Stimulation-Based Control of Dynamic Brain Networks

PLoS Computational Biology

Volumn 12, Issue 9, 2016, Pages

  Muldoon, Sarah Feldt ^a,b,c   Pasqualetti, Fabio ^d   Gu, Shi ^a,e   Cieslak, Matthew ^f   Grafton, Scott T ^f   Vettel, Jean M ^a,b,f   Bassett, Danielle S ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b U S ARMY RESEARCH LABORATORY   (United States)

^c UNIVERSITY AT BUFFALO   (United States)

^d University of California Riverside   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; BRAIN MAPPING; COMPUTATION THEORY; NETWORK ARCHITECTURE;

BRAIN DYNAMICS; BRAIN NETWORKS; BRAIN STATE; BRAIN STIMULATION; COMPUTATIONAL MODELLING; DATA DRIVEN; HUMAN PERFORMANCE; NETWORK LEVEL; NEUROLOGICAL DISORDERS; NEUROMODULATION;

COGNITIVE SYSTEMS;

BRAIN REGION; GLOBAL CHANGE; HUMAN; PREDICTION; THEORETICAL MODEL; ADULT; BIOLOGICAL MODEL; BIOLOGY; BRAIN; BRAIN MAPPING; COMPUTER SIMULATION; ELECTROTHERAPY; FEMALE; MALE; NERVE CELL NETWORK; PHYSIOLOGY; YOUNG ADULT;

ADULT; BRAIN; BRAIN MAPPING; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; ELECTRIC STIMULATION THERAPY; FEMALE; HUMANS; MALE; MODELS, NEUROLOGICAL; NERVE NET; YOUNG ADULT;

EID: 84989329186     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1005076     Document Type: Article

References (62)

