Structural covariance of the ventral visual stream predicts posttraumatic intrusion and nightmare symptoms: a multivariate data fusion analysis

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Abstract

Visual components of trauma memories are often vividly re-experienced by survivors with deleterious consequences for normal function. Neuroimaging research on trauma has primarily focused on threat-processing circuitry as core to trauma-related dysfunction. Conversely, limited attention has been given to visual circuitry which may be particularly relevant to posttraumatic stress disorder (PTSD). Prior work suggests that the ventral visual stream is directly related to the cognitive and affective disturbances observed in PTSD and may be predictive of later symptom expression. The present study used multimodal magnetic resonance imaging data ( n = 278) collected two weeks after trauma exposure from the AURORA study, a longitudinal, multisite investigation of adverse posttraumatic neuropsychiatric sequelae. Indices of gray and white matter were combined using data fusion to identify a structural covariance network (SCN) of the ventral visual stream 2 weeks after trauma. Participant’s loadings on the SCN were positively associated with both intrusion symptoms and intensity of nightmares. Further, SCN loadings moderated connectivity between a previously observed amygdala-hippocampal functional covariance network and the inferior temporal gyrus. Follow-up MRI data at 6 months showed an inverse relationship between SCN loadings and negative alterations in cognition in mood. Further, individuals who showed decreased strength of the SCN between 2 weeks and 6 months had generally higher PTSD symptom severity over time. The present findings highlight a role for structural integrity of the ventral visual stream in the development of PTSD. The ventral visual stream may be particularly important for the consolidation or retrieval of trauma memories and may contribute to efficient reactivation of visual components of the trauma memory, thereby exacerbating PTSD symptoms. Potentially chronic engagement of the network may lead to reduced structural integrity which becomes a risk factor for lasting PTSD symptoms.

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Advances in functional and structural MR image analysis and implementation as FSL.

Stephen M Smith, Mark Jenkinson, Mark Woolrich … (2005)

The techniques available for the interrogation and analysis of neuroimaging data have a large influence in determining the flexibility, sensitivity, and scope of neuroimaging experiments. The development of such methodologies has allowed investigators to address scientific questions that could not previously be answered and, as such, has become an important research area in its own right. In this paper, we present a review of the research carried out by the Analysis Group at the Oxford Centre for Functional MRI of the Brain (FMRIB). This research has focussed on the development of new methodologies for the analysis of both structural and functional magnetic resonance imaging data. The majority of the research laid out in this paper has been implemented as freely available software tools within FMRIB's Software Library (FSL).

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An integrated approach to correction for off-resonance effects and subject movement in diffusion MR imaging

Jesper L.R. Andersson, Stamatios N. Sotiropoulos (2016)

In this paper we describe a method for retrospective estimation and correction of eddy current (EC)-induced distortions and subject movement in diffusion imaging. In addition a susceptibility-induced field can be supplied and will be incorporated into the calculations in a way that accurately reflects that the two fields (susceptibility- and EC-induced) behave differently in the presence of subject movement. The method is based on registering the individual volumes to a model free prediction of what each volume should look like, thereby enabling its use on high b-value data where the contrast is vastly different in different volumes. In addition we show that the linear EC-model commonly used is insufficient for the data used in the present paper (high spatial and angular resolution data acquired with Stejskal–Tanner gradients on a 3 T Siemens Verio, a 3 T Siemens Connectome Skyra or a 7 T Siemens Magnetome scanner) and that a higher order model performs significantly better. The method is already in extensive practical use and is used by four major projects (the WU-UMinn HCP, the MGH HCP, the UK Biobank and the Whitehall studies) to correct for distortions and subject movement.

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Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data.

Stephen Smith, Mark Jenkinson, Heidi Johansen-Berg … (2006)

There has been much recent interest in using magnetic resonance diffusion imaging to provide information about anatomical connectivity in the brain, by measuring the anisotropic diffusion of water in white matter tracts. One of the measures most commonly derived from diffusion data is fractional anisotropy (FA), which quantifies how strongly directional the local tract structure is. Many imaging studies are starting to use FA images in voxelwise statistical analyses, in order to localise brain changes related to development, degeneration and disease. However, optimal analysis is compromised by the use of standard registration algorithms; there has not to date been a satisfactory solution to the question of how to align FA images from multiple subjects in a way that allows for valid conclusions to be drawn from the subsequent voxelwise analysis. Furthermore, the arbitrariness of the choice of spatial smoothing extent has not yet been resolved. In this paper, we present a new method that aims to solve these issues via (a) carefully tuned non-linear registration, followed by (b) projection onto an alignment-invariant tract representation (the "mean FA skeleton"). We refer to this new approach as Tract-Based Spatial Statistics (TBSS). TBSS aims to improve the sensitivity, objectivity and interpretability of analysis of multi-subject diffusion imaging studies. We describe TBSS in detail and present example TBSS results from several diffusion imaging studies.

