A checklist for assessing the methodological quality of concurrent tES-fMRI studies (ContES checklist): a consensus study and statement

doi:10.1038/s41596-021-00664-5

Review

. 2022 Mar;17(3):596-617.

doi: 10.1038/s41596-021-00664-5. Epub 2022 Feb 4.

A checklist for assessing the methodological quality of concurrent tES-fMRI studies (ContES checklist): a consensus study and statement

Hamed Ekhtiari¹, Peyman Ghobadi-Azbari^{2

3}, Axel Thielscher^{4

5}, Andrea Antal⁶, Lucia M Li^{7

8}, A Duke Shereen⁹, Yuranny Cabral-Calderin¹⁰, Daniel Keeser^{11

12

13}, Til Ole Bergmann^{14

15

16}, Asif Jamil¹⁷, Ines R Violante¹⁸, Jorge Almeida^{19

20}, Marcus Meinzer^{21

22}, Hartwig R Siebner^{4

23

24}, Adam J Woods²⁵, Charlotte J Stagg^{26

27}, Rany Abend²⁸, Daria Antonenko²², Tibor Auer¹⁸, Marc Bächinger^{29

30}, Chris Baeken^{31

32

33}, Helen C Barron^{26

27}, Henry W Chase³⁴, Jenny Crinion³⁵, Abhishek Datta^{36

37}, Matthew H Davis³⁸, Mohsen Ebrahimi³, Zeinab Esmaeilpour³⁹, Brian Falcone⁴⁰, Valentina Fiori⁴¹, Iman Ghodratitoostani⁴², Gadi Gilam^{43

44}, Roland H Grabner⁴⁵, Joel D Greenspan⁴⁶, Georg Groen⁴⁷, Gesa Hartwigsen⁴⁸, Tobias U Hauser^{49

50}, Christoph S Herrmann^{51

52

53}, Chi-Hung Juan^{54

55}, Bart Krekelberg⁵⁶, Stephanie Lefebvre⁵⁷, Sook-Lei Liew^{58

59

60

61}, Kristoffer H Madsen^{4

62}, Rasoul Mahdavifar-Khayati², Nastaran Malmir³, Paola Marangolo^{63

64}, Andrew K Martin^{21

65}, Timothy J Meeker⁶⁶, Hossein Mohaddes Ardabili^{67

68}, Marius Moisa⁶⁹, Davide Momi⁷⁰, Beni Mulyana⁷¹, Alexander Opitz⁷², Natasza Orlov^{73

74

75

76}, Patrick Ragert^{77

78}, Christian C Ruff⁶⁹, Giulio Ruffini^{79

80}, Michaela Ruttorf⁸¹, Arshiya Sangchooli³, Klaus Schellhorn⁸², Gottfried Schlaug⁸³, Bernhard Sehm^{78

84}, Ghazaleh Soleimani⁸⁵, Hosna Tavakoli^{3

86}, Benjamin Thompson^{87

88

89}, Dagmar Timmann⁹⁰, Aki Tsuchiyagaito⁷¹, Martin Ulrich⁴⁷, Johannes Vosskuhl⁵¹, Christiane A Weinrich^{6

