The normative modeling framework for computational psychiatry.


Journal

Nature protocols
ISSN: 1750-2799
Titre abrégé: Nat Protoc
Pays: England
ID NLM: 101284307

Informations de publication

Date de publication:
07 2022
Historique:
received: 16 08 2021
accepted: 17 03 2022
pubmed: 2 6 2022
medline: 12 7 2022
entrez: 1 6 2022
Statut: ppublish

Résumé

Normative modeling is an emerging and innovative framework for mapping individual differences at the level of a single subject or observation in relation to a reference model. It involves charting centiles of variation across a population in terms of mappings between biology and behavior, which can then be used to make statistical inferences at the level of the individual. The fields of computational psychiatry and clinical neuroscience have been slow to transition away from patient versus 'healthy' control analytic approaches, probably owing to a lack of tools designed to properly model biological heterogeneity of mental disorders. Normative modeling provides a solution to address this issue and moves analysis away from case-control comparisons that rely on potentially noisy clinical labels. Here we define a standardized protocol to guide users through, from start to finish, normative modeling analysis using the Predictive Clinical Neuroscience toolkit (PCNtoolkit). We describe the input data selection process, provide intuition behind the various modeling choices and conclude by demonstrating several examples of downstream analyses that the normative model may facilitate, such as stratification of high-risk individuals, subtyping and behavioral predictive modeling. The protocol takes ~1-3 h to complete.

Identifiants

pubmed: 35650452
doi: 10.1038/s41596-022-00696-5
pii: 10.1038/s41596-022-00696-5
pmc: PMC7613648
mid: EMS154602
doi:

Types de publication

Journal Article Review Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1711-1734

Subventions

Organisme : Wellcome Trust
ID : 098369/Z/12/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 215698/Z/19/Z
Pays : United Kingdom
Organisme : ZonMw
ID : ZONMW_91716415
Pays : Netherlands
Organisme : Wellcome Trust
ID : 215698
Pays : United Kingdom
Organisme : European Research Council
ID : 101001118
Pays : International

Informations de copyright

© 2022. Springer Nature Limited.

