in specific emotional processes. Neurite orientation dispersion and density imaging estimates microstructural integrity and </span></span></span>myelination via the neurite density index (NDI) and dispersion via the orientation dispersion index (ODI), with potential to more accurately evaluate microstructural alterations in the developing brain. Yet, no study has used these indices to examine associations between PFC microstructure and concurrent or developing infant emotionality.</div></div><div><h3>Methods</h3><div>We modeled PFC subregional NDI and ODI at 3 months with caregiver-reported infant NE and PE at 3 months (<em>n</em> = 61) and at 9 months (<em>n</em> = 50), using multivariable and subsequent bivariate regression models.</div></div><div><h3>Results</h3><div>The most robust statistically significant findings were positive associations among 3-month rostral anterior cingulate cortex<span><span> (ACC) ODI and caudal ACC NDI and concurrent NE, a positive association between 3-month lateral orbitofrontal cortex ODI and prospective NE, and a negative association between 3-month </span>dorsolateral PFC<span> ODI and concurrent PE. Multivariate models also revealed that other PFC subregional microstructure measures, as well as infant and caregiver sociodemographic and clinical factors, predicted infant 3- and 9-month NE and PE.</span></span></div></div><div><h3>Conclusions</h3><div>Greater NDI and ODI, reflecting greater microstructural complexity, in PFC regions supporting salience perception (rostral ACC), decision making<span> (lateral orbitofrontal cortex), action selection (caudal ACC), and attentional processes (dorsolateral PFC) might result in greater integration of these subregions with other neural networks and greater attention to salient negative external cues, thus higher NE and/or lower PE. 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引用次数: 0
摘要
背景高水平的婴儿负面情绪性(NE)和低水平的正面情绪性(PE)可预测未来的情绪和行为问题。前额叶皮层(PFC)支持情绪调节,每个前额叶皮层亚区都专门负责特定的情绪过程。神经元取向弥散和密度成像通过神经元密度指数(NDI)和取向弥散指数(ODI)估算微结构完整性和髓鞘化,有望更准确地评估发育中大脑的微结构改变。方法我们使用多变量和随后的双变量回归模型,将3个月时的PFC亚区域NDI和ODI与护理人员报告的3个月时婴儿NE和PE(n = 61)和9个月时婴儿NE和PE(n = 50)进行建模。结果 最有统计学意义的发现是,3 个月的喙前扣带回皮层(ACC)ODI 和尾部 ACC NDI 与同时的 NE 呈正相关,3 个月的外侧眶额皮层 ODI 与前瞻性 NE 呈正相关,3 个月的背外侧 PFC ODI 与同时的 PE 呈负相关。多变量模型还显示,其他前额叶皮质亚区微结构测量以及婴儿和照护者的社会人口学和临床因素可预测婴儿 3 个月和 9 个月的 NE 和 PE。结论在支持显著性感知(喙侧 ACC)、决策制定(外侧眶额叶皮层)、行动选择(尾侧 ACC)和注意过程(背外侧 PFC)的 PFC 区域中,NDI 和 ODI 越高,反映出微观结构越复杂,可能会导致这些亚区域与其他神经网络的整合程度越高,对显著的负面外部线索的注意程度越高,因此 NE 和 PE 越高和/或越低。这些发现为未来的精神病理学风险提供了潜在的婴儿皮质标记。
Early Infant Prefrontal Cortical Microstructure Predicts Present and Future Emotionality
Background
High levels of infant negative emotionality (NE) and low positive emotionality (PE) predict future emotional and behavioral problems. The prefrontal cortex (PFC) supports emotional regulation, with each PFC subregion specializing in specific emotional processes. Neurite orientation dispersion and density imaging estimates microstructural integrity and myelination via the neurite density index (NDI) and dispersion via the orientation dispersion index (ODI), with potential to more accurately evaluate microstructural alterations in the developing brain. Yet, no study has used these indices to examine associations between PFC microstructure and concurrent or developing infant emotionality.
Methods
We modeled PFC subregional NDI and ODI at 3 months with caregiver-reported infant NE and PE at 3 months (n = 61) and at 9 months (n = 50), using multivariable and subsequent bivariate regression models.
Results
The most robust statistically significant findings were positive associations among 3-month rostral anterior cingulate cortex (ACC) ODI and caudal ACC NDI and concurrent NE, a positive association between 3-month lateral orbitofrontal cortex ODI and prospective NE, and a negative association between 3-month dorsolateral PFC ODI and concurrent PE. Multivariate models also revealed that other PFC subregional microstructure measures, as well as infant and caregiver sociodemographic and clinical factors, predicted infant 3- and 9-month NE and PE.
Conclusions
Greater NDI and ODI, reflecting greater microstructural complexity, in PFC regions supporting salience perception (rostral ACC), decision making (lateral orbitofrontal cortex), action selection (caudal ACC), and attentional processes (dorsolateral PFC) might result in greater integration of these subregions with other neural networks and greater attention to salient negative external cues, thus higher NE and/or lower PE. These findings provide potential infant cortical markers of future psychopathology risk.
期刊介绍:
Biological Psychiatry is an official journal of the Society of Biological Psychiatry and was established in 1969. It is the first journal in the Biological Psychiatry family, which also includes Biological Psychiatry: Cognitive Neuroscience and Neuroimaging and Biological Psychiatry: Global Open Science. The Society's main goal is to promote excellence in scientific research and education in the fields related to the nature, causes, mechanisms, and treatments of disorders pertaining to thought, emotion, and behavior. To fulfill this mission, Biological Psychiatry publishes peer-reviewed, rapid-publication articles that present new findings from original basic, translational, and clinical mechanistic research, ultimately advancing our understanding of psychiatric disorders and their treatment. The journal also encourages the submission of reviews and commentaries on current research and topics of interest.