91}, Mehran Zare-Bidoky^{3

92}, Xiaochu Zhang⁹³, Benedikt Zoefel^{38

94

95}, Michael A Nitsche^{17

96}, Marom Bikson³⁹

Affiliations

¹ Laureate Institute for Brain Research, Tulsa, OK, USA. hekhtiari@laureateinstitute.org.
² Department of Biomedical Engineering, Shahed University, Tehran, Iran.
³ Iranian National Center for Addiction Studies (INCAS), Tehran University of Medical Sciences, Tehran, Iran.
⁴ Danish Research Centre for Magnetic Resonance, Centre for Functional and Diagnostic Imaging and Research, Copenhagen University Hospital Amager and Hvidovre, Hvidovre, Denmark.
⁵ Department of Health Technology, Technical University of Denmark, Kongens Lyngby, Denmark.
⁶ Department of Neurology, University Medical Center Goettingen, Goettingen, Germany.
⁷ Computational, Cognitive and Clinical Imaging Lab, Division of Brain Sciences, Department of Medicine, Imperial College London, London, UK.
⁸ UK DRI Centre for Care Research and Technology, Imperial College London, London, UK.
⁹ Advanced Science Research Center, The Graduate Center, City University of New York, New York, NY, USA.
¹⁰ Research Group Neural and Environmental Rhythms, Max Planck Institute for Empirical Aesthetics, Frankfurt, Germany.
¹¹ Department of Psychiatry and Psychotherapy, University Hospital LMU Munich, Munich, Germany.
¹² Department of Radiology, University Hospital LMU Munich, Munich, Germany.
¹³ NeuroImaging Core Unit Munich (NICUM), University Hospital LMU Munich, Munich, Germany.
¹⁴ Neuroimaging Center (NIC), Focus Program Translational Neuroscience (FTN), Johannes Gutenberg University Medical Center, Mainz, Germany.
¹⁵ Leibniz Institute for Resilience Research, Mainz, Germany.
¹⁶ Department of Neurology and Stroke and Hertie Institute for Clinical Brain Research, Eberhard Karls University of Tübingen, Tübingen, Germany.
¹⁷ Department of Psychology and Neurosciences, Leibniz Research Centre for Working Environment and Human Factors, Dortmund, Germany.
¹⁸ School of Psychology, Faculty of Health and Medical Sciences, University of Surrey, Guildford, UK.
¹⁹ Proaction Lab, Faculty of Psychology and Educational Sciences, University of Coimbra, Coimbra, Portugal.
²⁰ CINEICC, Faculty of Psychology and Educational Sciences, University of Coimbra, Coimbra, Portugal.
²¹ Centre for Clinical Research (UQCCR), The University of Queensland, Brisbane, Queensland, Australia.
²² Department of Neurology, University Medicine Greifswald, Greifswald, Germany.
²³ Department of Neurology, Copenhagen University Hospital Bispebjerg and Frederiksberg, Copenhagen, Denmark.
²⁴ Institute of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark.
²⁵ Center for Cognitive Aging and Memory, McKnight Brain Institute, Department of Clinical and Health Psychology, University of Florida, Gainesville, FL, USA.
²⁶ Wellcome Centre for Integrative Neuroimaging, University of Oxford, FMRIB, John Radcliffe Hospital, Oxford, UK.
²⁷ Medical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK.
²⁸ Section on Development and Affective Neuroscience, National Institute of Mental Health, Bethesda, MD, USA.
²⁹ Neural Control of Movement Lab, Department of Health Sciences and Technology, Zurich, Switzerland.
³⁰ Neuroscience Center Zurich, University of Zurich, Swiss Federal Institute of Technology Zurich, Zurich, Switzerland.
³¹ Department of Psychiatry and Medical Psychology, University Hospital Ghent, Ghent, Belgium.
³² Department of Psychiatry, Vrije Universiteit Brussel, University Hospital Brussels, Brussels, Belgium.
³³ Department of Electrical Engineering, Eindhoven University of Technology, Eindhoven, the Netherlands.
³⁴ Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.
³⁵ Institute of Cognitive Neuroscience, University College London, London, UK.
³⁶ Research and Development, Soterix Medical, New York, USA.
³⁷ The City College of the City University of New York, New York, USA.
³⁸ MRC Cognition and Brain Sciences Unit, University of Cambridge, Cambridge, UK.
³⁹ Department of Biomedical Engineering, The City College of New York of CUNY, New York, NY, USA.
⁴⁰ Northrop Grumman Company, Mission Systems, Falls Church, VA, USA.
⁴¹ Department of Clinical and Behavioral Neurology, IRCCS Santa Lucia Foundation, Rome, Italy.
⁴² Neurocognitive Engineering Laboratory (NEL), Center for Engineering Applied to Health, Institute of Mathematics and Computer Science (ICMC), University of Sao Paulo, Sao Paulo, Brazil.
⁴³ Systems Neuroscience and Pain Laboratory, Division of Pain Medicine, Department of Anesthesiology, Perioperative, and Pain Medicine, School of Medicine, Stanford University, Palo Alto, CA, USA.
⁴⁴ The Institute of Biomedical and Oral Research, Faculty of Dental Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.
⁴⁵ Educational Neuroscience, Institute of Psychology, University of Graz, Graz, Austria.
