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Brain connectivity signatures are becoming exceedingly useful for identifying patients, monitoring mental health disorders, and treatment. By using electroencephalography (EEG)-based cortical source localization along with energy landscape analysis techniques, we can statistically analyze transcranial magnetic stimulation (TMS)-invoked EEG signals, for obtaining connectivity among different brain regions at a high spatiotemporal resolution. (2) Methods: In this study, we analyze EEG-based source localized alpha wave activity in response to TMS administered to three locations, namely, the left motor cortex (49 subjects), left prefrontal cortex (27 subjects), and the posterior cerebellum, or vermis (27 subjects) by using energy landscape analysis techniques to uncover connectivity signatures. We then perform two sample t-tests and use the (5 \u00d7 10\u22125) Bonferroni corrected p-valued cases for reporting six reliably stable signatures. (3) Results: Vermis stimulation invoked the highest number of connectivity signatures and the left motor cortex stimulation invoked a sensorimotor network state. In total, six out of 29 reliable, stable connectivity signatures are found and discussed. (4) Conclusions: We extend previous findings to localized cortical connectivity signatures for medical applications that serve as a baseline for future dense electrode studies.<\/jats:p>","DOI":"10.3390\/s23084078","type":"journal-article","created":{"date-parts":[[2023,4,19]],"date-time":"2023-04-19T01:39:05Z","timestamp":1681868345000},"page":"4078","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Brain Connectivity Signature Extractions from TMS Invoked EEGs"],"prefix":"10.3390","volume":"23","author":[{"given":"Deepa","family":"Gupta","sequence":"first","affiliation":[{"name":"Computer Science and Electrical Engineering, University of Maryland Baltimore County, 1000 Hilltop Circle, Baltimore, MD 21227, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7206-5282","authenticated-orcid":false,"given":"Xiaoming","family":"Du","sequence":"additional","affiliation":[{"name":"Maryland Psychiatric Research Center, University of Maryland School of Medicine, 655 W. Baltimore Street, Baltimore, MD 21201, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ann","family":"Summerfelt","sequence":"additional","affiliation":[{"name":"Maryland Psychiatric Research Center, University of Maryland School of Medicine, 655 W. Baltimore Street, Baltimore, MD 21201, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"L. Elliot","family":"Hong","sequence":"additional","affiliation":[{"name":"Maryland Psychiatric Research Center, University of Maryland School of Medicine, 655 W. Baltimore Street, Baltimore, MD 21201, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9613-6110","authenticated-orcid":false,"given":"Fow-Sen","family":"Choa","sequence":"additional","affiliation":[{"name":"Computer Science and Electrical Engineering, University of Maryland Baltimore County, 1000 Hilltop Circle, Baltimore, MD 21227, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2023,4,18]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Charlson, F.J., Dieleman, J., Singh, L., and Whiteford, H.A. (2017). Donor Financing of Global Mental Health, 1995\u20142015: An Assessment of Trends, Channels, and Alignment with the Disease Burden. PLoS ONE, 12.","DOI":"10.1371\/journal.pone.0169384"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"435","DOI":"10.1038\/s41583-019-0177-6","article-title":"A Cross-Disorder Connectome Landscape of Brain Dysconnectivity","volume":"20","author":"Sporns","year":"2019","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"706","DOI":"10.1097\/WCO.0000000000000396","article-title":"Brain Connectivity and Neurological Disorders after Stroke","volume":"29","author":"Baldassarre","year":"2016","journal-title":"Curr. Opin. Neurol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1038\/nrneurol.2014.178","article-title":"Brain Connectivity in Neurodegenerative Diseases\u2014from Phenotype to Proteinopathy","volume":"10","author":"Pievani","year":"2014","journal-title":"Nat. Rev. Neurol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"3328","DOI":"10.1038\/s41467-022-31053-5","article-title":"Association between Resting-State Functional Brain Connectivity and Gene Expression Is Altered in Autism Spectrum Disorder","volume":"13","author":"Berto","year":"2022","journal-title":"Nat. Commun."