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Age, Motion, Medical, and Psychiatric Associations With Incidental Findings in Brain MRI

Tobe, Russell H; Tu, Lucia; Roberts, Maya; Kiar, Gregory; Breland, Melissa M; Tian, Yiwen; Kang, Minji; Ross, Rachel; Ryan, Margaret M; Valenza, Emmanuel; Alexander, Lindsay; MacKay-Brandt, Anna; Colcombe, Stanley J; Franco, Alexandre R; Milham, Michael P
IMPORTANCE/UNASSIGNED:Few investigations have evaluated rates of brain-based magnetic resonance imaging (MRI) incidental findings (IFs) in large lifespan samples, their stability over time, or their associations with health outcomes. OBJECTIVES/UNASSIGNED:To examine rates of brain-based IFs across the lifespan, their persistence, and their associations with phenotypic indicators of behavior, cognition, and health; to compare quantified motion with radiologist-reported motion and evaluate its associations with IF rates; and to explore IF consistency across multiple visits. DESIGN, SETTING, AND PARTICIPANTS/UNASSIGNED:This cross-sectional study included participants from the Nathan Kline Institute-Rockland Sample (NKI-RS), a lifespan community-ascertained sample, and the Healthy Brain Network (HBN), a cross-sectional community self-referred pediatric sample focused on mental health and learning disorders. The NKI-RS enrolled participants (ages 6-85 years) between March 2012 and March 2020 and had longitudinal participants followed up for as long as 4 years. The HBN enrolled participants (ages 5-21 years) between August 2015 and October 2021. Clinical neuroradiology MRI reports were coded for radiologist-reported motion as well as presence, type, and clinical urgency (category 1, no abnormal findings; 2, no referral recommended; 3, consider referral; and 4, immediate referral) of IFs. MRI reports were coded from June to October 2021. Data were analyzed from November 2021 to February 2023. MAIN OUTCOMES AND MEASURES/UNASSIGNED:Rates and type of IFs by demographic characteristics, health phenotyping, and motion artifacts; longitudinal stability of IFs; and Euler number in projecting radiologist-reported motion. RESULTS/UNASSIGNED:A total of 1300 NKI-RS participants (781 [60.1%] female; mean [SD] age, 38.9 [21.8] years) and 2772 HBN participants (976 [35.2%] female; mean [SD] age, 10.0 [3.5] years) had health phenotyping and neuroradiology-reviewed MRI scans. IFs were common, with 284 of 2956 children (9.6%) and 608 of 1107 adults (54.9%) having IFs, but rarely of clinical concern (category 1: NKI-RS, 619 [47.6%]; HBN, 2561 [92.4%]; category 2: NKI-RS, 647 [49.8%]; HBN, 178 [6.4%]; category 3: NKI-RS, 79 [6.1%]; HBN, 30 [1.1%]; category 4: NKI-RS: 12 [0.9%]; HBN, 6 [0.2%]). Overall, 46 children (1.6%) and 79 adults (7.1%) required referral for their IFs. IF frequency increased with age. Elevated blood pressure and BMI were associated with increased T2 hyperintensities and age-related cortical atrophy. Radiologist-reported motion aligned with Euler-quantified motion, but neither were associated with IF rates. CONCLUSIONS AND RELEVANCE/UNASSIGNED:In this cross-sectional study, IFs were common, particularly with increasing age, although rarely clinically significant. While T2 hyperintensity and age-related cortical atrophy were associated with BMI and blood pressure, IFs were not associated with other behavioral, cognitive, and health phenotyping. Motion may not limit clinical IF detection.
PMCID:10865144
PMID: 38349653
ISSN: 2574-3805
CID: 5635302

An open-access dataset of naturalistic viewing using simultaneous EEG-fMRI

Telesford, Qawi K; Gonzalez-Moreira, Eduardo; Xu, Ting; Tian, Yiwen; Colcombe, Stanley J; Cloud, Jessica; Russ, Brian E; Falchier, Arnaud; Nentwich, Maximilian; Madsen, Jens; Parra, Lucas C; Schroeder, Charles E; Milham, Michael P; Franco, Alexandre R
In this work, we present a dataset that combines functional magnetic imaging (fMRI) and electroencephalography (EEG) to use as a resource for understanding human brain function in these two imaging modalities. The dataset can also be used for optimizing preprocessing methods for simultaneously collected imaging data. The dataset includes simultaneously collected recordings from 22 individuals (ages: 23-51) across various visual and naturalistic stimuli. In addition, physiological, eye tracking, electrocardiography, and cognitive and behavioral data were collected along with this neuroimaging data. Visual tasks include a flickering checkerboard collected outside and inside the MRI scanner (EEG-only) and simultaneous EEG-fMRI recordings. Simultaneous recordings include rest, the visual paradigm Inscapes, and several short video movies representing naturalistic stimuli. Raw and preprocessed data are openly available to download. We present this dataset as part of an effort to provide open-access data to increase the opportunity for discoveries and understanding of the human brain and evaluate the correlation between electrical brain activity and blood oxygen level-dependent (BOLD) signals.
PMCID:10447527
PMID: 37612297
ISSN: 2052-4463
CID: 5596052