⁴⁶ Department of Neural and Pain Sciences, University of Maryland School of Dentistry, Baltimore, MD, USA.
⁴⁷ Department of Psychiatry, University of Ulm, Ulm, Germany.
⁴⁸ Lise Meitner Research Group Cognition and Plasticity, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany.
⁴⁹ Max Planck University College London Centre for Computational Psychiatry and Ageing Research, University College London, London, UK.
⁵⁰ Wellcome Centre for Human Neuroimaging, University College London, London, UK.
⁵¹ Experimental Psychology Lab, Cluster of Excellence "Hearing4all", European Medical School, University of Oldenburg, Oldenburg, Germany.
⁵² Neuroimaging Unit, European Medical School, University of Oldenburg, Oldenburg, Germany.
⁵³ Research Centre Neurosensory Science, University of Oldenburg, Oldenburg, Germany.
⁵⁴ Institute of Cognitive Neuroscience, National Central University, Taoyuan, Taiwan.
⁵⁵ Cognitive Intelligence and Precision Healthcare Research Center, National Central University, Taoyuan, Taiwan.
⁵⁶ Center for Molecular and Behavioral Neuroscience, Rutgers University-Newark, Newark, NJ, USA.
⁵⁷ Translational Research Centre, University Hospital of Psychiatry, University of Bern, Bern, Switzerland.
⁵⁸ Chan Division of Occupational Science and Occupational Therapy, University of Southern California, Los Angeles, CA, USA.
⁵⁹ USC Stevens Neuroimaging and Informatics Institute, Department of Neurology, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
⁶⁰ Department of Biomedical Engineering, University of Southern California, Los Angeles, CA, USA.
⁶¹ Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, CA, USA.
⁶² Department of Applied Mathematics and Computer Science, Technical University of Denmark, K, Lyngby, Denmark.
⁶³ Department of Humanities Studies, University Federico II, Naples, Italy.
⁶⁴ Aphasia Research Lab, IRCCS Santa Lucia Foundation, Rome, Italy.
⁶⁵ Department of Psychology, University of Kent, Canterbury, UK.
⁶⁶ Department of Neurosurgery, Johns Hopkins University, Baltimore, MD, USA.
⁶⁷ Psychiatry and Behavioral Sciences Research Center, Ibn-e-Sina Hospital, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.
⁶⁸ Student Research Committee, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.
⁶⁹ Zurich Center for Neuroeconomics, Department of Economics, University of Zurich, Zurich, Switzerland.
⁷⁰ Krembil Centre for Neuroinformatics, Centre for Addiction and Mental Health (CAMH), Toronto, Ontario, Canada.
⁷¹ Laureate Institute for Brain Research, Tulsa, OK, USA.
⁷² Department of Biomedical Engineering, University of Minnesota, Minneapolis, MN, USA.
⁷³ Department of Psychosis Studies, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
⁷⁴ Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Boston, MA, USA.
⁷⁵ Department of Radiology, Xuanwu Hospital, Capital Medical University, Beijing, China.
⁷⁶ Department of Psychology, Jagiellonian University, Cracow, Poland.
⁷⁷ Institute for General Kinesiology and Exercise Science, University of Leipzig, Leipzig, Germany.
⁷⁸ Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany.
⁷⁹ Neuroelectrics Corporation, Cambridge, Cambridge, MA, USA.
⁸⁰ Neuroelectrics Corporation, Barcelona, Barcelona, Spain.
⁸¹ Computer Assisted Clinical Medicine, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
⁸² neuroConn GmbH, Ilmenau, Germany.
⁸³ Neuroimaging-Neuromodulation and Stroke Recovery Laboratories, Department of Neurology, Baystate-University of Massachusetts Medical School, and Department of Biomedical Engineering, Institute of Applied Life Sciences, University of Massachusetts, Amherst, MA, USA.
⁸⁴ Department of Neurology, Martin-Luther-University Halle-Wittenberg, Halle (Saale), Germany.
⁸⁵ Department of Biomedical Engineering, Amirkabir University of Technology, Tehran, Iran.
⁸⁶ Department of Cognitive Neuroscience, Institute for Cognitive Sciences Studies, Tehran, Iran.
⁸⁷ School of Optometry and Vision Science, University of Auckland, Auckland, New Zealand.
⁸⁸ School of Optometry and Vision Science, University of Waterloo, Waterloo, Ontario, Canada.
⁸⁹ Centre for Eye and Vision Research, Hong Kong, Hong Kong.
⁹⁰ Department of Neurology and Center for Translational Neuro- and Behavioral Sciences (C-TNBS), Essen University Hospital, University of Duisburg-Essen, Essen, Germany.
⁹¹ Department of Cognitive Neurology, University Medical Center Goettingen, Goettingen, Germany.
⁹² Shahid-Sadoughi University of Medical Sciences, Yazd, Iran.
⁹³ Department of Psychology, School of Humanities & Social Science, University of Science & Technology of China, Hefei, China.
⁹⁴ Centre de Recherche Cerveau et Cognition (CerCo), CNRS, Toulouse, France.
⁹⁵ Université Toulouse III Paul Sabatier, Toulouse, France.
⁹⁶ Department of Neurology, University Medical Hospital Bergmannsheil, Bochum, Germany.

