Enhancing the Temporal Complexity of Distributed Brain Networks with Patterned Cerebellar Stimulation

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Farzan, Faranak ^a   Pascual Leone, Alvaro ^b   Schmahmann, Jeremy D ^c   Halko, Mark ^b  

^a UNIVERSITY OF TORONTO   (Canada)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATTENTION; BRAIN; BRAIN FUNCTION; CEREBELLUM; CEREBELLUM VERMIS; DEFAULT MODE NETWORK; ELECTROENCEPHALOGRAPHY; HUMAN; OSCILLATION; ADULT; BRAIN MAPPING; FEMALE; MALE; NERVE TRACT; PHYSIOLOGY; PROCEDURES; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

ADULT; BRAIN MAPPING; CEREBELLUM; ELECTROENCEPHALOGRAPHY; FEMALE; HUMANS; MALE; NEURAL PATHWAYS; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 84962263918     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep23599     Document Type: Article

References (60)

1. Bassett, D. S. & Gazzaniga, M. S. Understanding complexity in the human brain. Trends Cogn Sci 15, 200-209, doi: 10.1016/j. tics.2011.03.006 (2011).
2. McIntosh, A. R., Kovacevic, N. & Itier, R. J. Increased brain signal variability accompanies lower behavioral variability in development. PLoS Comput Biol 4, e1000106, doi: 10.1371/journal.pcbi.1000106 (2008).
3. McIntosh, A. R. et al. Spatiotemporal dependency of age-related changes in brain signal variability. Cereb Cortex 24, 1806-1817, doi: 10.1093/cercor/bht030 (2014).
4. Costa, M., Goldberger, A. L. & Peng, C. K. Multiscale entropy analysis of biological signals. Phys Rev E Stat Nonlin Soft Matter Phys 71, 021906 (2005).
5. Liang, W. K. et al. Revealing the brain's adaptability and the transcranial direct current stimulation facilitating effect in inhibitory control by multiscale entropy. NeuroImage 90, 218-234, doi: 10.1016/j.neuroimage.2013.12.048 (2014).
6. Allen, G., Buxton, R. B., Wong, E. C. & Courchesne, E. Attentional activation of the cerebellum independent of motor involvement. Science 275, 1940-1943 (1997).
7. Stoodley, C. J., Valera, E. M. & Schmahmann, J. D. Functional topography of the cerebellum for motor and cognitive tasks: An fMRI study. NeuroImage 59, 1560-1570, doi: 10.1016/j.neuroimage.2011.08.065 (2012).
8. Stoodley, C. J. & Schmahmann, J. D. Evidence for topographic organization in the cerebellum of motor control versus cognitive and affective processing. Cortex 46, 831-844, doi: 10.1016/j.cortex.2009.11.008 (2010).
9. Schmahmann, J. D. The role of the cerebellum in cognition and emotion: Personal reflections since 1982 on the dysmetria of thought hypothesis, and its historical evolution from theory to therapy. Neuropsychol Rev 20, 236-260, doi: 10.1007/s11065-010-9142-x (2010).
10. Schmahmann, J. D., Macmore, J. & Vangel, M. Cerebellar stroke without motor deficit: Clinical evidence for motor and non-motor domains within the human cerebellum. Neuroscience 162, 852-861, doi: 10.1016/j.neuroscience.2009.06.023 (2009).
11. Schmahmann, J. D. Disorders of the cerebellum: Ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. J Neuropsychiatry Clin Neurosci 16, 367-378, doi: 10.1176/appi.neuropsych.16.3.367 (2004).
12. Strick, P. L., Dum, R. P. & Fiez, J. A. Cerebellum and nonmotor function. Annu Rev Neurosci 32, 413-434, doi: 10.1146/annurev. neuro.31.060407.125606 (2009).
13. Schmahmann, J. D. An emerging concept. The cerebellar contribution to higher function. Arch Neurol 48, 1178-1187 (1991).
14. Ivry, R. B. & Keele, S. W. Timing functions of the cerebellum. J Cogn Neurosci 1, 136-152, doi: 10.1162/jocn.1989.1.2.136 (1989).
15. Keele, S. W. & Ivry, R. Does the cerebellum provide a common computation for diverse tasks? A timing hypothesis. Ann N Y Acad Sci 608, 179-207; discussion 207-111 (1990).
16. Jacobson, G. A., Rokni, D. & Yarom, Y. A model of the olivo-cerebellar system as a temporal pattern generator. Trends Neurosci 31, 617-625, doi: 10.1016/j.tins.2008.09.005 (2008).
17. Yarom, Y. & Cohen, D. The olivocerebellar system as a generator of temporal patterns. Ann N Y Acad Sci 978, 122-134 (2002).