Références

Wang, D. et al. Parcellating cortical functional networks in individuals. Nat. Neurosci. 18, 1853–1860 (2015).
pubmed: 26551545 pmcid: 4661084 doi: 10.1038/nn.4164
Finn, E. S. & Constable, R. T. Individual variation in functional brain connectivity: implications for personalized approaches to psychiatric disease. Dialogues Clin. Neurosci. 18, 277–287 (2016).
pubmed: 27757062 pmcid: 5067145 doi: 10.31887/DCNS.2016.18.3/efinn
Braga, R. M. & Buckner, R. L. Parallel interdigitated distributed networks within the individual estimated by intrinsic functional connectivity. Neuron 95, 457–471 (2017).
pubmed: 28728026 pmcid: 5519493 doi: 10.1016/j.neuron.2017.06.038
Poldrack, R. A. Precision neuroscience: dense sampling of individual brains. Neuron 95, 727–729 (2017).
pubmed: 28817793 doi: 10.1016/j.neuron.2017.08.002
Vanderwal, T. et al. Individual differences in functional connectivity during naturalistic viewing conditions. Neuroimage 157, 521–530 (2017).
Braun, U. et al. From maps to multi-dimensional network mechanisms of mental disorders. Neuron 97, 14–31 (2018).
pubmed: 29301099 pmcid: 5757246 doi: 10.1016/j.neuron.2017.11.007
Gratton, C. et al. Defining individual-specific functional neuroanatomy for precision psychiatry. Biol. Psychiatry 88, 28–39 (2020).
pubmed: 31916942 doi: 10.1016/j.biopsych.2019.10.026
Hyman, S. E. Can neuroscience be integrated into the DSM-V? Nat. Rev. Neurosci. 8, 725–732 (2007).
pubmed: 17704814 doi: 10.1038/nrn2218
Insel, T. et al. Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. Am. J. Psychiatry 167, 748–751 (2010).
pubmed: 20595427 doi: 10.1176/appi.ajp.2010.09091379
Michelini, G., Palumbo, I. M., DeYoung, C. G., Latzman, R. D. & Kotov, R. Linking RDoC and HiTOP: a new interface for advancing psychiatric nosology and neuroscience. Clin. Psychol. Rev. 86, 102025 (2021).
pubmed: 33798996 pmcid: 8165014 doi: 10.1016/j.cpr.2021.102025
Narrow, W. E. & Kuhl, E. A. Dimensional approaches to psychiatric diagnosis in DSM-5. J. Ment. Health Policy Econ. 14, 197–200 (2011).
pubmed: 22345361
Cuthbert, B. N. & Insel, T. R. Toward the future of psychiatric diagnosis: the seven pillars of RDoC. BMC Med. 11, 126 (2013).
pubmed: 23672542 pmcid: 3653747 doi: 10.1186/1741-7015-11-126
Sanislow, C. A. RDoC at 10: changing the discourse for psychopathology. World Psychiatry 19, 311–312 (2020).
pubmed: 32931117 pmcid: 7491616 doi: 10.1002/wps.20800
Kotov, R. et al. The Hierarchical Taxonomy of Psychopathology (HiTOP): a dimensional alternative to traditional nosologies. J. Abnorm. Psychol. 126, 454–477 (2017).
pubmed: 28333488 doi: 10.1037/abn0000258
Kotov, R. et al. The Hierarchical Taxonomy of Psychopathology (HiTOP): a quantitative nosology based on consensus of evidence. Annu. Rev. Clin. Psychol. 17, 081219–093304 (2021).
Haro, J. M. et al. ROAMER: roadmap for mental health research in Europe. Int. J. Methods Psychiatr. Res. 23, 1–14 (2014).
pubmed: 24375532 doi: 10.1002/mpr.1406
Schumann, G. et al. Stratified medicine for mental disorders. Eur. Neuropsychopharmacol. 24, 5–50 (2014).
pubmed: 24176673 doi: 10.1016/j.euroneuro.2013.09.010
Feczko, E. et al. The heterogeneity problem: approaches to identify psychiatric subtypes. Trends Cogn. Sci. 23, 584–601 (2019).
pubmed: 31153774 pmcid: 6821457 doi: 10.1016/j.tics.2019.03.009
Shen, X. et al. Using connectome-based predictive modeling to predict individual behavior from brain connectivity. Nat. Protoc. 12, 506–518 (2017).
pubmed: 28182017 pmcid: 5526681 doi: 10.1038/nprot.2016.178
Sripada, C. et al. Basic units of inter-individual variation in resting state connectomes. Sci. Rep. 9, 1900 (2019).
pubmed: 30760808 pmcid: 6374507 doi: 10.1038/s41598-018-38406-5
Woo, C.-W., Chang, L. J., Lindquist, M. A. & Wager, T. D. Building better biomarkers: brain models in translational neuroimaging. Nat. Neurosci. 20, 365–377 (2017).
pubmed: 28230847 pmcid: 5988350 doi: 10.1038/nn.4478