Specific and common functional connectivity deficits in drug-free generalized anxiety disorder and panic disorder: A data-driven analysis

Li, Wei; Cui, Huiru; Li, Hui; Colcombe, Stan; Smith, Robert C; Cao, Xinyi; Pang, Jiaoyan; Hu, Qiang; Zhang, Lanlan; Yang, Zhi; Wang, Jijun; Li, Chunbo
Evidence of comparing neural network differences between anxiety disorder subtypes is limited, while it is crucial to reveal the pathogenesis of anxiety disorders. The present study aimed to investigate specific and common resting-state functional connectivity (FC) networks in generalized anxiety disorder (GAD), panic disorder (PD), and healthy controls (HC). We employed the gRAICAR algorithm to decompose the resting-state fMRI into independent components and align the components across 61 subjects (22 GAD, 18 PD and 21 HC). The default mode network and precuneus network exhibited GAD-specific aberrance, the anterior default mode network showed atypicality specific to PD, and the right fronto-parietal network showed aberrance common to GAD and PD. Between GAD-specific networks, FC between bilateral dorsolateral prefrontal cortex (DLPFC) was positively correlated with interoceptive sensitivity. In the common network, altered FCs between DLPFC and angular gyrus, and between orbitofrontal cortex and precuneus, were positively correlated with anxiety severity and interoceptive sensitivity. The pathological mechanism of PD could closely relate to the dysfunction of prefrontal cortex, while GAD could involve more extensive brain areas, which may be related to fear generalization.
PMID: 36459805
ISSN: 1872-7123
CID: 5374172

A longitudinal resource for studying connectome development and its psychiatric associations during childhood

Tobe, Russell H; MacKay-Brandt, Anna; Lim, Ryan; Kramer, Melissa; Breland, Melissa M; Tu, Lucia; Tian, Yiwen; Trautman, Kristin Dietz; Hu, Caixia; Sangoi, Raj; Alexander, Lindsay; Gabbay, Vilma; Castellanos, F Xavier; Leventhal, Bennett L; Craddock, R Cameron; Colcombe, Stanley J; Franco, Alexandre R; Milham, Michael P
Most psychiatric disorders are chronic, associated with high levels of disability and distress, and present during pediatric development. Scientific innovation increasingly allows researchers to probe brain-behavior relationships in the developing human. As a result, ambitions to (1) establish normative pediatric brain development trajectories akin to growth curves, (2) characterize reliable metrics for distinguishing illness, and (3) develop clinically useful tools to assist in the diagnosis and management of mental health and learning disorders have gained significant momentum. To this end, the NKI-Rockland Sample initiative was created to probe lifespan development as a large-scale multimodal dataset. The NKI-Rockland Sample Longitudinal Discovery of Brain Development Trajectories substudy (N = 369) is a 24- to 30-month multi-cohort longitudinal pediatric investigation (ages 6.0-17.0 at enrollment) carried out in a community-ascertained sample. Data include psychiatric diagnostic, medical, behavioral, and cognitive phenotyping, as well as multimodal brain imaging (resting fMRI, diffusion MRI, morphometric MRI, arterial spin labeling), genetics, and actigraphy. Herein, we present the rationale, design, and implementation of the Longitudinal Discovery of Brain Development Trajectories protocol.
PMCID:9197863
PMID: 35701428
ISSN: 2052-4463
CID: 5277832

Toward next-generation primate neuroscience: A collaboration-based strategic plan for integrative neuroimaging