18. Kuntalp, M. Computational model of an adaptive rhythm generator within the olivocerebellar system. Network 16, 55-84 (2005).
19. Middleton, F. A. & Strick, P. L. Cerebellar projections to the prefrontal cortex of the primate. J Neurosci 21, 700-712 (2001).
20. Schmahmann, J. D. & Pandya, D. N. Anatomic organization of the basilar pontine projections from prefrontal cortices in rhesus monkey. J Neurosci 17, 438-458 (1997).
21. Schmahmann, J. D. & Pandya, D. N. The cerebrocerebellar system. Int Rev Neurobiol 41, 31-60 (1997).
22. Buckner, R. L. The cerebellum and cognitive function: 25 years of insight from anatomy and neuroimaging. Neuron 80, 807-815, doi: 10.1016/j.neuron.2013.10.044 (2013).
23. Buckner, R. L., Krienen, F. M., Castellanos, A., Diaz, J. C. & Yeo, B. T. The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol 106, 2322-2345, doi: 10.1152/jn.00339.2011 (2011).
24. Marien, P., Engelborghs, S., Fabbro, F. & De Deyn, P. P. The lateralized linguistic cerebellum: A review and a new hypothesis. Brain and language 79, 580-600, doi: 10.1006/brln.2001.2569 (2001).
25. Koch, G. et al. Changes in intracortical circuits of the human motor cortex following theta burst stimulation of the lateral cerebellum. Clin Neurophysiol 119, 2559-2569, doi: 10.1016/j.clinph.2008.08.008 (2008).
26. Halko, M. A., Farzan, F., Eldaief, M. C., Schmahmann, J. D. & Pascual-Leone, A. Intermittent theta-burst stimulation of the lateral cerebellum increases functional connectivity of the default network. J Neurosci 34, 12049-12056, doi: 10.1523/JNEUROSCI.1776-14.2014 (2014).
27. Rossi, S., Hallett, M., Rossini, P. M. & Pascual-Leone, A. Screening questionnaire before TMS: An update. Clin Neurophysiol 122, 1686, doi: 10.1016/j.clinph.2010.12.037 (2011).
28. Huang, Y. Z., Edwards, M. J., Rounis, E., Bhatia, K. P. & Rothwell, J. C. Theta burst stimulation of the human motor cortex. Neuron 45, 201-206, doi: S0896627304008463 [pii] 10.1016/j.neuron.2004.12.033 [doi] (2005).
29. Rossini, P. M. et al. Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: Basic principles and procedures for routine clinical and research application. An updated report from an I.F.C.N. Committee. Clin Neurophysiol 126, 1071-1107, doi: 10.1016/j.clinph.2015.02.001 (2015).
30. Demirtas-Tatlidede, A. et al. Safety and proof of principle study of cerebellar vermal theta burst stimulation in refractory schizophrenia. Schizophr Res 124, 91-100, doi: 10.1016/j.schres.2010.08.015 (2010).
31. Raichle, M. E. et al. A default mode of brain function. Proc Natl Acad Sci USA 98, 676-682, doi: 10.1073/pnas.98.2.676 (2001).
32. Schmahmann, J. D., Doyon, J., Toga, A., Petrides, M. & Evans, A. In San Diego (ed Academic Press) (2000).
33. Delorme, A. & Makeig, S. EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134, 9-21 (2004).
34. Maris, E. & Oostenveld, R. Nonparametric statistical testing of EEG-and MEG-data. J Neurosci Methods 164, 177-190, doi: 10.1016/j.jneumeth.2007.03.024 (2007).
35. Zhou, D. et al. Effects of transcranial direct current stimulation (tDCS) on multiscale complexity of dual-task postural control in older adults. Exp Brain Res, doi: 10.1007/s00221-015-4310-0 (2015).
36. Misic, B., Mills, T., Taylor, M. J. & McIntosh, A. R. Brain noise is task dependent and region specific. J Neurophysiol 104, 2667-2676, doi: 10.1152/jn.00648.2010 (2010).
37. Mostofsky, S. H., Reiss, A. L., Lockhart, P. & Denckla, M. B. Evaluation of cerebellar size in attention-deficit hyperactivity disorder. J Child Neurol 13, 434-439 (1998).
38. Lim, L. et al. Disorder-specific grey matter deficits in attention deficit hyperactivity disorder relative to autism spectrum disorder. Psychol Med 45, 965-976, doi: 10.1017/S0033291714001974 (2015).
39. Dutta, A., McKie, S. & Deakin, J. F. Resting state networks in major depressive disorder. Psychiatry Res 224, 139-151, doi: 10.1016/j. pscychresns.2014.10.003 (2014).
