Stimulation-Based Control of Dynamic Brain Networks

Abstract

The ability to modulate brain states using targeted stimulation is increasingly being employed to treat neurological disorders and to enhance human performance. Despite the growing interest in brain stimulation as a form of neuromodulation, much remains unknown about the network-level impact of these focal perturbations. To study the system wide impact of regional stimulation, we employ a data-driven computational model of nonlinear brain dynamics to systematically explore the effects of targeted stimulation. Validating predictions from network control theory, we uncover the relationship between regional controllability and the focal versus global impact of stimulation, and we relate these findings to differences in the underlying network architecture. Finally, by mapping brain regions to cognitive systems, we observe that the default mode system imparts large global change despite being highly constrained by structural connectivity. This work forms an important step towards the development of personalized stimulation protocols for medical treatment or performance enhancement.

Full text

Its licence does not allow us to show the full text. Read it at PubMed Central:

References 62

1. 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. 2015 3;220(2):1093–1107.

   Not in our library10.1007/s00429-013-0702-8

2. 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

   Not in our library10.1371/journal.pone.0050073

3. 3.

   Tierney TS, Vasudeva VS, Weir S, Hayes MT. Neuromodulation for neurodegenerative conditions. Frontiers in bioscience (Elite edition). 2013;5:490–499.

   Not in our library10.2741/e630

4. 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.

   Not in our library10.1016/b978-0-12-404706-8.00015-2

5. 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.

   Not in our library10.1590/0004-282x20130116

6. 6.

   DeGiorgio CM, Krahl SE. Neurostimulation for Drug-Resistant Epilepsy. Continuum: Lifelong Learning in Neurology. 2013 6;19(3 Epilepsy):743–755.

   Not in our library10.1212/01.con.0000431397.61970.2b

7. 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. 2013 10;553:148–152.

   Not in our library10.1016/j.neulet.2013.08.013

8. 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

   Not in our library10.3389/fpsyt.2013.00158

9. 9.

   Jürgens TP, Leone M. Pearls and pitfalls: neurostimulation in headache. Cephalalgia: an international journal of headache. 2013 6;33(8):512–525.

   Not in our library10.1177/0333102413483933

10. 10.
    Induction of neuroplasticity and recovery in post-stroke aphasia by non-invasive brain stimulation · 2013

    Not checked
11. 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. 2013 11;34(11):2053–2056.

    Not in our library10.1007/s10072-013-1412-y

12. 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.

    Not in our library10.2174/0929867311320030012

13. 13.

    Berardelli A, Suppa A. Noninvasive brain stimulation in Huntington’s disease. Handbook of clinical neurology. 2013;116:555–560.

    Not in our library10.1016/b978-0-444-53497-2.00044-9

14. 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. 2013 5;10(3):339–352.

    Not in our library10.1586/erd.12.90

15. 15.

    Lozano AM, Lipsman N. Probing and regulating dysfunctional circuits using deep brain stimulation. Neuron. 2013 2;77(3):406–424.

    Not in our library10.1016/j.neuron.2013.01.020

16. 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. 2014 1;50:137–147.

    Not in our library10.1016/j.cortex.2013.07.013

17. 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.

    Not in our library10.1515/revneuro-2013-0019

18. 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. 2013 3;60(3):610–624.

    Not in our library10.1109/tbme.2013.2244890

19. 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. 2009 10;198(4):439–444.

    Not in our library10.1007/s00221-009-1938-7

20. 20.

    Hess CW. Modulation of cortical-subcortical networks in Parkinson’s disease by applied field effects. Frontiers in human neuroscience. 2013;7:565

    Not in our library10.3389/fnhum.2013.00565

21. 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. 2006 4;66(8):1192–1199.

    Not in our library10.1212/01.wnl.0000214237.58321.c3

22. 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

    Not in our library10.1038/ncomms3032

23. 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. 2012 2;59(3):2504–2510.

    Not in our library10.1016/j.neuroimage.2011.08.097

24. 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.