Milham, Michael; Petkov, Chris; Belin, Pascal; Ben Hamed, Suliann; Evrard, Henry; Fair, Damien; Fox, Andrew; Froudist-Walsh, Sean; Hayashi, Takuya; Kastner, Sabine; Klink, Chris; Majka, Piotr; Mars, Rogier; Messinger, Adam; Poirier, Colline; Schroeder, Charles; Shmuel, Amir; Silva, Afonso C; Vanduffel, Wim; Van Essen, David C; Wang, Zheng; Roe, Anna Wang; Wilke, Melanie; Xu, Ting; Aarabi, Mohammad Hadi; Adolphs, Ralph; Ahuja, Aarit; Alvand, Ashkan; Amiez, Celine; Autio, Joonas; Azadi, Reza; Baeg, Eunha; Bai, Ruiliang; Bao, Pinglei; Basso, Michele; Behel, Austin K; Bennett, Yvonne; Bernhardt, Boris; Biswal, Bharat; Boopathy, Sethu; Boretius, Susann; Borra, Elena; Boshra, Rober; Buffalo, Elizabeth; Cao, Long; Cavanaugh, James; Celine, Amiez; Chavez, Gianfranco; Chen, Li Min; Chen, Xiaodong; Cheng, Luqi; Chouinard-Decorte, Francois; Clavagnier, Simon; Cléry, Justine; Colcombe, Stan J; Conway, Bevil; Cordeau, Melina; Coulon, Olivier; Cui, Yue; Dadarwal, Rakshit; Dahnke, Robert; Desrochers, Theresa; Deying, Li; Dougherty, Kacie; Doyle, Hannah; Drzewiecki, Carly M; Duyck, Marianne; Arachchi, Wasana Ediri; Elorette, Catherine; Essamlali, Abdelhadi; Evans, Alan; Fajardo, Alfonso; Figueroa, Hector; Franco, Alexandre; Freches, Guilherme; Frey, Steve; Friedrich, Patrick; Fujimoto, Atsushi; Fukunaga, Masaki; Gacoin, Maeva; Gallardo, Guillermo; Gao, Lixia; Gao, Yang; Garside, Danny; Garza-Villarreal, Eduardo A; Gaudet-Trafit, Maxime; Gerbella, Marzio; Giavasis, Steven; Glen, Daniel; Ribeiro Gomes, Ana Rita; Torrecilla, Sandra Gonzalez; Gozzi, Alessandro; Gulli, Roberto; Haber, Suzanne; Hadj-Bouziane, Fadila; Fujimoto, Satoka Hashimoto; Hawrylycz, Michael; He, Quansheng; He, Ye; Heuer, Katja; Hiba, Bassem; Hoffstaedter, Felix; Hong, Seok-Jun; Hori, Yuki; Hou, Yujie; Howard, Amy; de la Iglesia-Vaya, Maria; Ikeda, Takuro; Jankovic-Rapan, Lucija; Jaramillo, Jorge; Jedema, Hank P; Jin, Hecheng; Jiang, Minqing; Jung, Benjamin; Kagan, Igor; Kahn, Itamar; Kiar, Gregory; Kikuchi, Yuki; Kilavik, Bjørg; Kimura, Nobuyuki; Klatzmann, Ulysse; Kwok, Sze Chai; Lai, Hsin-Yi; Lamberton, Franck; Lehman, Julia; Li, Pengcheng; Li, Xinhui; Li, Xinjian; Liang, Zhifeng; Liston, Conor; Little, Roger; Liu, Cirong; Liu, Ning; Liu, Xiaojin; Liu, Xinyu; Lu, Haidong; Loh, Kep Kee; Madan, Christopher; Magrou, Loïc; Margulies, Daniel; Mathilda, Froesel; Mejia, Sheyla; Meng, Yao; Menon, Ravi; Meunier, David; Mitchell, A J; Mitchell, Anna; Murphy, Aidan; Mvula, Towela; Ortiz-Rios, Michael; Ortuzar Martinez, Diego Emanuel; Pagani, Marco; Palomero-Gallagher, Nicola; Pareek, Vikas; Perkins, Pierce; Ponce, Fernanda; Postans, Mark; Pouget, Pierre; Qian, Meizhen; Ramirez, Julian Bene; Raven, Erika; Restrepo, Isabel; Rima, Samy; Rockland, Kathleen; Rodriguez, Nadira Yusif; Roger, Elise; Hortelano, Eduardo Rojas; Rosa, Marcello; Rossi, Andrew; Rudebeck, Peter; Russ, Brian; Sakai, Tomoko; Saleem, Kadharbatcha S; Sallet, Jerome; Sawiak, Stephen; Schaeffer, David; Schwiedrzik, Caspar M; Seidlitz, Jakob; Sein, Julien; Sharma, Jitendra; Shen, Kelly; Sheng, Wei-An; Shi, Neo Sunhang; Shim, Won Mok; Simone, Luciano; Sirmpilatze, Nikoloz; Sivan, Virginie; Song, Xiaowei; Tanenbaum, Aaron; Tasserie, Jordy; Taylor, Paul; Tian, Xiaoguang; Toro, Roberto; Trambaiolli, Lucas; Upright, Nick; Vezoli, Julien; Vickery, Sam; Villalon, Julio; Wang, Xiaojie; Wang, Yufan; Weiss, Alison R; Wilson, Charlie; Wong, Ting-Yat; Woo, Choong-Wan; Wu, Bichan; Xiao, Du; Xu, Augix Guohua; Xu, Dongrong; Xufeng, Zhou; Yacoub, Essa; Ye, Ningrong; Ying, Zhang; Yokoyama, Chihiro; Yu, Xiongjie; Yue, Shasha; Yuheng, Lu; Yumeng, Xin; Zaldivar, Daniel; Zhang, Shaomin; Zhao, Yuguang; Zuo, Zhanguang
Open science initiatives are creating opportunities to increase research coordination and impact in nonhuman primate (NHP) imaging. The PRIMatE Data and Resource Exchange community recently developed a collaboration-based strategic plan to advance NHP imaging as an integrative approach for multiscale neuroscience.
PMID: 34731649
ISSN: 1097-4199
CID: 5499342