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Author and article information

Contributors

Nathaniel G. Harnett: nharnett@mclean.harvard.edu

Journal

Journal ID (nlm-ta): Transl Psychiatry

Journal ID (iso-abbrev): Transl Psychiatry

Title: Translational Psychiatry

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2158-3188

Publication date (Electronic): 8 August 2022

Publication date PMC-release: 8 August 2022

Publication date Collection: 2022

Volume: 12

Electronic Location Identifier: 321

Affiliations

[1 ]GRID grid.240206.2, ISNI 0000 0000 8795 072X, Division of Depression and Anxiety, , McLean Hospital, ; Belmont, MA USA

[2 ]GRID grid.38142.3c, ISNI 000000041936754X, Department of Psychiatry, , Harvard Medical School, ; Boston, MA USA

[3 ]GRID grid.189967.8, ISNI 0000 0001 0941 6502, Department of Psychiatry and Behavioral Sciences, , Emory University School of Medicine, ; Atlanta, GA USA

[4 ]GRID grid.264727.2, ISNI 0000 0001 2248 3398, Department of Psychology, , Temple University, ; Philadelphia, PA USA

[5 ]GRID grid.254444.7, ISNI 0000 0001 1456 7807, Department of Psychiatry and Behavioral Neurosciences, , Wayne State University, ; Detroit, MI USA

[6 ]GRID grid.266757.7, ISNI 0000000114809378, Department of Psychological Sciences, , University of Missouri - St. Louis, ; St. Louis, MO USA

[7 ]GRID grid.4367.6, ISNI 0000 0001 2355 7002, Department of Emergency Medicine, , Washington University School of Medicine, ; St. Louis, MO USA

[8 ]GRID grid.40263.33, ISNI 0000 0004 1936 9094, Department of Emergency Medicine & Department of Health Services, Policy, and Practice, , The Alpert Medical School of Brown University, Rhode Island Hospital and The Miriam Hospital, ; Providence, RI USA

[9 ]GRID grid.10698.36, ISNI 0000000122483208, Institute for Trauma Recovery, Department of Anesthesiology, , University of North Carolina at Chapel Hill, ; Chapel Hill, NC USA

[10 ]GRID grid.410711.2, ISNI 0000 0001 1034 1720, Department of Biostatistics, Gillings School of Global Public Health, , University of North Carolina, ; Chapel Hill, NC USA

[11 ]GRID grid.266102.1, ISNI 0000 0001 2297 6811, Departments of Psychiatry and Neurology, , University of California San Francisco, ; San Francisco, CA USA

[12 ]GRID grid.189967.8, ISNI 0000 0001 0941 6502, Department of Biomedical Informatics, , Emory University School of Medicine, ; Atlanta, GA USA

[13 ]GRID grid.213917.f, ISNI 0000 0001 2097 4943, Department of Biomedical Engineering, , Georgia Institute of Technology and Emory University, ; Atlanta, GA USA

[14 ]GRID grid.240206.2, ISNI 0000 0000 8795 072X, Institute for Technology in Psychiatry, , McLean Hospital, ; Belmont, MA USA

[15 ]The Many Brains Project, Belmont, MA USA

[16 ]GRID grid.10698.36, ISNI 0000000122483208, Department of Psychology and Neuroscience & Department of Sociology, , University of North Carolina at Chapel Hill, ; Chapel Hill, NC USA

[17 ]GRID grid.240206.2, ISNI 0000 0000 8795 072X, Department of Psychiatry, , McLean Hospital, ; Belmont, MA USA

[18 ]GRID grid.168645.8, ISNI 0000 0001 0742 0364, Department of Emergency Medicine, , University of Massachusetts Chan Medical School, ; Worcester, MA USA

[19 ]GRID grid.412807.8, ISNI 0000 0004 1936 9916, Department of Emergency Medicine, , Vanderbilt University Medical Center, ; Nashville, TN USA

[20 ]GRID grid.239864.2, ISNI 0000 0000 8523 7701, Department of Emergency Medicine, , Henry Ford Health System, ; Detroit, MI USA

[21 ]GRID grid.257413.6, ISNI 0000 0001 2287 3919, Department of Emergency Medicine, , Indiana University School of Medicine, ; Indianapolis, IN USA