1. Volz LJ, Sarfeld AS, Diekhoff S, Rehme AK, Pool EM, Eickhoff SB, et al. Motor cortex excitability and connectivity in chronic stroke: a multimodal model of functional reorganization. Brain structure & function. 2015Mar;220(2):1093–1107. doi: 10.1007/s00429-013-0702-8
2. Helfrich C, Pierau SS, Freitag CM, Roeper J, Ziemann U, Bender S, Monitoring cortical excitability during repetitive transcranial magnetic stimulation in children with ADHD: a single-blind, sham-controlled TMS-EEG study. PloS one. 2012;7(11):e50073. doi: 10.1371/journal.pone.005007323185537
3. Tierney TS, Vasudeva VS, Weir S, Hayes MT, Neuromodulation for neurodegenerative conditions. Frontiers in bioscience (Elite edition). 2013;5:490–499. doi: 10.2741/E630
4. Temel Y, Hescham SA, Jahanshahi A, Janssen MLF, Tan SKH, van Overbeeke JJ, et al. Neuromodulation in psychiatric disorders. International review of neurobiology. 2012;107:283–314. doi: 10.1016/B978-0-12-404706-8.00015-223206687
5. Terra VC, Amorim R, Silvado C, Oliveira AJd, Jorge CL, Faveret E, et al. Vagus nerve stimulator in patients with epilepsy: indications and recommendations for use.; 2013. Associação Arquivos de Neuro-Psiquiatria. doi: 10.1590/0004-282X20130116
6. DeGiorgio CM, Krahl SE, Neurostimulation for Drug-Resistant Epilepsy. Continuum: Lifelong Learning in Neurology. 2013Jun;19(3 Epilepsy):743–755. doi: 10.1212/01.CON.0000431397.61970.2b23739108
7. Di Lazzaro V, Rothwell JC, Talelli P, Capone F, Ranieri F, Wallace AC, et al. Inhibitory theta burst stimulation of affected hemisphere in chronic stroke: A proof of principle, sham-controlled study. Neuroscience Letters. 2013Oct;553:148–152. doi: 10.1016/j.neulet.2013.08.01323978513
8. Vanneste S, Fregni F, De Ridder D, Head-to-Head Comparison of Transcranial Random Noise Stimulation, Transcranial AC Stimulation, and Transcranial DC Stimulation for Tinnitus. Frontiers in psychiatry. 2013;4:158. doi: 10.3389/fpsyt.2013.0015824391599
9. Jürgens TP, Leone M, Pearls and pitfalls: neurostimulation in headache. Cephalalgia: an international journal of headache. 2013Jun;33(8):512–525. doi: 10.1177/0333102413483933
10. Shah PP, Szaflarski JP, Allendorfer J, Hamilton RH, Induction of neuroplasticity and recovery in post-stroke aphasia by non-invasive brain stimulation. Frontiers in human neuroscience. 2013;7:888. doi: 10.3389/fnhum.2013.0088824399952
11. Bonnì S, Mastropasqua C, Bozzali M, Caltagirone C, Koch G, Theta burst stimulation improves visuo-spatial attention in a patient with traumatic brain injury. Neurological sciences: official journal of the Italian Neurological Society and of the Italian Society of Clinical Neurophysiology. 2013Nov;34(11):2053–2056. doi: 10.1007/s10072-013-1412-y
12. Hasan A, Falkai P, Wobrock T, Transcranial brain stimulation in schizophrenia: targeting cortical excitability, connectivity and plasticity. Current medicinal chemistry. 2013;20(3):405–413. doi: 10.2174/092986731132003001223157633
13. Berardelli A, Suppa A, Noninvasive brain stimulation in Huntington’s disease. Handbook of clinical neurology. 2013;116:555–560. doi: 10.1016/B978-0-444-53497-2.00044-924112923
14. Andrade DC, Borges I, Bravo GL, Bolognini N, Fregni F, Therapeutic time window of noninvasive brain stimulation for pain treatment: inhibition of maladaptive plasticity with early intervention. Expert review of medical devices. 2013May;10(3):339–352. doi: 10.1586/erd.12.9023668706
15. Lozano AM, Lipsman N, Probing and regulating dysfunctional circuits using deep brain stimulation. Neuron. 2013Feb;77(3):406–424. doi: 10.1016/j.neuron.2013.01.02023395370
16. Meinzer M, Jähnigen S, Copland DA, Darkow R, Grittner U, Avirame K, et al. Transcranial direct current stimulation over multiple days improves learning and maintenance of a novel vocabulary. Cortex; a journal devoted to the study of the nervous system and behavior. 2014Jan;50:137–147. doi: 10.1016/j.cortex.2013.07.013
17. Ferreri F, Rossini PM, TMS and TMS-EEG techniques in the study of the excitability, connectivity, and plasticity of the human motor cortex. Reviews in the neurosciences. 2013;24(4):431–442. doi: 10.1515/revneuro-2013-001923907420
18. Johnson MD, Lim HH, Netoff TI, Connolly AT, Johnson N, Roy A, et al. Neuromodulation for brain disorders: challenges and opportunities. IEEE Trans Biomed Eng. 2013Mar;60(3):610–624. doi: 10.1109/TBME.2013.224489023380851
19. Chaieb L, Kovacs G, Cziraki C, Greenlee M, Paulus W, Antal A, Short-duration transcranial random noise stimulation induces blood oxygenation level dependent response attenuation in the human motor cortex. Experimental brain research. 2009Oct;198(4):439–444. doi: 10.1007/s00221-009-1938-719649624