},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Carson, R.G., Ruddy, K.L., and McNickle, E. (2016). What Do TMS-Evoked Motor Potentials Tell Us about Motor Learning?. Prog. Mot. Control Theor. Transl., 143\u2013157.","DOI":"10.1007\/978-3-319-47313-0_8"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"2475","DOI":"10.1152\/jn.00543.2011","article-title":"Time-Frequency Analysis of Short-Lasting Modulation of EEG induced by intracortical and transcallosal paired TMS over motor areas","volume":"107","author":"Zamboni","year":"2012","journal-title":"J. Neurophysiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1740","DOI":"10.1002\/hbm.22288","article-title":"The Spontaneous Fluctuation of the Excitability of a Single Node Modulates the Internodes Connectivity: A TMS-EEG Study","volume":"35","author":"Giambattistelli","year":"2014","journal-title":"Hum. Brain Mapp."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1016\/S0165-0173(03)00191-7","article-title":"Combining Transcranial Magnetic Stimulation and Functional Imaging in Cognitive Brain Research: Possibilities and Limitations","volume":"43","author":"Sack","year":"2003","journal-title":"Brain Res. Rev."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1016\/j.neubiorev.2014.12.014","article-title":"The Contribution of TMS\u2013EEG Coregistration in the Exploration of the Human Cortical Connectome","volume":"49","author":"Bortoletto","year":"2015","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"881","DOI":"10.1162\/jocn_a_01094","article-title":"A TMS Investigation on the Role of Lateral Occipital Complex and Caudal Intraparietal Sulcus in the Perception of Object Form and Orientation","volume":"29","author":"Chouinard","year":"2017","journal-title":"J. Cogn. Neurosci."},{"key":"ref_12","first-page":"e3456","article-title":"Transcranial Magnetic Stimulation as a Therapeutic Option for Neurologic and Psychiatric Illnesses","volume":"10","author":"Habib","year":"2018","journal-title":"Cureus"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1111\/j.1460-9568.2012.08035.x","article-title":"Exploration and Modulation of Brain Network Interactions with Noninvasive Brain Stimulation in Combination with Neuroimaging","volume":"35","author":"Shafi","year":"2012","journal-title":"Eur. J. Neurosci."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1136\/jnnp.74.1.9","article-title":"Hans Berger (1873\u20131941), Richard Caton (1842\u20131926), and Electroencephalography","volume":"74","author":"Haas","year":"2003","journal-title":"J. Neurol. Neurosurg. Psychiatry"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1007\/s10548-009-0115-4","article-title":"A Review of Combined TMS-EEG Studies to Characterize Lasting Effects of Repetitive TMS and Assess Their Usefulness in Cognitive and Clinical Neuroscience","volume":"22","author":"Thut","year":"2010","journal-title":"Brain Topogr."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"734","DOI":"10.1162\/jocn.2008.20048","article-title":"The Functional Effect of Transcranial Magnetic Stimulation: Signal Suppression or Neural Noise Generation?","volume":"20","author":"Harris","year":"2008","journal-title":"J. Cogn. Neurosci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1007\/s11920-019-1076-2","article-title":"Investigational and Therapeutic Applications of Transcranial Magnetic Stimulation in Schizophrenia","volume":"21","author":"Mehta","year":"2019","journal-title":"Curr. Psychiatry Rep."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"400","DOI":"10.1176\/appi.ajp.2020.20071050","article-title":"Examining and Modulating Neural Circuits in Psychiatric Disorders with Transcranial Magnetic Stimulation and Electroencephalography: Present Practices and Future Developments","volume":"178","author":"Ferrarelli","year":"2021","journal-title":"AJP"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1001\/archpsyc.1965.01730040077011","article-title":"Alpha Blocking and Schizophrenia: I. Methodology and Initial Studies","volume":"13","author":"SALAMON","year":"1965","journal-title":"Arch. Gen. Psychiatry"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1088","DOI":"10.1016\/S0006-3223(00)00907-0","article-title":"Clinical and Biological Concomitants of Resting State EEG Power Abnormalities in Schizophrenia","volume":"48","author":"Sponheim","year":"2000","journal-title":"Biol. Psychiatry"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"69","DOI":"10.1007\/s00221-016-4773-7","article-title":"N100 as a Generic Cortical Electrophysiological Marker Based on Decomposition of TMS-Evoked Potentials across Five Anatomic Locations","volume":"235","author":"Du","year":"2017","journal-title":"Exp. Brain Res."