    Not in our library10.1007/s10548-011-0196-8

25. 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. 2013 4;23(4):873–884.

    Not in our library10.1093/cercor/bhs078

26. 26.

    Levit-Binnun N, Handzy NZ, Moses E, Modai I, Peled A. Transcranial Magnetic Stimulation at M1 disrupts cognitive networks in schizophrenia. Schizophrenia Research. 2007 7;93(1-3):334–344.

    Not in our library10.1016/j.schres.2007.02.019

27. 27.

    Grefkes C, Fink GR. Reorganization of cerebral networks after stroke: new insights from neuroimaging with connectivity approaches. Brain: a journal of neurology. 2011 5;134(Pt 5):1264–1276.

    Not in our library10.1093/brain/awr033

28. 28.

    Arzouan Y, Moses E, Peled A, Levit-Binnun N. Impaired network stability in schizophrenia revealed by TMS perturbations. Schizophrenia Research. 2014 1;152(1):322–324.

    Not in our library10.1016/j.schres.2013.11.017

29. 29.

    Bestmann S, Feredoes E. Combined neurostimulation and neuroimaging in cognitive neuroscience: past, present, and future. Annals of the New York Academy of Sciences. 2013 8;1296(1):11–30.

    Not in our library10.1111/nyas.12110

30. 30.
    Controllability of structural brain networks · 2015

    No notice
31. 31.
    Mapping the Structural Core of Human Cerebral Cortex · 2008

    No notice
32. 32.

    Wilson HR, Cowan JD. Excitatory and inhibitory interactions in localized populations of model neurons. Biophysj. 1972 1;12(1):1–24.

    Not in our library10.1016/s0006-3495(72)86068-5

33. 33.

    Wilson HR, Cowan JD. A mathematical theory of the functional dynamics of cortical and thalamic nervous tissue. Kybernetik. 1973 9;13(2):55–80.

    Not in our library10.1007/bf00288786

34. 34.

    Power JD, Cohen AL, Nelson SM, Wig GS, Barnes KA, Church JA, et al Functional Network Organization of the Human Brain. Neuron. 2011 11;72(4):665–678.

    Not in our library10.1016/j.neuron.2011.09.006

35. 35.

    Horn A, Ostwald D, Reisert M, Blankenburg F. The structural–functional connectome and the default mode network of the human brain. NeuroImage. 2014 11;102(P1):142–151.

    Not in our library10.1016/j.neuroimage.2013.09.069

36. 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. 2015 11;112(44):13681–13686.

    Not in our library10.1073/pnas.1502829112

37. 37.

    Bassett DS, Brown JA, Deshpande V, Carlson JM, Grafton ST. Conserved and variable architecture of human white matter connectivity. NeuroImage. 2011 1;54(2):1262–1279.

    Not in our library10.1016/j.neuroimage.2010.09.006

38. 38.

    Lecce F, Walsh V, Didino D, Cappelletti M. ’How many’ and’how much’ dissociate in the parietal lobe. Cortex. 2015;73:73–79.

    Not in our library10.1016/j.cortex.2015.08.007

39. 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.

    Not in our library10.1016/j.brs.2014.11.004

40. 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.

    Not in our library10.1016/j.bbr.2014.12.032

Cited by papers we hold 8

• Temporal sequences of brain activity at rest are constrained by white matter structure and modulated by cognitive demands · 2020
  No notice
• Multimodal network dynamics underpinning working memory · 2020
  No notice
• Awakening: Predicting external stimulation to force transitions between different brain states · 2019
  No notice
• Connectomics of bipolar disorder: a critical review, and evidence for dynamic instabilities within interoceptive networks · 2018
  Corrected
• Measuring behavior across scales · 2018
  No notice
• Developmental increases in white matter network controllability support a growing diversity of brain dynamics · 2017
  No notice
• Cliques and cavities in the human connectome · 2017
  No notice
• Optimally controlling the human connectome: the role of network topology · 2016
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.