PMID: 35121855
PMCID: PMC7612687
DOI: 10.1038/s41596-021-00664-5

Review

A checklist for assessing the methodological quality of concurrent tES-fMRI studies (ContES checklist): a consensus study and statement

Hamed Ekhtiari et al. Nat Protoc. 2022 Mar.

. 2022 Mar;17(3):596-617.

doi: 10.1038/s41596-021-00664-5. Epub 2022 Feb 4.

Authors

Affiliations

¹ Laureate Institute for Brain Research, Tulsa, OK, USA. hekhtiari@laureateinstitute.org.
² Department of Biomedical Engineering, Shahed University, Tehran, Iran.
³ Iranian National Center for Addiction Studies (INCAS), Tehran University of Medical Sciences, Tehran, Iran.
⁴ Danish Research Centre for Magnetic Resonance, Centre for Functional and Diagnostic Imaging and Research, Copenhagen University Hospital Amager and Hvidovre, Hvidovre, Denmark.
⁵ Department of Health Technology, Technical University of Denmark, Kongens Lyngby, Denmark.
⁶ Department of Neurology, University Medical Center Goettingen, Goettingen, Germany.
⁷ Computational, Cognitive and Clinical Imaging Lab, Division of Brain Sciences, Department of Medicine, Imperial College London, London, UK.
⁸ UK DRI Centre for Care Research and Technology, Imperial College London, London, UK.
⁹ Advanced Science Research Center, The Graduate Center, City University of New York, New York, NY, USA.
¹⁰ Research Group Neural and Environmental Rhythms, Max Planck Institute for Empirical Aesthetics, Frankfurt, Germany.
¹¹ Department of Psychiatry and Psychotherapy, University Hospital LMU Munich, Munich, Germany.
¹² Department of Radiology, University Hospital LMU Munich, Munich, Germany.
¹³ NeuroImaging Core Unit Munich (NICUM), University Hospital LMU Munich, Munich, Germany.
¹⁴ Neuroimaging Center (NIC), Focus Program Translational Neuroscience (FTN), Johannes Gutenberg University Medical Center, Mainz, Germany.
¹⁵ Leibniz Institute for Resilience Research, Mainz, Germany.
¹⁶ Department of Neurology and Stroke and Hertie Institute for Clinical Brain Research, Eberhard Karls University of Tübingen, Tübingen, Germany.
¹⁷ Department of Psychology and Neurosciences, Leibniz Research Centre for Working Environment and Human Factors, Dortmund, Germany.
¹⁸ School of Psychology, Faculty of Health and Medical Sciences, University of Surrey, Guildford, UK.
¹⁹ Proaction Lab, Faculty of Psychology and Educational Sciences, University of Coimbra, Coimbra, Portugal.
²⁰ CINEICC, Faculty of Psychology and Educational Sciences, University of Coimbra, Coimbra, Portugal.
²¹ Centre for Clinical Research (UQCCR), The University of Queensland, Brisbane, Queensland, Australia.
²² Department of Neurology, University Medicine Greifswald, Greifswald, Germany.
²³ Department of Neurology, Copenhagen University Hospital Bispebjerg and Frederiksberg, Copenhagen, Denmark.
²⁴ Institute of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark.
²⁵ Center for Cognitive Aging and Memory, McKnight Brain Institute, Department of Clinical and Health Psychology, University of Florida, Gainesville, FL, USA.
²⁶ Wellcome Centre for Integrative Neuroimaging, University of Oxford, FMRIB, John Radcliffe Hospital, Oxford, UK.
²⁷ Medical Research Council Brain Network Dynamics Unit, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK.
²⁸ Section on Development and Affective Neuroscience, National Institute of Mental Health, Bethesda, MD, USA.
²⁹ Neural Control of Movement Lab, Department of Health Sciences and Technology, Zurich, Switzerland.
³⁰ Neuroscience Center Zurich, University of Zurich, Swiss Federal Institute of Technology Zurich, Zurich, Switzerland.
³¹ Department of Psychiatry and Medical Psychology, University Hospital Ghent, Ghent, Belgium.
³² Department of Psychiatry, Vrije Universiteit Brussel, University Hospital Brussels, Brussels, Belgium.
³³ Department of Electrical Engineering, Eindhoven University of Technology, Eindhoven, the Netherlands.
³⁴ Department of Psychiatry, University of Pittsburgh School of Medicine, Pittsburgh, PA, USA.
³⁵ Institute of Cognitive Neuroscience, University College London, London, UK.
³⁶ Research and Development, Soterix Medical, New York, USA.
³⁷ The City College of the City University of New York, New York, USA.
³⁸ MRC Cognition and Brain Sciences Unit, University of Cambridge, Cambridge, UK.
³⁹ Department of Biomedical Engineering, The City College of New York of CUNY, New York, NY, USA.
⁴⁰ Northrop Grumman Company, Mission Systems, Falls Church, VA, USA.
⁴¹ Department of Clinical and Behavioral Neurology, IRCCS Santa Lucia Foundation, Rome, Italy.
⁴² Neurocognitive Engineering Laboratory (NEL), Center for Engineering Applied to Health, Institute of Mathematics and Computer Science (ICMC), University of Sao Paulo, Sao Paulo, Brazil.
⁴³ Systems Neuroscience and Pain Laboratory, Division of Pain Medicine, Department of Anesthesiology, Perioperative, and Pain Medicine, School of Medicine, Stanford University, Palo Alto, CA, USA.
⁴⁴ The Institute of Biomedical and Oral Research, Faculty of Dental Medicine, Hebrew University of Jerusalem, Jerusalem, Israel.