Marquand, A. F. et al. Conceptualizing mental disorders as deviations from normative functioning. Mol. Psychiatry 24, 1415–1424 (2019).
pubmed: 31201374 pmcid: 6756106 doi: 10.1038/s41380-019-0441-1
Gau, R. et al. Brainhack: developing a culture of open, inclusive, community-driven neuroscience. Neuron 109, 1769–1775 (2021).
pubmed: 33932337 pmcid: 9153215 doi: 10.1016/j.neuron.2021.04.001
Olah, C. & Carter, S. Research debt. Distill 2, e5 (2017).
doi: 10.23915/distill.00005
Fraza, C. J., Dinga, R., Beckmann, C. F. & Marquand, A. F. Warped Bayesian linear regression for normative modelling of big data. Neuroimage 245, 118715 (2021).
pubmed: 34798518 doi: 10.1016/j.neuroimage.2021.118715
Dinga, R. et al. Normative modeling of neuroimaging data using generalized additive models of location scale and shape. Preprint at bioRxiv https://doi.org/10.1101/2021.06.14.448106 (2021).
Kia, S. M. et al. Hierarchical Bayesian regression for multi-site normative modeling of neuroimaging data. In Medical Image Computing and Computer Assisted Intervention – MICCAI 2020 (eds. Martel, A. L. et al.) 699–709 (Springer International, 2020); https://doi.org/10.1007/978-3-030-59728-3_68
Kia, S. M. et al. Federated multi-site normative modeling using hierarchical Bayesian regression. Preprint at bioRxiv https://doi.org/10.1101/2021.05.28.446120 (2021).
Floris, D. L. et al. Atypical brain asymmetry in autism—a candidate for clinically meaningful stratification. Biol. Psychiatry Cogn. Neurosci. Neuroimaging https://doi.org/10.1016/j.bpsc.2020.08.008 (2020).
Zabihi, M. et al. Dissecting the heterogeneous cortical anatomy of autism spectrum disorder using normative models. Biol. Psychiatry Cogn. Neurosci. Neuroimaging 4, 567–578 (2019).
pubmed: 30799285 pmcid: 6551348
Zabihi, M. et al. Fractionating autism based on neuroanatomical normative modeling. Transl. Psychiatry 10, 1–10 (2020).
doi: 10.1038/s41398-020-01057-0
Wolfers, T. et al. Individual differences v. the average patient: mapping the heterogeneity in ADHD using normative models. Psychol. Med. 50, 314–323 (2020).
pubmed: 30782224 doi: 10.1017/S0033291719000084
Wolfers, T. et al. Refinement by integration: aggregated effects of multimodal imaging markers on adult ADHD. J. Psychiatry Neurosci. 42, 386–394 (2017).
pubmed: 28832320 pmcid: 5662460 doi: 10.1503/jpn.160240
Verdi, S., Marquand, A. F., Schott, J. M. & Cole, J. H. Beyond the average patient: how neuroimaging models can address heterogeneity in dementia. Brain https://doi.org/10.1093/brain/awab165 (2021).
Wolfers, T. et al. Replicating extensive brain structural heterogeneity in individuals with schizophrenia and bipolar disorder. Human Brain Mapp. https://doi.org/10.1002/hbm.25386 (2020).
Wolfers, T. et al. Mapping the heterogeneous phenotype of schizophrenia and bipolar disorder using normative models. JAMA Psychiatry 75, 1146–1155 (2018).
pubmed: 30304337 pmcid: 6248110 doi: 10.1001/jamapsychiatry.2018.2467
Wolfers, T. et al. Replicating extensive brain structural heterogeneity in individuals with schizophrenia and bipolar disorder. Hum. Brain Mapp. 42, 2546–2555 (2021).
pubmed: 33638594 pmcid: 8090780 doi: 10.1002/hbm.25386
Sripada, C., Angstadt, M., Rutherford, S. & Taxali, A. Brain network mechanisms of general intelligence. Preprint at bioRxiv https://doi.org/10.1101/657205 (2019).
Sripada, C. et al. Brain Connectivity Patterns in Children Linked to Neurocognitive Abilities. Preprint at bioRxiv https://doi.org/10.1101/2020.09.10.291500 (2020).
Rosenberg, M. D. et al. A neuromarker of sustained attention from whole-brain functional connectivity. Nat. Neurosci. 19, 165–171 (2015).
pubmed: 26595653 pmcid: 4696892 doi: 10.1038/nn.4179
Rosenberg, M. D. et al. Functional connectivity predicts changes in attention observed across minutes, days, and months. Proc. Natl Acad. Sci. USA 117, 3797–3807 (2020).
pubmed: 32019892 pmcid: 7035597 doi: 10.1073/pnas.1912226117
Marquand, A. F., Haak, K. V. & Beckmann, C. F. Functional corticostriatal connection topographies predict goal directed behaviour in humans. Nat. Hum. Behav. 1, 0146 (2017).