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.biopsych.2018.06.007","article-title":"Aberrant Middle Prefrontal-Motor Cortex Connectivity Mediates Motor Inhibitory Biomarker in Schizophrenia","volume":"85","author":"Du","year":"2019","journal-title":"Biol. Psychiatry"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.schres.2021.10.005","article-title":"Intermittent Theta Burst Stimulation of Cerebellar Vermis Enhances Fronto-Cerebellar Resting State Functional Connectivity in Schizophrenia with Predominant Negative Symptoms: A Randomized Controlled Trial","volume":"238","author":"Basavaraju","year":"2021","journal-title":"Schizophr. Res."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"20160287","DOI":"10.1098\/rsta.2016.0287","article-title":"Energy Landscape Analysis of Neuroimaging Data","volume":"375","author":"Ezaki","year":"2017","journal-title":"Philos. Trans. R. Soc. A Math. Phys. Eng. Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"89","DOI":"10.3390\/e12010089","article-title":"Maximum Entropy Approaches to Living Neural Networks","volume":"12","author":"Yeh","year":"2010","journal-title":"Entropy"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"e237898","DOI":"10.1155\/2014\/237898","article-title":"Highlighting the Structure-Function Relationship of the Brain with the Ising Model and Graph Theory","volume":"2014","author":"Das","year":"2014","journal-title":"BioMed Res. Int."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1016\/j.conb.2016.03.001","article-title":"Towards the Design Principles of Neural Population Codes","volume":"37","author":"Schneidman","year":"2016","journal-title":"Curr. Opin. Neurobiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1370","DOI":"10.1038\/ncomms2388","article-title":"A Pairwise Maximum Entropy Model Accurately Describes Resting-State Human Brain Networks","volume":"4","author":"Watanabe","year":"2013","journal-title":"Nat. Commun."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Klepl, D., He, F., Wu, M., De Marco, M., Blackburn, D.J., and Sarrigiannis, P. (2021). Characterising Alzheimer\u2019s Disease with EEG-Based Energy Landscape Analysis. arXiv.","DOI":"10.1109\/JBHI.2021.3105397"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/j.jneumeth.2003.10.009","article-title":"EEGLAB: An Open Source Toolbox for Analysis of Single-Trial EEG Dynamics Including Independent Component Analysis","volume":"134","author":"Delorme","year":"2004","journal-title":"J. Neurosci. Methods"},{"key":"ref_31","first-page":"5","article-title":"Standardized Low-Resolution Brain Electromagnetic Tomography (SLORETA): Technical Details","volume":"24","year":"2002","journal-title":"Methods Find Exp. Clin. Pharmacol."},{"key":"ref_32","unstructured":"Talairach, J., and Tournoux, P. (1988). Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging. Thieme, 1\u2013122."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1016\/S0896-6273(00)81138-1","article-title":"Dynamic Statistical Parametric Mapping: Combining FMRI and MEG for High-Resolution Imaging of Cortical Activity","volume":"26","author":"Dale","year":"2000","journal-title":"Neuron"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1348","DOI":"10.1038\/nn.3470","article-title":"Multi-Task Connectivity Reveals Flexible Hubs for Adaptive Task Control","volume":"16","author":"Cole","year":"2013","journal-title":"Nat. Neurosci."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"809","DOI":"10.21037\/atm.2019.12.45","article-title":"Psychological Resilience Negatively Correlates with Resting-State Brain Network Flexibility in Young Healthy Adults: A Dynamic Functional Magnetic Resonance Imaging Study","volume":"7","author":"Long","year":"2019","journal-title":"Ann. Transl. Med."},{"key":"ref_36","unstructured":"Kandel, E.R., Schwartz, J.H., Jessell, T.M., Jessell, M.B.T., Siegelbaum, S., and Hudspeth, A.J. (2000). Principles of Neural Science, McGraw-Hill."