Predicting multiscan MRI outcomes in children with neurodevelopmental conditions following MRI simulator training

Simhal, Anish K; Filho, José O A; Segura, Patricia; Cloud, Jessica; Petkova, Eva; Gallagher, Richard; Castellanos, F Xavier; Colcombe, Stan; Milham, Michael P; Di Martino, Adriana
Pediatric brain imaging holds significant promise for understanding neurodevelopment. However, the requirement to remain still inside a noisy, enclosed scanner remains a challenge. Verbal or visual descriptions of the process, and/or practice in MRI simulators are the norm in preparing children. Yet, the factors predictive of successfully obtaining neuroimaging data remain unclear. We examined data from 250 children (6-12 years, 197 males) with autism and/or attention-deficit/hyperactivity disorder. Children completed systematic MRI simulator training aimed to habituate to the scanner environment and minimize head motion. An MRI session comprised multiple structural, resting-state, task and diffusion scans. Of the 201 children passing simulator training and attempting scanning, nearly all (94%) successfully completed the first structural scan in the sequence, and 88% also completed the following functional scan. The number of successful scans decreased as the sequence progressed. Multivariate analyses revealed that age was the strongest predictor of successful scans in the session, with younger children having lower success rates. After age, sensorimotor atypicalities contributed most to prediction. Results provide insights on factors to consider in designing pediatric brain imaging protocols.
PMCID:8517836
PMID: 34649041
ISSN: 1878-9307
CID: 5068032

Is it time to switch your T1W sequence? Assessing the impact of prospective motion correction on the reliability and quality of structural imaging

Ai, Lei; Craddock, R Cameron; Tottenham, Nim; Dyke, Jonathan P; Lim, Ryan; Colcombe, Stanley; Milham, Michael; Franco, Alexandre R
New large neuroimaging studies, such as the Adolescent Brain Cognitive Development study (ABCD) and Human Connectome Project (HCP) Development studies are adopting a new T1-weighted imaging sequence with prospective motion correction (PMC) in favor of the more traditional 3-Dimensional Magnetization-Prepared Rapid Gradient-Echo Imaging (MPRAGE) sequence. Here, we used a developmental dataset (ages 5-21, N = 348) from the Healthy Brain Network (HBN) Initiative to directly compare two widely used MRI structural sequences: one based on the Human Connectome Project (MPRAGE) and another based on the ABCD study (MPRAGE+PMC). We aimed to determine if the morphometric measurements obtained from both protocols are equivalent or if one sequence has a clear advantage over the other. The sequences were also compared through quality control measurements. Inter- and intra-sequence reliability were assessed with another set of participants (N = 71) from HBN that performed two MPRAGE and two MPRAGE+PMC sequences within the same imaging session, with one MPRAGE (MPRAGE1) and MPRAGE+PMC (MPRAGE+PMC1) pair at the beginning of the session and another pair (MPRAGE2 and MPRAGE+PMC2) at the end of the session. Intraclass correlation coefficients (ICC) scores for morphometric measurements such as volume and cortical thickness showed that intra-sequence reliability is the highest with the two MPRAGE+PMC sequences and lowest with the two MPRAGE sequences. Regarding inter-sequence reliability, ICC scores were higher for the MPRAGE1 - MPRAGE+PMC1 pair at the beginning of the session than the MPRAGE1 - MPRAGE2 pair, possibly due to the higher motion artifacts in the MPRAGE2 run. Results also indicated that the MPRAGE+PMC sequence is robust, but not impervious, to high head motion. For quality control metrics, the traditional MPRAGE yielded better results than MPRAGE+PMC in 5 of the 8 measurements. In conclusion, morphometric measurements evaluated here showed high inter-sequence reliability between the MPRAGE and MPRAGE+PMC sequences, especially in images with low head motion. We suggest that studies targeting hyperkinetic populations use the MPRAGE+PMC sequence, given its robustness to head motion and higher reliability scores. However, neuroimaging researchers studying non-hyperkinetic participants can choose either MPRAGE or MPRAGE+PMC sequences, but should carefully consider the apparent tradeoff between relatively increased reliability, but reduced quality control metrics when using the MPRAGE+PMC sequence.
PMID: 33248256
ISSN: 1095-9572
CID: 4734762