⁴⁵ Educational Neuroscience, Institute of Psychology, University of Graz, Graz, Austria.
⁴⁶ Department of Neural and Pain Sciences, University of Maryland School of Dentistry, Baltimore, MD, USA.
⁴⁷ Department of Psychiatry, University of Ulm, Ulm, Germany.
⁴⁸ Lise Meitner Research Group Cognition and Plasticity, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany.
⁴⁹ Max Planck University College London Centre for Computational Psychiatry and Ageing Research, University College London, London, UK.
⁵⁰ Wellcome Centre for Human Neuroimaging, University College London, London, UK.
⁵¹ Experimental Psychology Lab, Cluster of Excellence "Hearing4all", European Medical School, University of Oldenburg, Oldenburg, Germany.
⁵² Neuroimaging Unit, European Medical School, University of Oldenburg, Oldenburg, Germany.
⁵³ Research Centre Neurosensory Science, University of Oldenburg, Oldenburg, Germany.
⁵⁴ Institute of Cognitive Neuroscience, National Central University, Taoyuan, Taiwan.
⁵⁵ Cognitive Intelligence and Precision Healthcare Research Center, National Central University, Taoyuan, Taiwan.
⁵⁶ Center for Molecular and Behavioral Neuroscience, Rutgers University-Newark, Newark, NJ, USA.
⁵⁷ Translational Research Centre, University Hospital of Psychiatry, University of Bern, Bern, Switzerland.
⁵⁸ Chan Division of Occupational Science and Occupational Therapy, University of Southern California, Los Angeles, CA, USA.
⁵⁹ USC Stevens Neuroimaging and Informatics Institute, Department of Neurology, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
⁶⁰ Department of Biomedical Engineering, University of Southern California, Los Angeles, CA, USA.
⁶¹ Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, CA, USA.
⁶² Department of Applied Mathematics and Computer Science, Technical University of Denmark, K, Lyngby, Denmark.
⁶³ Department of Humanities Studies, University Federico II, Naples, Italy.
⁶⁴ Aphasia Research Lab, IRCCS Santa Lucia Foundation, Rome, Italy.
⁶⁵ Department of Psychology, University of Kent, Canterbury, UK.
⁶⁶ Department of Neurosurgery, Johns Hopkins University, Baltimore, MD, USA.
⁶⁷ Psychiatry and Behavioral Sciences Research Center, Ibn-e-Sina Hospital, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.
⁶⁸ Student Research Committee, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.
⁶⁹ Zurich Center for Neuroeconomics, Department of Economics, University of Zurich, Zurich, Switzerland.
⁷⁰ Krembil Centre for Neuroinformatics, Centre for Addiction and Mental Health (CAMH), Toronto, Ontario, Canada.
⁷¹ Laureate Institute for Brain Research, Tulsa, OK, USA.
⁷² Department of Biomedical Engineering, University of Minnesota, Minneapolis, MN, USA.
⁷³ Department of Psychosis Studies, Institute of Psychiatry, Psychology and Neuroscience, King's College London, London, UK.
⁷⁴ Athinoula A. Martinos Center for Biomedical Imaging, Massachusetts General Hospital, Boston, MA, USA.
⁷⁵ Department of Radiology, Xuanwu Hospital, Capital Medical University, Beijing, China.
⁷⁶ Department of Psychology, Jagiellonian University, Cracow, Poland.
⁷⁷ Institute for General Kinesiology and Exercise Science, University of Leipzig, Leipzig, Germany.
⁷⁸ Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany.
⁷⁹ Neuroelectrics Corporation, Cambridge, Cambridge, MA, USA.
⁸⁰ Neuroelectrics Corporation, Barcelona, Barcelona, Spain.
⁸¹ Computer Assisted Clinical Medicine, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
⁸² neuroConn GmbH, Ilmenau, Germany.
⁸³ Neuroimaging-Neuromodulation and Stroke Recovery Laboratories, Department of Neurology, Baystate-University of Massachusetts Medical School, and Department of Biomedical Engineering, Institute of Applied Life Sciences, University of Massachusetts, Amherst, MA, USA.
⁸⁴ Department of Neurology, Martin-Luther-University Halle-Wittenberg, Halle (Saale), Germany.
⁸⁵ Department of Biomedical Engineering, Amirkabir University of Technology, Tehran, Iran.
⁸⁶ Department of Cognitive Neuroscience, Institute for Cognitive Sciences Studies, Tehran, Iran.
⁸⁷ School of Optometry and Vision Science, University of Auckland, Auckland, New Zealand.
⁸⁸ School of Optometry and Vision Science, University of Waterloo, Waterloo, Ontario, Canada.
⁸⁹ Centre for Eye and Vision Research, Hong Kong, Hong Kong.
⁹⁰ Department of Neurology and Center for Translational Neuro- and Behavioral Sciences (C-TNBS), Essen University Hospital, University of Duisburg-Essen, Essen, Germany.
⁹¹ Department of Cognitive Neurology, University Medical Center Goettingen, Goettingen, Germany.
⁹² Shahid-Sadoughi University of Medical Sciences, Yazd, Iran.
⁹³ Department of Psychology, School of Humanities & Social Science, University of Science & Technology of China, Hefei, China.
⁹⁴ Centre de Recherche Cerveau et Cognition (CerCo), CNRS, Toulouse, France.
⁹⁵ Université Toulouse III Paul Sabatier, Toulouse, France.
⁹⁶ Department of Neurology, University Medical Hospital Bergmannsheil, Bochum, Germany.