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"15466","DOI":"10.1523\/JNEUROSCI.1488-13.2013","article-title":"Right supramarginal gyrus is crucial to overcome emotional egocentricity bias in social judgments","volume":"33","author":"Silani","year":"2013","journal-title":"J. Neurosci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"16494","DOI":"10.1073\/pnas.1008121107","article-title":"Phonological decisions require both the left and right supramarginal gyri","volume":"107","author":"Hartwigsen","year":"2010","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1016\/j.tics.2011.08.003","article-title":"Large-Scale Brain Networks and Psychopathology: A Unifying Triple Network Model","volume":"15","author":"Menon","year":"2011","journal-title":"Trends Cogn. Sci."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"23","DOI":"10.3389\/fnsys.2015.00023","article-title":"A Role of Right Middle Frontal Gyrus in Reorienting of Attention: A Case Study","volume":"9","author":"Japee","year":"2015","journal-title":"Front. Syst. Neurosci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"e63591","DOI":"10.7554\/eLife.63591","article-title":"Functional Specialization within the Inferior Parietal Lobes across Cognitive Domains","volume":"10","author":"Numssen","year":"2021","journal-title":"eLife"},{"key":"ref_42","first-page":"85","article-title":"Three-Dimension EEG-Based Connectivity Biomarkers for Neurological Disorder Detections","volume":"12123","author":"Gupta","year":"2022","journal-title":"Proc. SPIE Smart Biomed. Physiol. Sens. Technol. XIX"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.brs.2012.02.005","article-title":"Electric Field Depth\u2013Focality Tradeoff in Transcranial Magnetic Stimulation: Simulation Comparison of 50 Coil Designs","volume":"6","author":"Deng","year":"2013","journal-title":"Brain Stimul."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"767","DOI":"10.1007\/s10548-020-00797-y","article-title":"Dual-Site RTMS Is More Effective than Single-Site RTMS in Tinnitus Patients: A Blinded Randomized Controlled Trial","volume":"33","author":"Noh","year":"2020","journal-title":"Brain Topogr."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"026059","DOI":"10.1088\/1741-2552\/ac697c","article-title":"Angle-Tuned Coils: Attractive Building Blocks for TMS with Improved Depth-Spread Performance","volume":"19","author":"Bagherzadeh","year":"2022","journal-title":"J. Neural Eng."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1038\/s41394-020-0320-7","article-title":"Enabling and Promoting Walking Rehabilitation by Paired Associative Stimulation after Incomplete Paraplegia: A Case Report","volume":"6","author":"Shulga","year":"2020","journal-title":"Spinal Cord Ser. Cases"},{"key":"ref_47","unstructured":"Sherrington, C.S. (1906). The Integrative Action of the Nervous System, Yale University Press."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"1049","DOI":"10.1038\/79871","article-title":"Subcortical and Cortical Brain Activity during the Feeling of Self-Generated Emotions","volume":"3","author":"Damasio","year":"2000","journal-title":"Nat. Neurosci."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"2349","DOI":"10.1523\/JNEUROSCI.5587-06.2007","article-title":"Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control","volume":"27","author":"Seeley","year":"2007","journal-title":"J. Neurosci."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Varanasi, S., Tuli, R., Han, F., Chen, R., and Choa, F.-S. (2023). Age Related Functional Connectivity Signature Extraction Using Energy-Based Machine Learning Techniques. Sensors, 23.","DOI":"10.3390\/s23031603"},{"key":"ref_51","first-page":"47","article-title":"Comparing Energy Levels in Brain Regions of Interest in ADHD Subjects","volume":"12123","author":"Udall","year":"2022","journal-title":"Proc. SPIE Smart Biomed. Physiol. Sens. Technol. XIV"}],"container-title":["Sensors"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1424-8220\/23\/8\/4078\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:18:17Z","timestamp":1760123897000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1424-8220\/23\/8\/4078"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,18]]},"references-count":51,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2023,4]]}},"alternative-id":["s23084078"],"URL":"https:\/\/doi.org\/10.3390\/s23084078","relation":{},"ISSN":["1424-8220"],"issn-type":[{"value":"1424-8220","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,4,18]]}}}