[22 ]GRID grid.413116.0, ISNI 0000 0004 0625 1409, Department of Emergency Medicine, , University of Florida College of Medicine-Jacksonville, ; Jacksonville, FL USA

[23 ]GRID grid.411897.2, ISNI 0000 0004 6070 865X, Department of Emergency Medicine, , Cooper Medical School of Rowan University, ; Camden, NJ USA

[24 ]GRID grid.261331.4, ISNI 0000 0001 2285 7943, Department of Emergency Medicine, , Ohio State University College of Medicine, ; Columbus, OH USA

[25 ]GRID grid.261331.4, ISNI 0000 0001 2285 7943, Ohio State University College of Nursing, ; Columbus, OH USA

[26 ]GRID grid.265892.2, ISNI 0000000106344187, Department of Emergency Medicine, , University of Alabama School of Medicine, ; Birmingham, AL USA

[27 ]GRID grid.265892.2, ISNI 0000000106344187, Department of Surgery, Division of Acute Care Surgery, , University of Alabama School of Medicine, ; Birmingham, AL USA

[28 ]GRID grid.265892.2, ISNI 0000000106344187, Center for Injury Science, , University of Alabama at Birmingham, ; Birmingham, AL USA

[29 ]GRID grid.261277.7, ISNI 0000 0001 2219 916X, Department of Emergency Medicine, , Oakland University William Beaumont School of Medicine, ; Rochester, MI USA

[30 ]GRID grid.189967.8, ISNI 0000 0001 0941 6502, Department of Emergency Medicine, , Emory University School of Medicine, ; Atlanta, GA USA

[31 ]GRID grid.25879.31, ISNI 0000 0004 1936 8972, Department of Surgery, Department of Neurosurgery, , University of Pennsylvania, ; Philadelphia, PA USA

[32 ]GRID grid.25879.31, ISNI 0000 0004 1936 8972, Perelman School of Medicine, , University of Pennsylvania, ; Philadelphia, PA USA

[33 ]GRID grid.25879.31, ISNI 0000 0004 1936 8972, Department of Surgery, Division of Traumatology, Surgical Critical Care and Emergency Surgery, , University of Pennsylvania, ; Philadelphia, PA USA

[34 ]GRID grid.239276.b, ISNI 0000 0001 2181 6998, Einstein Medical Center, ; Philadelphia, PA USA

[35 ]GRID grid.429808.f, ISNI 0000 0004 0419 595X, Department of Emergency Medicine, , Jefferson University Hospitals, ; Philadelphia, PA USA

[36 ]GRID grid.254444.7, ISNI 0000 0001 1456 7807, Department of Emergency Medicine, , Wayne State University, Ascension St. John Hospital, ; Detroit, MI USA

[37 ]GRID grid.32224.35, ISNI 0000 0004 0386 9924, Department of Emergency Medicine, , Massachusetts General Hospital, ; Boston, MA USA

[38 ]GRID grid.416444.7, ISNI 0000 0004 0370 2980, Department of Emergency Medicine, , Saint Joseph Mercy Hospital, ; Ypsilanti, MI USA

[39 ]GRID grid.266683.f, ISNI 0000 0001 2166 5835, Department of Emergency Medicine, , University of Massachusetts Medical School-Baystate, ; Springfield, MA USA

[40 ]GRID grid.254444.7, ISNI 0000 0001 1456 7807, Department of Emergency Medicine, , Wayne State University, Detroit Receiving Hospital, ; Detroit, MI USA

[41 ]GRID grid.267308.8, ISNI 0000 0000 9206 2401, Department of Emergency Medicine, McGovern Medical School, , University of Texas Health, ; Houston, TX USA

[42 ]GRID grid.62560.37, ISNI 0000 0004 0378 8294, Department of Emergency Medicine, , Brigham and Women’s Hospital, ; Boston, MA USA

[43 ]GRID grid.38142.3c, ISNI 000000041936754X, Department of Emergency Medicine, , Harvard Medical School, ; Boston, MA USA

[44 ]GRID grid.410370.1, ISNI 0000 0004 4657 1992, National Center for PTSD, Behavioral Science Division, , VA Boston Healthcare System, ; Boston, MA USA

[45 ]GRID grid.189504.1, ISNI 0000 0004 1936 7558, Department of Psychiatry, , Boston University School of Medicine, ; Boston, MA USA