PMID: 35121855
PMCID: PMC7612687
DOI: 10.1038/s41596-021-00664-5

Abstract

Low-intensity transcranial electrical stimulation (tES), including alternating or direct current stimulation, applies weak electrical stimulation to modulate the activity of brain circuits. Integration of tES with concurrent functional MRI (fMRI) allows for the mapping of neural activity during neuromodulation, supporting causal studies of both brain function and tES effects. Methodological aspects of tES-fMRI studies underpin the results, and reporting them in appropriate detail is required for reproducibility and interpretability. Despite the growing number of published reports, there are no consensus-based checklists for disclosing methodological details of concurrent tES-fMRI studies. The objective of this work was to develop a consensus-based checklist of reporting standards for concurrent tES-fMRI studies to support methodological rigor, transparency and reproducibility (ContES checklist). A two-phase Delphi consensus process was conducted by a steering committee (SC) of 13 members and 49 expert panelists through the International Network of the tES-fMRI Consortium. The process began with a circulation of a preliminary checklist of essential items and additional recommendations, developed by the SC on the basis of a systematic review of 57 concurrent tES-fMRI studies. Contributors were then invited to suggest revisions or additions to the initial checklist. After the revision phase, contributors rated the importance of the 17 essential items and 42 additional recommendations in the final checklist. The state of methodological transparency within the 57 reviewed concurrent tES-fMRI studies was then assessed by using the checklist. Experts refined the checklist through the revision and rating phases, leading to a checklist with three categories of essential items and additional recommendations: (i) technological factors, (ii) safety and noise tests and (iii) methodological factors. The level of reporting of checklist items varied among the 57 concurrent tES-fMRI papers, ranging from 24% to 76%. On average, 53% of checklist items were reported in a given article. In conclusion, use of the ContES checklist is expected to enhance the methodological reporting quality of future concurrent tES-fMRI studies and increase methodological transparency and reproducibility.