Measurement reliability for individual differences in multilayer network dynamics: Cautions and considerations

Yang, Zhen; Telesford, Qawi K; Franco, Alexandre R; Lim, Ryan; Gu, Shi; Xu, Ting; Ai, Lei; Castellanos, Francisco X; Yan, Chao-Gan; Colcombe, Stan; Milham, Michael P
Multilayer network models have been proposed as an effective means of capturing the dynamic configuration of distributed neural circuits and quantitatively describing how communities vary over time. Beyond general insights into brain function, a growing number of studies have begun to employ these methods for the study of individual differences. However, test-retest reliabilities for multilayer network measures have yet to be fully quantified or optimized, potentially limiting their utility for individual difference studies. Here, we systematically evaluated the impact of multilayer community detection algorithms, selection of network parameters, scan duration, and task condition on test-retest reliabilities of multilayer network measures (i.e., flexibility, integration, and recruitment). A key finding was that the default method used for community detection by the popular generalized Louvain algorithm can generate erroneous results. Although available, an updated algorithm addressing this issue is yet to be broadly adopted in the neuroimaging literature. Beyond the algorithm, the present work identified parameter selection as a key determinant of test-retest reliability; however, optimization of these parameters and expected reliabilities appeared to be dataset-specific. Once parameters were optimized, consistent with findings from the static functional connectivity literature, scan duration was a much stronger determinant of reliability than scan condition. When the parameters were optimized and scan duration was sufficient, both passive (i.e., resting state, Inscapes, and movie) and active (i.e., flanker) tasks were reliable, although reliability in the movie watching condition was significantly higher than in the other three tasks. The minimal data requirement for achieving reliable measures for the movie watching condition was 20 min, and 30 min for the other three tasks. Our results caution the field against the use of default parameters without optimization based on the specific datasets to be employed - a process likely to be limited for most due to the lack of test-retest samples to enable parameter optimization.
PMID: 33130272
ISSN: 1095-9572
CID: 4684102

Evaluating fMRI-Based Estimation of Eye Gaze During Naturalistic Viewing

Son, Jake; Ai, Lei; Lim, Ryan; Xu, Ting; Colcombe, Stanley; Franco, Alexandre Rosa; Cloud, Jessica; LaConte, Stephen; Lisinski, Jonathan; Klein, Arno; Craddock, R Cameron; Milham, Michael
The collection of eye gaze information during functional magnetic resonance imaging (fMRI) is important for monitoring variations in attention and task compliance, particularly for naturalistic viewing paradigms (e.g., movies). However, the complexity and setup requirements of current in-scanner eye tracking solutions can preclude many researchers from accessing such information. Predictive eye estimation regression (PEER) is a previously developed support vector regression-based method for retrospectively estimating eye gaze from the fMRI signal in the eye's orbit using a 1.5-min calibration scan. Here, we provide confirmatory validation of the PEER method's ability to infer eye gaze on a TR-by-TR basis during movie viewing, using simultaneously acquired eye tracking data in five individuals (median angular deviation < 2°). Then, we examine variations in the predictive validity of PEER models across individuals in a subset of data (n = 448) from the Child Mind Institute Healthy Brain Network Biobank, identifying head motion as a primary determinant. Finally, we accurately classify which of the two movies is being watched based on the predicted eye gaze patterns (area under the curve = 0.90 ± 0.02) and map the neural correlates of eye movements derived from PEER. PEER is a freely available and easy-to-use tool for determining eye fixations during naturalistic viewing.
PMID: 31595961
ISSN: 1460-2199
CID: 4150762

Concerns regarding the prediction of behavioral measures from multilayer network switching [Letter]

Yang, Zhen; Telesford, Qawi K; Franco, Alexandre R; Xu, Ting; Colcombe, Stan; Milham, Michael P
PMCID:6708307
PMID: 31409701
ISSN: 1091-6490
CID: 4150752