20. Hess CW, Modulation of cortical-subcortical networks in Parkinson’s disease by applied field effects. Frontiers in human neuroscience. 2013;7:565. doi: 10.3389/fnhum.2013.0056524062667
21. Grafton ST, Turner RS, Desmurget M, Bakay R, Delong M, Vitek J, et al. Normalizing motor-related brain activity: subthalamic nucleus stimulation in Parkinson disease. Neurology. 2006Apr;66(8):1192–1199. doi: 10.1212/01.wnl.0000214237.58321.c316636237
22. Soekadar SR, Witkowski M, Cossio EG, Birbaumer N, Robinson SE, Cohen LG, In vivo assessment of human brain oscillations during application of transcranial electric currents. Nature Communications. 2013;4:2032. doi: 10.1038/ncomms303223787780
23. Parks NA, Maclin EL, Low KA, Beck DM, Fabiani M, Gratton G, Examining cortical dynamics and connectivity with simultaneous single-pulse transcranial magnetic stimulation and fast optical imaging. NeuroImage. 2012Feb;59(3):2504–2510. doi: 10.1016/j.neuroimage.2011.08.09721925608
24. Pascual-Leone A, Freitas C, Oberman L, Horvath JC, Halko M, Eldaief M, et al. Characterizing Brain Cortical Plasticity and Network Dynamics Across the Age-Span in Health and Disease with TMS-EEG and TMS-fMRI. Brain Topogr. 2011;24(3-4):302–315. doi: 10.1007/s10548-011-0196-821842407
25. Leitão J, Thielscher A, Werner S, Pohmann R, Noppeney U, Effects of parietal TMS on visual and auditory processing at the primary cortical level—a concurrent TMS-fMRI study. Cerebral Cortex. 2013Apr;23(4):873–884. doi: 10.1093/cercor/bhs07822490546
26. Levit-Binnun N, Handzy NZ, Moses E, Modai I, Peled A, Transcranial Magnetic Stimulation at M1 disrupts cognitive networks in schizophrenia. Schizophrenia Research. 2007Jul;93(1-3):334–344. doi: 10.1016/j.schres.2007.02.01917433627
27. Grefkes C, Fink GR, Reorganization of cerebral networks after stroke: new insights from neuroimaging with connectivity approaches. Brain: a journal of neurology. 2011May;134(Pt 5):1264–1276. doi: 10.1093/brain/awr033
28. Arzouan Y, Moses E, Peled A, Levit-Binnun N, Impaired network stability in schizophrenia revealed by TMS perturbations. Schizophrenia Research. 2014Jan;152(1):322–324. doi: 10.1016/j.schres.2013.11.01724331871
29. Bestmann S, Feredoes E, Combined neurostimulation and neuroimaging in cognitive neuroscience: past, present, and future. Annals of the New York Academy of Sciences. 2013Aug;1296(1):11–30. doi: 10.1111/nyas.1211023631540
30. Gu S, Pasqualetti F, Cieslak M, Telesford QK, Yu AB, Kahn AE, et al. Controllability of structural brain networks. Nature Communications. 2015;6:8414. doi: 10.1038/ncomms941426423222
31. Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ, et al. Mapping the structural core of human cerebral cortex. PLoS Biology. 2008Jul;6(7):e159. doi: 10.1371/journal.pbio.006015918597554
32. Wilson HR, Cowan JD, Excitatory and inhibitory interactions in localized populations of model neurons. Biophysj. 1972Jan;12(1):1–24. doi: 10.1016/S0006-3495(72)86068-5
33. Wilson HR, Cowan JD, A mathematical theory of the functional dynamics of cortical and thalamic nervous tissue. Kybernetik. 1973Sep;13(2):55–80. doi: 10.1007/BF002887864767470
34. Power JD, Cohen AL, Nelson SM, Wig GS, Barnes KA, Church JA, et al. Functional Network Organization of the Human Brain. Neuron. 2011Nov;72(4):665–678. doi: 10.1016/j.neuron.2011.09.00622099467
35. Horn A, Ostwald D, Reisert M, Blankenburg F, The structural–functional connectome and the default mode network of the human brain. NeuroImage. 2014Nov;102(P1):142–151. doi: 10.1016/j.neuroimage.2013.09.06924099851
36. Gu S, Satterthwaite TD, Medaglia JD, Yang M, Gur RE, Gur RC, et al. Emergence of system roles in normative neurodevelopment. Proceedings of the National Academy of Sciences of the United States of America. 2015Nov;112(44):13681–13686. doi: 10.1073/pnas.150282911226483477
37. Bassett DS, Brown JA, Deshpande V, Carlson JM, Grafton ST, Conserved and variable architecture of human white matter connectivity. NeuroImage. 2011Jan;54(2):1262–1279. doi: 10.1016/j.neuroimage.2010.09.00620850551
38. Lecce F, Walsh V, Didino D, Cappelletti M, ’How many’ and’how much’ dissociate in the parietal lobe. Cortex. 2015;73:73–79. doi: 10.1016/j.cortex.2015.08.00726386441
39. Kraft A, Dyrholm M, Kehrer S, Kaufmann C, Bruening J, Kathmann N, et al. TMS over the right precuneus reduces the bilateral field advantage in visual short term memory capacity. Brain Stimul. 2015;8(2):216–223. doi: 10.1016/j.brs.2014.11.00425481073