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Conflict of interest statement

Declaration of competing interest

The City University of New York holds patents on brain stimulation with Marom Bikson as inventor. Marom Bikson has equity in Soterix Medical Inc. Marom Bikson consults, received grants, assigned inventions, and/or serves on the SAB of Boston Scientific, GlaxoSmithKline, Mecta, Halo Neuroscience, X. Christoph S. Herrmann holds a patent for transcranial electric stimulation. Michael A. Nitsche is on the Scientific Advisory Boards of Neuroelectrics, and Neurodevice. Giulio Ruffini is a co-founder and works for Neuroelectrics, a company dedicated to providing non-invasive stimulation solutions for patients. Klaus Schellhorn is Managing Director of neuroConn GmbH and a shareholder in neurocare group AG. Hartwig R. Siebner has received honoraria as speaker from Sanofi Genzyme, Denmark and Novartis, Denmark, as consultant from Sanofi Genzyme, Denmark and Lundbeck AS, Denmark, and as editor-in-chief (Neuroimage Clinical) and senior editor (NeuroImage) from Elsevier Publishers, Amsterdam, The Netherlands. He has received royalties as book editor from Springer Publishers, Stuttgart, Germany and from Gyldendal Publishers, Copenhagen, Denmark.

Figures

**Extended Data Fig. 1. PRISMA flow diagram for concurrent tES-fMRI studies.**
Diagram of the literature search (identification) and selection process (screening, eligibility, inclusion).

**Extended Data Fig. 2. Relationships between reporting score and publication context.**
a, Relation between reporting score of each article with its word count (Note: Article word count is not exactly accurate, since it is measured by counting the words from the beginning of the introduction to the end of the discussion part, thus it might include the running title of each page, footnotes, and the captions of figures and tables). b, Relation between reporting score of each article with its journal word limit (Note: word limitation for journals with no word limitation is counted as 15000). c, Relation between reporting score of each article with journal impact factor. d, Article reporting scores across the years. Relationships of figure a, b, and c were assessed using linear regressions, while a Kruskal-Wallis test was performed for figure d.

**Figure 1. Flowchart diagram of the Delphi process to develop the checklist.**
The Delphi process started with members of the steering committee defining the research problem. Then the field of concurrent tES-fMRI studies was systematically explored to find eligible people to invite to the steering committee and expert panel. The checklist was then developed by the steering committee and then was sent for revisions to the expert panel. After this phase the checklist was revised by the steering committee and then was sent for the rating phase. At the final stage, the ratings were analyzed. “n” indicates the number of participants in each group.

**Figure 2. Collected responses from contributors regarding the importance of the main items (rating phase).**
This figure depicts the rating of the checklist items by 54 respondents in the rating phase. Each item was rated from 1-5 (not important-extremely important). 14 items reached the 80% threshold (rated as either moderately, highly, or extremely important by more than 80% of the respondents). The items that did not reach this threshold are marked with "†"). 16 items reached the 70% threshold (rated as either moderately, highly, or extremely important by more than 70% of the respondents). The one item, which did not reach this threshold is marked with "‡". Full text of the items is provided in Tables 1-3.

**Figure 3. Collected responses of the contributors regarding the importance of recommendations (rating phase).**
Each additional recommendation was rated either “Yes” or “No” with respect to the question of whether it should be included as a recommendation. The recommendations rated with Yes by fewer than 50% of the respondents are marked with “#”. Recommendations are represented by their summary in the figure. Full text of the recommendations is provided in Tables 1-3.

**Figure 4. State of reproducibility/transparency in concurrent tES-fMRI research in the context of the ContES checklist.**
Assessments by 3 independent raters are based on 57 tES-fMRI papers, from the first published study up to January 1, 2020. a, Percentage of the articles that adhered to each checklist item. b, The checklist items adhered to by the 57 articles.