[46 ]GRID grid.281208.1, ISNI 0000 0004 0419 3073, National Center for PTSD, Clinical Neurosciences Division, , VA Connecticut Healthcare System, ; West Haven, CT USA

[47 ]GRID grid.47100.32, ISNI 0000000419368710, Department of Psychiatry, , Yale School of Medicine, ; New Haven, CT USA

[48 ]GRID grid.47100.32, ISNI 0000000419368710, Department of Psychology, , Yale University, ; New Haven, CT USA

[49 ]GRID grid.4367.6, ISNI 0000 0001 2355 7002, Department of Psychological & Brain Sciences, , Washington University in St. Louis, ; St. Louis, MO USA

[50 ]GRID grid.261331.4, ISNI 0000 0001 2285 7943, Division of Biosciences, , Ohio State University College of Dentistry, ; Columbus, OH USA

[51 ]GRID grid.261331.4, ISNI 0000 0001 2285 7943, Institute for Behavioral Medicine Research, , OSU Wexner Medical Center, ; Columbus, OH USA

[52 ]GRID grid.214458.e, ISNI 0000000086837370, Department of Anesthesiology, , University of Michigan Medical School, ; Ann Arbor, MI USA

[53 ]GRID grid.214458.e, ISNI 0000000086837370, Department of Internal Medicine-Rheumatology, , University of Michigan Medical School, ; Ann Arbor, MI USA

[54 ]GRID grid.1013.3, ISNI 0000 0004 1936 834X, Kolling Institute, , University of Sydney, ; St Leonards, New South Wales Australia

[55 ]GRID grid.1013.3, ISNI 0000 0004 1936 834X, Faculty of Medicine and Health, , University of Sydney, Northern Sydney Local Health District, ; New South Wales, Australia

[56 ]GRID grid.16753.36, ISNI 0000 0001 2299 3507, Physical Therapy & Human Movement Sciences, Feinberg School of Medicine, , Northwestern University, ; Chicago, IL USA

[57 ]GRID grid.38142.3c, ISNI 000000041936754X, Department of Health Care Policy, , Harvard Medical School, ; Boston, MA USA

[58 ]GRID grid.38142.3c, ISNI 000000041936754X, Department of Epidemiology, Harvard T.H. Chan School of Public Health, , Harvard University, ; Boston, MA USA

[59 ]GRID grid.10698.36, ISNI 0000000122483208, Department of Emergency Medicine, , University of North Carolina at Chapel Hill, ; Chapel Hill, NC USA

[60 ]GRID grid.10698.36, ISNI 0000000122483208, Institute for Trauma Recovery, Department of Psychiatry, , University of North Carolina at Chapel Hill, ; Chapel Hill, NC USA

[61 ]GRID grid.240206.2, ISNI 0000 0000 8795 072X, McLean Imaging Center, , McLean Hospital, ; Belmont, MA USA

Author information

Katherine E. Finegold http://orcid.org/0000-0001-6298-2802

Lauren A. M. Lebois http://orcid.org/0000-0001-5816-9181

Sanne J. H. van Rooij http://orcid.org/0000-0002-0160-7248

Timothy D. Ely http://orcid.org/0000-0002-5690-5234

Tanja Jovanovic http://orcid.org/0000-0002-6456-0053

Steven E. Bruce http://orcid.org/0000-0002-5807-4382

Thomas C. Neylan http://orcid.org/0000-0002-1572-2626

Sarah D. Linnstaedt http://orcid.org/0000-0001-5295-7072

Laura T. Germine http://orcid.org/0000-0001-8690-8412

Sophia Sheikh http://orcid.org/0000-0003-1939-3126

Jose L. Pascual http://orcid.org/0000-0002-1613-7912

Anna M. Chang http://orcid.org/0000-0002-6494-9843

Leon D. Sanchez http://orcid.org/0000-0002-8807-0913

Mark W. Miller http://orcid.org/0000-0001-6393-8563

Deanna M. Barch http://orcid.org/0000-0003-1693-8506

Diego A. Pizzagalli http://orcid.org/0000-0002-7772-1143

Ronald C. Kessler http://orcid.org/0000-0003-4831-2305

Samuel A. McLean http://orcid.org/0000-0001-9482-3582

Kerry J. Ressler http://orcid.org/0000-0002-5158-1103

Jennifer S. Stevens http://orcid.org/0000-0003-4674-0314

Article

Publisher ID: 2085

DOI: 10.1038/s41398-022-02085-8

PMC ID: 9360028

PubMed ID: 35941117

SO-VID: d396f3a1-2a2f-4a9b-ac4a-337171fb110a

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.