Similar neural pathways link psychological stress and brain-age in health and multiple sclerosis

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Author(s): Marc-Andre Schulz ¹ ^, ² ^, ¹⁵ , Stefan Hetzer ² ^, ³ , Fabian Eitel ¹ ^, ² , Susanna Asseyer ⁴ ^, ⁵ ^, ⁶ ^, ⁷ , Lil Meyer-Arndt ⁷ ^, ⁸ ^, ⁹ , Tanja Schmitz-Hübsch ⁴ ^, ⁵ ^, ⁶ ^, ⁷ , Judith Bellmann-Strobl ⁴ ^, ⁶ ^, ⁷ , James H. Cole ¹⁰ ^, ¹¹ , Stefan M. Gold ¹² ^, ¹³ ^, ¹⁴ , Friedemann Paul ⁴ ^, ⁵ ^, ⁶ ^, ⁷ ^, ¹⁶ , Kerstin Ritter ¹ ^, ² ^, ¹⁶ , Martin Weygandt ⁴ ^, ⁵ ^, ⁶ ^, ⁷ ^, ¹⁶ ^, ¹⁷ ^, ^∗

Publication date (Electronic): 18 August 2023

Journal: iScience

Publisher: Elsevier

Keywords: Age, Neuroscience, Neural networks, Machine learning

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Summary

Clinical and neuroscientific studies suggest a link between psychological stress and reduced brain health in health and neurological disease but it is unclear whether mediating pathways are similar. Consequently, we applied an arterial-spin-labeling MRI stress task in 42 healthy persons and 56 with multiple sclerosis, and investigated regional neural stress responses, associations between functional connectivity of stress-responsive regions and the brain-age prediction error, a highly sensitive machine learning brain health biomarker, and regional brain-age constituents in both groups. Stress responsivity did not differ between groups. Although elevated brain-age prediction errors indicated worse brain health in patients, anterior insula–occipital cortex (healthy persons: occipital pole; patients: fusiform gyrus) functional connectivity correlated with brain-age prediction errors in both groups. Finally, also gray matter contributed similarly to regional brain-age across groups. These findings might suggest a common stress–brain health pathway whose impact is amplified in multiple sclerosis by disease-specific vulnerability factors.

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Highlights

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Stress can reduce brain health in health and neurological disease including MS
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It is unclear if mediating pathways are similar in healthy persons and MS patients
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Insular-occipital connectivity during stress correlated with brain-age in both
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This might suggest a common link between psychological stress and brain health

Abstract

Age; Neuroscience; Neural networks; Machine learning

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Most cited references 67

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Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain.

N. Tzourio-Mazoyer, B Landeau, D Papathanassiou … (2003)

An anatomical parcellation of the spatially normalized single-subject high-resolution T1 volume provided by the Montreal Neurological Institute (MNI) (D. L. Collins et al., 1998, Trans. Med. Imag. 17, 463-468) was performed. The MNI single-subject main sulci were first delineated and further used as landmarks for the 3D definition of 45 anatomical volumes of interest (AVOI) in each hemisphere. This procedure was performed using a dedicated software which allowed a 3D following of the sulci course on the edited brain. Regions of interest were then drawn manually with the same software every 2 mm on the axial slices of the high-resolution MNI single subject. The 90 AVOI were reconstructed and assigned a label. Using this parcellation method, three procedures to perform the automated anatomical labeling of functional studies are proposed: (1) labeling of an extremum defined by a set of coordinates, (2) percentage of voxels belonging to each of the AVOI intersected by a sphere centered by a set of coordinates, and (3) percentage of voxels belonging to each of the AVOI intersected by an activated cluster. An interface with the Statistical Parametric Mapping package (SPM, J. Ashburner and K. J. Friston, 1999, Hum. Brain Mapp. 7, 254-266) is provided as a freeware to researchers of the neuroimaging community. We believe that this tool is an improvement for the macroscopical labeling of activated area compared to labeling assessed using the Talairach atlas brain in which deformations are well known. However, this tool does not alleviate the need for more sophisticated labeling strategies based on anatomical or cytoarchitectonic probabilistic maps.

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Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS).