**Figure 5. Scheme of the concurrent tES-fMRI approach in the context of the ContES checklist.**
**(a) Summary of technological considerations.** MR conditional stimulator (1, item 1.1) is connected to the head through RF waveguide or RF penetration panel (7, item 1.7). Box cable should be aligned with the wall of the scanner room and run parallel to the bore axis (8, item 1.8). MR conditional stimulator is connected to the outer filter box or RF band-stop filter adapter as well as to the presentation computer trigger output cable. Synchronization module (9, item 1.9) should be connected to the presentation computer as well as to the MRI control computer. Electrode positioning (3, item 1.3) is used to accurately stimulate cortical target regions and exert neuromodulatory effects. A method allowing quantification of contact medium (e.g., syringes) should be used to achieve a consistent and appropriate amount of contact medium (5, item 1.5). MR conditional skin-electrode (e.g., saline solution, conductive paste, gel) (2, item 1.2) is used to facilitate delivery of current to the scalp (4, item 1.4). Electrode placement visualization can be used to reproducibly center each electrode on the head so that intrascanner stimulation allows verification of correct positioning of the electrodes on the head (6, item 1.6). **(b) Summary of safety considerations.** MR Conditionality Specifics for tES Setting include the technical specifications of the MR scanner, the applied fMRI sequences, and the used tES settings and configuration to fall within the specifics of MR conditionality based on tES manufacturer guideline (10, item 2.1). The Safety of the tES-fMRI Setting includes electrode temperature testing, electric current tolerance testing, etc. with real human subjects or phantoms (11, item 2.2). tES-fMRI Setting Test − Subjective Intolerance Reporting shows the number of cases that have not tolerated the tES-fMRI session (12, item 2.3). tES-fMRI Setting Test - Noise/Artifact shows the noise/artifact induced by the tES setting in the fMRI signal with real human subjects or phantoms before starting the study (13, item 2.4). The impedance is monitored before entering the scanner room and/or in the scanner room and/or inside the scanner and/or during scanning (14, item 2.5). **(c) Summary of methodological considerations.** Concurrent tES-fMRI Timing shows the timing of concurrent tES within the fMRI paradigm (15, item 3.1). Imaging Session Timing shows the imaging events before and after concurrent tES-fMRI and respective sequences (16, item 3.2). tES Experience Report includes the assessment of the subjective experience of receiving tES inside the scanner (17, item 3.3).

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References

1. Ligneul R, Obeso I, Ruff CC, Dreher J-C. Dynamical Representation of Dominance Relationships in the Human Rostromedial Prefrontal Cortex. Curr Biol. 2016;26:3107–3115. - PubMed
1. Zhang Y, Yu H, Yin Y, Zhou X. Intention Modulates the Effect of Punishment Threat in Norm Enforcement via the Lateral Orbitofrontal Cortex. J Neurosci. 2016;36:9217–9226. - PMC - PubMed
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[1] Ligneul R, Obeso I, Ruff CC, Dreher J-C. Dynamical Representation of Dominance Relationships in the Human Rostromedial Prefrontal Cortex. Curr Biol. 2016;26:3107–3115. - PubMed

[2] Ligneul R, Obeso I, Ruff CC, Dreher J-C. Dynamical Representation of Dominance Relationships in the Human Rostromedial Prefrontal Cortex. Curr Biol. 2016;26:3107–3115. - PubMed

[3] Zhang Y, Yu H, Yin Y, Zhou X. Intention Modulates the Effect of Punishment Threat in Norm Enforcement via the Lateral Orbitofrontal Cortex. J Neurosci. 2016;36:9217–9226. - PMC - PubMed

[4] Zhang Y, Yu H, Yin Y, Zhou X. Intention Modulates the Effect of Punishment Threat in Norm Enforcement via the Lateral Orbitofrontal Cortex. J Neurosci. 2016;36:9217–9226. - PMC - PubMed

[5] Baker JM, Rorden C, Fridriksson J. Using transcranial direct-current stimulation to treat stroke patients with aphasia. Stroke. 2010;41:1229–1236. - PMC - PubMed

[6] Baker JM, Rorden C, Fridriksson J. Using transcranial direct-current stimulation to treat stroke patients with aphasia. Stroke. 2010;41:1229–1236. - PMC - PubMed

[7] Wang Y, et al. Neural substrates of updating the prediction through prediction error during decision making. 2017;157:1–12. - PubMed

[8] Wang Y, et al. Neural substrates of updating the prediction through prediction error during decision making. 2017;157:1–12. - PubMed

[9] Frangou P, Correia M, Kourtzi Z. GABA, not BOLD, reveals dissociable learning-dependent plasticity mechanisms in the human brain. Elife. 2018;7 - PMC - PubMed

[10] Frangou P, Correia M, Kourtzi Z. GABA, not BOLD, reveals dissociable learning-dependent plasticity mechanisms in the human brain. Elife. 2018;7 - PMC - PubMed

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A checklist for assessing the methodological quality of concurrent tES-fMRI studies (ContES checklist): a consensus study and statement

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A checklist for assessing the methodological quality of concurrent tES-fMRI studies (ContES checklist): a consensus study and statement

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