Marquand, A. et al. Quantitative prediction of subjective pain intensity from whole-brain fMRI data using Gaussian processes. Neuroimage 49, 2178–2189 (2010).
Wager, T. D. et al. An fMRI-based neurologic signature of physical pain. N. Engl. J. Med. 368, 1388–1397 (2013).
pubmed: 23574118 pmcid: 3691100 doi: 10.1056/NEJMoa1204471
Sripada, C., Angstadt, M., Rutherford, S., Taxali, A. & Shedden, K. Toward a “treadmill test” for cognition: improved prediction of general cognitive ability from the task activated brain. Hum. Brain Mapp. 41, 3186–3197 (2020).
Taxali, A., Angstadt, M., Rutherford, S. & Sripada, C. Boost in test–retest reliability in resting state fMRI with predictive modeling. Cereb. Cortex 31, 2822–2833 (2021).
Finn, E. S. et al. Functional connectome fingerprinting: identifying individuals using patterns of brain connectivity. Nat. Neurosci. 18, 1664–1671 (2015).
pubmed: 26457551 pmcid: 5008686 doi: 10.1038/nn.4135
Wang, H.-T. et al. Finding the needle in a high-dimensional haystack: canonical correlation analysis for neuroscientists. Neuroimage 216, 116745 (2020).
Smith, S. M. et al. A positive-negative mode of population covariation links brain connectivity, demographics and behavior. Nat. Neurosci. 18, 1565–1567 (2015).
pubmed: 26414616 pmcid: 4625579 doi: 10.1038/nn.4125
Dadi, K. et al. Benchmarking functional connectome-based predictive models for resting-state fMRI. Neuroimage 192, 115–134 (2019).
Lake, E. M. R. et al. The functional brain organization of an individual allows prediction of measures of social abilities transdiagnostically in autism and attention-deficit/hyperactivity disorder. Biol. Psychiatry 86, 315–326 (2019).
pubmed: 31010580 pmcid: 7311928 doi: 10.1016/j.biopsych.2019.02.019
Cole, J. H. & Franke, K. Predicting age using neuroimaging: innovative brain ageing biomarkers. Trends Neurosci. 40, 681–690 (2017).
pubmed: 29074032 doi: 10.1016/j.tins.2017.10.001
Han, L. K. M. et al. Brain aging in major depressive disorder: results from the ENIGMA major depressive disorder working group. Mol. Psychiatry 26, 5124–5139 (2021).
pubmed: 32424236 doi: 10.1038/s41380-020-0754-0
Sturmfels, P. et al. A domain guided CNN architecture for predicting age from structural brain images. Preprint at arXiv https://doi.org/10.48550/arXiv.1808.04362 (2018).
Alfaro-Almagro, F. et al. Image processing and quality control for the first 10,000 brain imaging datasets from UK Biobank. Neuroimage 166, 400–424 (2018).
Donders, A. R. T., van der Heijden, G. J. M. G., Stijnen, T. & Moons, K. G. M. Review: a gentle introduction to imputation of missing values. J. Clin. Epidemiol. 59, 1087–1091 (2006).
Madley-Dowd, P., Hughes, R., Tilling, K. & Heron, J. The proportion of missing data should not be used to guide decisions on multiple imputation. J. Clin. Epidemiol. 110, 63–73 (2019).
pubmed: 30878639 pmcid: 6547017 doi: 10.1016/j.jclinepi.2019.02.016
Burt, J. B., Helmer, M., Shinn, M., Anticevic, A. & Murray, J. D. Generative modeling of brain maps with spatial autocorrelation. Neuroimage 220, 117038 (2020).
Shinn, M. et al. Spatial and temporal autocorrelation weave human brain networks. Preprint at bioRxiv https://doi.org/10.1101/2021.06.01.446561 (2021).
Smith, S. M. & Nichols, T. E. Threshold-free cluster enhancement: addressing problems of smoothing, threshold dependence and localisation in cluster inference. Neuroimage 44, 83–98 (2009).
Guo, C., Kang, J. & Johnson, T. D. A spatial Bayesian latent factor model for image-on-image regression. Biometrics https://doi.org/10.1111/biom.13420 (2020).
Woolrich, M. W., Behrens, T. E. J. & Smith, S. M. Constrained linear basis sets for HRF modelling using variational Bayes. Neuroimage 21, 1748–1761 (2004).
Liu, W., Zhu, P., Anderson, J. S., Yurgelun-Todd, D. & Fletcher, P. T. Spatial regularization of functional connectivity using high-dimensional Markov random fields. Med. Image Comput. Comput. Assist. Interv. 13, 363–370 (2010).