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One method of evaluating the degree of neurologic impairment in MS has been the combination of grades (0 = normal to 5 or 6 = maximal impairment) within 8 Functional Systems (FS) and an overall Disability Status Scale (DSS) that had steps from 0 (normal) to 10 (death due to MS). A new Expanded Disability Status Scale (EDSS) is presented, with each of the former steps (1,2,3 . . . 9) now divided into two (1.0, 1.5, 2.0 . . . 9.5). The lower portion is obligatorily defined by Functional System grades. The FS are Pyramidal, Cerebellar, Brain Stem, Sensory, Bowel & Bladder, Visual, Cerebral, and Other; the Sensory and Bowel & Bladder Systems have been revised. Patterns of FS and relations of FS by type and grade to the DSS are demonstrated.

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A Unified Approach to Interpreting Model Predictions

Scott R. Lundberg, Su-In Lee (2017)

Understanding why a model makes a certain prediction can be as crucial as the prediction's accuracy in many applications. However, the highest accuracy for large modern datasets is often achieved by complex models that even experts struggle to interpret, such as ensemble or deep learning models, creating a tension between accuracy and interpretability. In response, various methods have recently been proposed to help users interpret the predictions of complex models, but it is often unclear how these methods are related and when one method is preferable over another. To address this problem, we present a unified framework for interpreting predictions, SHAP (SHapley Additive exPlanations). SHAP assigns each feature an importance value for a particular prediction. Its novel components include: (1) the identification of a new class of additive feature importance measures, and (2) theoretical results showing there is a unique solution in this class with a set of desirable properties. The new class unifies six existing methods, notable because several recent methods in the class lack the proposed desirable properties. Based on insights from this unification, we present new methods that show improved computational performance and/or better consistency with human intuition than previous approaches. To appear in NIPS 2017

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Author and article information

Contributors

Martin Weygandt

Journal

Journal ID (nlm-ta): iScience

Journal ID (iso-abbrev): iScience

Title: iScience

Publisher: Elsevier

ISSN (Electronic): 2589-0042

Publication date PMC-release: 18 August 2023

Publication date Collection: 15 September 2023

Publication date (Electronic): 18 August 2023

Volume: 26

Issue: 9

Electronic Location Identifier: 107679

Affiliations

[1 ]Charité – Universitätsmedizin Berlin (corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health), Department of Psychiatry and Psychotherapy, Berlin, Germany

[2 ]Bernstein Center for Computational Neuroscience, Berlin, Germany

[3 ]Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin Center for Advanced Neuroimaging, Berlin, Germany

[4 ]Experimental and Clinical Research Center, A Cooperation Between the Max Delbrück Center for Molecular Medicine in the Helmholtz Association and Charité Universitätsmedizin Berlin, Berlin, Germany

[5 ]Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Experimental and Clinical Research Center, Berlin, Germany

[6 ]Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC), Berlin, Germany

[7 ]NeuroCure Clinical Research Center, Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin and Humboldt-Universität zu Berlin, Berlin, Germany

[8 ]Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Department of Neurology, Berlin, Germany

[9 ]Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Regenerative Immunology and Aging, BIH Center for Regenerative Therapies, Berlin, Germany

[10 ]Centre for Medical Image Computing, Department of Computer Science, University College London, London, UK

[11 ]Dementia Research Centre, Institute of Neurology, University College London, London, UK

[12 ]Institute of Neuroimmunology and Multiple Sclerosis (INIMS), Center for Molecular Neurobiology Hamburg, University Medical Center Hamburg-Eppendorf, Hamburg, Germany

[13 ]Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Department of Psychiatry and Psychotherapy, Campus Benjamin Franklin, Berlin, Germany

[14 ]Charité – Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Medical Department, Section Psychosomatic Medicine, Berlin, Germany

[15 ]Department of Psychiatry, Psychotherapy, and Psychosomatics, Rheinisch-Westfälische Technische Hochschule (RWTH), Aachen University, Aachen, Germany

Author notes

[∗ ]Corresponding author weygandtmartin@ 123456gmail.com

[16]

These authors contributed equally

[17]

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Article

Publisher Item ID: S2589-0042(23)01756-X Publisher ID: 107679

DOI: 10.1016/j.isci.2023.107679

PMC ID: 10480681

PubMed ID: 37680475

SO-VID: cfc8ea69-a481-4618-be4a-b93a74305b1e

License:

This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

History

Date received : 28 October 2022

Date revision received : 30 July 2023

Date accepted : 14 August 2023

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Similar neural pathways link psychological stress and brain-age in health and multiple sclerosis

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Most cited references 67

Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain.

Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS).

A Unified Approach to Interpreting Model Predictions

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