40. Bonni S, Veniero D, Mastropasqua C, Ponzo V, Caltagirone C, Bozzali M, et al. TMS evidence for a selective role of the precuneus in source memory retrieval. Behav Brain Res. 2015;282:70–75. doi: 10.1016/j.bbr.2014.12.03225541040
41. Crescentini C, Di Bucchianico M, Fabbro F, Urgesi C, Excitatory stimulation of the right inferior parietal cortex lessens implicit religiousness/spirituality. Neuropsychologia. 2015;70:71–79. doi: 10.1016/j.neuropsychologia.2015.02.01625697502
42. Pasqualetti F, Zampieri S, Bullo F, Controllability metrics, limitations and algorithms for complex networks. IEEE Trans Control Netw Syst. 2014;1:40–52. doi: 10.1109/TCNS.2014.2310254
43. Kailath T, Linear Systems. Prentice-Hall; 1980.
44. Honey CJ, Sporns O, Cammoun L, Gigandet X, Thiran JP, Meuli R, et al. Predicting human resting-state functional connectivity from structural connectivity. Proc Natl Acad Sci USA. 2009;106(6):2035–40. doi: 10.1073/pnas.081116810619188601
45. Honey CJ, Thivierge JP, Sporns O, Can structure predict function in the human brain?Neuroimage. 2010;52(3):766–776. 20116438
46. Goñi J, van den Heuvel MP, Avena-Koenigsberger A, Velez de Mendizabal N, Betzel RF, Griffa A, et al. Resting-brain functional connectivity predicted by analytic measures of network communication. Proc Natl Acad Sci U S A. 2014;111(2):833–838. doi: 10.1073/pnas.131552911124379387
47. Hermundstad AM, Bassett DS, Brown KS, Aminoff EM, Clewett D, Freeman S, et al. Structural foundations of resting-state and task-based functional connectivity in the human brain. Proceedings of the National Academy of Sciences of the United States of America. 2013Apr;110(15):6169–6174. doi: 10.1073/pnas.121956211023530246
48. Hermundstad AM, Brown KS, Bassett DS, Aminoff EM, Frithsen A, Johnson A, et al. Structurally-Constrained Relationships between Cognitive States in the Human Brain. PLoS Computational Biology. 2014May;10(5):e1003591. doi: 10.1371/journal.pcbi.100359124830758
49. Cornelius SP, Kath WL, Motter AE, Realistic control of network dynamics. Nat Commun. 2013;4:1942. doi: 10.1038/ncomms293923803966
50. Sun J, Motter AE, Controllability transition and nonlocality in network control. Phys Rev Lett. 2013;110(20):208701. doi: 10.1103/PhysRevLett.110.20870125167459
51. Goñi J, van den Heuvel MP, Avena-Koenigsberger A, Velez de Mendizabal N, Betzel RF, Griffa A, et al. Resting-brain functional connectivity predicted by analytic measures of network communication. Proceedings of the National Academy of Sciences of the United States of America. 2014Jan;111(2):833–838. doi: 10.1073/pnas.131552911124379387
52. Cieslak M, Grafton ST, Local termination pattern analysis: a tool for comparing white matter morphology. Brain imaging and behavior. 2014Jun;8(2):292–299. doi: 10.1007/s11682-013-9254-z23999931
53. Yeh FC, Tseng WYI, NTU-90: a high angular resolution brain atlas constructed by q-space diffeomorphic reconstruction. NeuroImage. 2011Sep;58(1):91–99. doi: 10.1016/j.neuroimage.2011.06.02121704171
54. Dale AM, Fischl B, Sereno MI, Segmentation and surface reconstruction. NeuroImage. 1999Feb;9(2):179–194. doi: 10.1006/nimg.1998.03959931268
55. Cammoun L, Gigandet X, Meskaldji D, Thiran JP, Sporns O, Do KQ, et al. Mapping the human connectome at multiple scales with diffusion spectrum MRI. Journal of Neuroscience Methods. 2012Jan;203(2):386–397. doi: 10.1016/j.jneumeth.2011.09.03122001222
56. Wei X, Yoo SS, Dickey CC, Zou KH, Guttmann CRG, Panych LP, Functional MRI of auditory verbal working memory: long-term reproducibility analysis. NeuroImage. 2004Mar;21(3):1000–1008. doi: 10.1016/j.neuroimage.2003.10.03915006667
57. Kalman RE, Ho YC, Narendra KS, Controllability of linear dynamical systems. Contributions to Differential Equations. 1963;1(1):189–213.
58. Marx B, Koenig D, Georges D, Optimal sensor and actuator location for descriptor systems using generalized Gramians and balanced realizations. 2004;3:2729–2734vol.3.
59. Shaker HR, Tahavori M, Optimal sensor and actuator location for unstable systems. Journal of Vibration and Control. 2012Jul;19(12):1077546312451302–1920.
60. Hamdan AMA, Nayfeh AH, Measures of modal controllability and observability for first- and second-order linear systems. Journal of Guidance, Control, and Dynamics. 1989;12(3):421–428. doi: 10.2514/3.20424
61. Kramer M, Eden U, Cash S, Kolaczyk E, Network inference with confidence from multivariate time series. Physical Review E. 2009Jun;79(6):061916. doi: 10.1103/PhysRevE.79.061916
62. Feldt S, Osterhage H, Mormann F, Lehnertz K, Zochowski M, Internetwork and intranetwork communications during bursting dynamics: Applications to seizure prediction. Physical Review E. 2007Aug;76(2):021920. doi: 10.1103/PhysRevE.76.021920