pubmed: 20879336 pmcid: 4214154
Song, H. F., Kennedy, H. & Wang, X.-J. Spatial embedding of structural similarity in the cerebral cortex. Proc. Natl Acad. Sci. USA 111, 16580–16585 (2014).
pubmed: 25368200 pmcid: 4246295 doi: 10.1073/pnas.1414153111
Roberts, J. A. et al. The contribution of geometry to the human connectome. Neuroimage 124, 379–393 (2016).
Bijsterbosch, J. et al. Challenges and future directions for representations of functional brain organization. Nat. Neurosci. 23, 1484–1495 (2020).
pubmed: 33106677 doi: 10.1038/s41593-020-00726-z
Huertas, I. et al. A Bayesian spatial model for neuroimaging data based on biologically informed basis functions. Neuroimage 161, 134–148 (2017).
Kia, S. M. & Marquand, A. Normative modeling of neuroimaging data using scalable multi-task Gaussian processes. Preprint at arXiv https://doi.org/10.48550/arXiv.1806.01047 (2018).
Kia, S. M., Beckmann, C. F. & Marquand, A. F. Scalable multi-task Gaussian process tensor regression for normative modeling of structured variation in neuroimaging data. Preprint at arXiv https://doi.org/10.48550/arXiv.1808.00036 (2018).
Jahn, A. et al. Andy’s Brain Book https://andysbrainbook.readthedocs.io/en/latest (2020).
Casey, B. J. et al. The Adolescent Brain Cognitive Development (ABCD) study: imaging acquisition across 21 sites. Dev. Cogn. Neurosci. 32, 43–54 (2018).
pubmed: 29567376 pmcid: 5999559 doi: 10.1016/j.dcn.2018.03.001
Thompson, P. M. et al. ENIGMA and global neuroscience: a decade of large-scale studies of the brain in health and disease across more than 40 countries. Transl. Psychiatry 10, 100 (2020).
pubmed: 32198361 pmcid: 7083923 doi: 10.1038/s41398-020-0705-1
Beer, J. C. et al. Longitudinal ComBat: a method for harmonizing longitudinal multi-scanner imaging data. Neuroimage 220, 117129 (2020).
Fortin, J.-P. et al. Harmonization of multi-site diffusion tensor imaging data. Neuroimage 161, 149–170 (2017).
Fortin, J.-P. et al. Harmonization of cortical thickness measurements across scanners and sites. Neuroimage 167, 104–120 (2018).
Johnson, W. E., Li, C. & Rabinovic, A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics 8, 118–127 (2007).
pubmed: 16632515 doi: 10.1093/biostatistics/kxj037
Nygaard, V., Rødland, E. A. & Hovig, E. Methods that remove batch effects while retaining group differences may lead to exaggerated confidence in downstream analyses. Biostatistics 17, 29–39 (2016).
pubmed: 26272994 doi: 10.1093/biostatistics/kxv027
Noirhomme, Q. et al. Biased binomial assessment of cross-validated estimation of classification accuracies illustrated in diagnosis predictions. Neuroimage Clin. 4, 687–694 (2014).
Marquand, A. F., Wolfers, T., Mennes, M., Buitelaar, J. & Beckmann, C. F. Beyond lumping and splitting: a review of computational approaches for stratifying psychiatric disorders. Biol. Psychiatry Cogn. Neurosci. Neuroimaging 1, 433–447 (2016).
pubmed: 27642641 pmcid: 5013873
Rahimi, A. & Recht, B. Random features for large-scale kernel machines. In NIPS'07: Proceedings of the 20th International Conference on Neural Information Processing Systems 1177–1184 (2007).
Lv, J. et al. Individual deviations from normative models of brain structure in a large cross-sectional schizophrenia cohort. Mol. Psychiatry 26, 3512–3523 (2021).
Snelson, E., Ghahramani, Z. & Rasmussen, C. Warped Gaussian processes. in Advances in Neural Information Processing Systems vol. 16 (MIT Press, 2004).
Hensman, J., Fusi, N. & Lawrence, N. D. Gaussian processes for big data. Preprint at arXiv https://doi.org/10.48550/arXiv.1309.6835 (2013).
Bethlehem, R. et al. Brain charts for the human lifespan. Nature https://doi.org/10.1038/s41586-022-04554-y (2022).
Rutherford, S. et al. Charting brain growth and aging at high spatial precision. eLife 11, e72904 (2022).
Rutherford, S. et al. The Normative Modeling Framework for Computational Psychiatry (Zenodo, 2021); https://doi.org/10.5281/zenodo.5592153