40. Gardner, A. et al. Towards mapping the brain connectome in depression: Functional connectivity by perfusion SPECT. Psychiatry Res 223, 171-177, doi: 10.1016/j.pscychresns.2014.05.008 (2014).
41. Marien, P. et al. Consensus paper: Language and the cerebellum: An ongoing enigma. Cerebellum 13, 386-410, doi: 10.1007/s12311-013-0540-5 (2014).
42. Guell, X., Hoche, F. & Schmahmann, J. D. Metalinguistic deficits in patients with cerebellar dysfunction: Empirical support for the dysmetria of thought theory. Cerebellum 14, 50-58, doi: 10.1007/s12311-014-0630-z (2015).
43. Garrard, P., Martin, N. H., Giunti, P. & Cipolotti, L. Cognitive and social cognitive functioning in spinocerebellar ataxia : A preliminary characterization. J Neurol 255, 398-405, doi: 10.1007/s00415-008-0680-6 (2008).
44. Van Overwalle, F., Baetens, K., Marien, P. & Vandekerckhove, M. Cerebellar areas dedicated to social cognition? A comparison of meta-analytic and connectivity results. Soc Neurosci 10, 337-344, doi: 10.1080/17470919.2015.1005666 (2015).
45. Holmes, G. The cerebellum of man (Hughlings Jackson memorial lecture). Brain 62, 1-30 (1939).
46. Shimizu, H. et al. Therapeutic efficacy of transcranial magnetic stimulation for hereditary spinocerebellar degeneration. Tohoku J Exp Med 189, 203-211 (1999).
47. Schutter, D. J. & Van Honk, J. The cerebellum in emotion regulation: A repetitive transcranial magnetic stimulation study. Cerebellum 8, 28-34, doi: 10.1007/s12311-008-0056-6 (2009).
48. Farzan, F. et al. Cerebellar TMS in treatment of a patient with cerebellar ataxia: Evidence from clinical, biomechanics and neurophysiological assessments. Cerebellum 12, 707-712, doi: 10.1007/s12311-013-0485-8 (2013).
49. Pope, P. A. & Miall, R. C. Restoring cognitive functions using non-invasive brain stimulation techniques in patients with cerebellar disorders. Front Psychiatry 5, 33, doi: 10.3389/fpsyt.2014.00033 (2014).
50. Misic, B. et al. Coordinated Information Generation and Mental Flexibility: Large-Scale Network Disruption in Children with Autism. Cereb Cortex, doi: 10.1093/cercor/bhu082 (2014).
51. Mizuno, T. et al. Assessment of EEG dynamical complexity in Alzheimer's disease using multiscale entropy. Clin Neurophysiol 121, 1438-1446, doi: 10.1016/j.clinph.2010.03.025 (2010).
52. Tononi, G., Sporns, O. & Edelman, G. M. A measure for brain complexity: Relating functional segregation and integration in the nervous system. Proc Natl Acad Sci USA 91, 5033-5037 (1994).
53. Tononi, G., Edelman, G. M. & Sporns, O. Complexity and coherency: Integrating information in the brain. Trends Cogn Sci 2, 474-484 (1998).
54. Sporns, O., Tononi, G. & Edelman, G. M. Connectivity and complexity: The relationship between neuroanatomy and brain dynamics. Neural netw 13, 909-922 (2000).
55. McDonough, I. M. & Nashiro, K. Network complexity as a measure of information processing across resting-state networks: Evidence from the Human Connectome Project. Front Hum Neurosci 8, 409, doi: 10.3389/fnhum.2014.00409 (2014).
56. Buzsaki, G., Anastassiou, C. A. & Koch, C. The origin of extracellular fields and currents-EEG, ECoG, LFP and spikes. Nat Rev Neurosci 13, 407-420, doi: 10.1038/nrn3241 (2012).
57. Scheeringa, R. et al. Frontal theta EEG activity correlates negatively with the default mode network in resting state. Int J Psychophysiol 67, 242-251, doi: 10.1016/j.ijpsycho.2007.05.017 (2008).
58. Marstaller, L., Burianova, H. & Sowman, P. F. High gamma oscillations in medial temporal lobe during overt production of speech and gestures. PLOS One 9, e111473, doi: 10.1371/journal.pone.0111473 (2014).
59. Koch, G. Repetitive transcranial magnetic stimulation: A tool for human cerebellar plasticity. Funct Neurol 25, 159-163, doi: 4590 [pii] (2011).
60. Popa, T., Russo, M. & Meunier, S. Long-lasting inhibition of cerebellar output. Brain Stimul 3, 161-169, doi: 10.1016/j. brs.2009.10.001 (2010).