Auteurs

Saige Rutherford (S)

Donders Institute for Brain, Cognition, and Behavior, Radboud University, Nijmegen, the Netherlands. saige.rutherford@donders.ru.nl.
Department of Cognitive Neuroscience, Radboud University Medical Center, Nijmegen, the Netherlands. saige.rutherford@donders.ru.nl.
Department of Psychiatry, University of Michigan, Ann Arbor, MI, USA. saige.rutherford@donders.ru.nl.

Seyed Mostafa Kia (SM)

Donders Institute for Brain, Cognition, and Behavior, Radboud University, Nijmegen, the Netherlands.
Department of Cognitive Neuroscience, Radboud University Medical Center, Nijmegen, the Netherlands.
Department of Psychiatry, Utrecht University Medical Center, Utrecht, the Netherlands.

Thomas Wolfers (T)

Department of Psychology, University of Oslo, Oslo, Norway.
Norwegian Center for Mental Disorders Research, University of Oslo, Oslo, Norway.

Charlotte Fraza (C)

Donders Institute for Brain, Cognition, and Behavior, Radboud University, Nijmegen, the Netherlands.
Department of Cognitive Neuroscience, Radboud University Medical Center, Nijmegen, the Netherlands.

Mariam Zabihi (M)

Donders Institute for Brain, Cognition, and Behavior, Radboud University, Nijmegen, the Netherlands.
Department of Cognitive Neuroscience, Radboud University Medical Center, Nijmegen, the Netherlands.

Richard Dinga (R)

Donders Institute for Brain, Cognition, and Behavior, Radboud University, Nijmegen, the Netherlands.
Department of Cognitive Neuroscience, Radboud University Medical Center, Nijmegen, the Netherlands.

Pierre Berthet (P)

Department of Psychology, University of Oslo, Oslo, Norway.
Norwegian Center for Mental Disorders Research, University of Oslo, Oslo, Norway.

Amanda Worker (A)

Department of Psychological Medicine, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.

Serena Verdi (S)

Centre for Medical Image Computing, Medical Physics and Biomedical Engineering, University College London, London, UK.
Dementia Research Centre, UCL Queen Square Institute of Neurology, London, UK.

Henricus G Ruhe (HG)

Donders Institute for Brain, Cognition, and Behavior, Radboud University, Nijmegen, the Netherlands.
Department of Psychiatry, Radboud University Medical Center, Nijmegen, the Netherlands.

Christian F Beckmann (CF)

Donders Institute for Brain, Cognition, and Behavior, Radboud University, Nijmegen, the Netherlands.
Department of Cognitive Neuroscience, Radboud University Medical Center, Nijmegen, the Netherlands.
Centre for Functional MRI of the Brain, University of Oxford, Oxford, UK.

Andre F Marquand (AF)

Donders Institute for Brain, Cognition, and Behavior, Radboud University, Nijmegen, the Netherlands.
Department of Cognitive Neuroscience, Radboud University Medical Center, Nijmegen, the Netherlands.
Department of Psychological Medicine, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH