Shaping intrinsic neural oscillations with periodic stimulation

Journal of Neuroscience

Volumn 36, Issue 19, 2016, Pages 5328-5337

  Herrmann, Christoph S ^a   Murray, Micah M ^b,c   Ionta, Silvio ^b,d   Hutt, Axel ^e   Lefebvre, Jérémie ^b,f,g  

^a UNIVERSITY OF OLDENBURG   (Germany)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c University of Lausanne   (Switzerland)

^d ETH ZURICH   (Switzerland)

^e DEUTSCHER WETTERDIENST   (Germany)

^f UNIVERSITY HEALTH NETWORK   (Canada)

^g UNIVERSITY OF TORONTO   (Canada)

Author keywords

Dynamics; Networks; Oscillations; Spectrum; Stimulation; Synchrony

Indexed keywords

ARTICLE; CONNECTOME; CORTICAL SYNCHRONIZATION; ELECTRONEUROLOGY; INTRINSIC NEURAL OSCILLATION; MATHEMATICAL MODEL; NERVE CELL NETWORK; NERVE CELL STIMULATION; OSCILLATION; OSCILLATORY POTENTIAL; PERIODICITY; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; SPECTROSCOPY; SPIKE; TRANSCRANIAL MAGNETIC STIMULATION; ACTION POTENTIAL; BIOLOGICAL MODEL; BRAIN; CYTOLOGY; ELECTROENCEPHALOGRAPHY; ELECTROSTIMULATION; HUMAN; NERVE CELL; PHYSIOLOGY; SYNAPTIC POTENTIAL;

ACTION POTENTIALS; BRAIN; ELECTRIC STIMULATION; ELECTROENCEPHALOGRAPHY; HUMANS; MODELS, NEUROLOGICAL; NEURONS; PERIODICITY; SYNAPTIC POTENTIALS;

EID: 84966671613     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0236-16.2016     Document Type: Article

References (58)

1. Alagapan S, Schmidt SL, Lefebvre J, Hadar E, Shin HW, Fröhlich F (2016) Modulation of cortical oscillations by low-frequency direct cortical stimulation is state-dependent. PLoS Biol 14:e1002424. CrossRef Medline
2. Ali MM, Sellers KK, Fröhlich F (2013) Transcranial alternating current stimulation modulates large-scale cortical network activity by network resonance. J Neurosci 33: 11262-11275. CrossRef Medline
3. Amari S (1977) Dynamics of pattern formation in lateral inhibition type neural fields. Biol Cybern 27: 77-87. CrossRef Medline
4. Başar E (2012) A review of alpha activity in integrative brain function: fundamental physiology, sensory coding, cognition and pathology. Int J Psychophysiol 86: 1-24. CrossRef Medline
5. Başar E, Güntekin B (2012) A short review of alpha activity in cognitive processes and in cognitive impairment. Int J Psychophysiol 86: 25-38. CrossRef Medline
6. Brunel N (2000) Dynamics of sparsely connected networks of excitatory and inhibitory spiking neurons. J Comput Neurosci 8: 183-208.
7. Buzsáki G, Wang XJ (2012) Mechanisms of gamma oscillations. Annu Rev Neurosci 35: 203-225. CrossRef Medline
8. Cecere R, Rees G, Romei V (2015) Individual differences in alpha frequency drive crossmodal illusory perception. Curr Biol 25: 231-235. CrossRef Medline
9. Chanes L, Quentin R, Tallon-Baudry C, Valero-Cabré A (2013) Causal frequency-specific contributions of frontal spatiotemporal patterns induced by non-invasive neurostimulation to human visual performance. J Neurosci 33: 5000-5005. CrossRef Medline
10. de la Rocha J, Doiron B, Shea-Brown E, Josic K, Reyes A (2007) Correlation between neural spike trains increases with firing rate. Nature 448: 802-806. CrossRef
11. Dreyer AM, Herrmann CS (2015) Frequency-modulated steady-state visual evoked potentials: a new stimulation method for brain-computer interfaces. J Neurosci Methods 241: 1-9. CrossRef Medline
12. Engel AK, Singer W (2001) Temporal binding and the neural correlates of sensory awareness. Trends Cogn Sci 5: 16-25. CrossRef Medline
13. Engel AK, Fries P, Singer W (2001) Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci 2: 704-716. CrossRef Medline
14. Fröhlich F (2015) Experiments and models of cortical oscillations as a target for non-invasive brain stimulation. Prog Brain Res 222: 41-73. CrossRef Medline
15. Fröhlich F, McCormick DA (2010) Endogenous electric fields may guide neocortical network activity. Neuron 67: 129-143. CrossRef Medline
16. Gabbianni A, Koch C (1998) Principles of spike train analysis. In: Methods in neuronal modeling, pp 313-360. Cambridge, MA: MIT.
17. Gutmann B, Mierau A, Hülsdünker T, Hildebrand C, Przyklenk A, Hollmann W, Strüder HK (2015) Effects of physical exercise on individual resting state EEG alpha peak frequency. Neural Plast 2015:717312. CrossRef Medline
18. Haegens S, Cousijn H, Wallis G, Harrison PJ, Nobre AC (2014) Inter-and intra-individual variability in alpha peak frequency. Neuroimage 92: 46-55. CrossRef Medline
19. Helfrich RF, Schneider TR, Rach S, Trautmann-Lengsfeld SA, Engel AK, Herrmann CS (2014) Entrainment of brain oscillations by transcranial alternating current stimulation. Curr Biol 24: 333-339. CrossRef Medline
20. Hellwig B (2000) A quantitative analysis of the local connectivity between pyramidal neurons in layers 2/3 of the rat visual cortex. Biol Cybern 82: 111-121. CrossRef Medline
21. Henry MJ, Herrmann B, Obleser J (2014) Entrained neural oscillations in multiple frequency bands comodulate behavior. Proc Natl Acad SciU S A 111: 14935-14940. CrossRef Medline
22. Herrmann CS (2001) Human EEG responses to 1-100 Hz flicker: resonance phenomena in visual cortex and their potential correlation to cognitive phenomena. Exp Brain Res 137: 346-353. CrossRef Medline
23. Huerta PT, Volpe BT (2009) Transcranial magnetic stimulation, synaptic plasticity and network oscillations. J Neuroeng Rehabil 6: 7. CrossRef Medline
24. Hülsdünker T, Mierau A, Strüder HK (2015) Higher balance task demands are associated with an increase in individual alpha peak frequency. Front Hum Neurosci 9: 695. CrossRef Medline
25. Hutt A, Buhry L (2014) Study of GABAergic extra-synaptic tonic inhibition in single neurons and neural populations by traversing neural scales: application to propofol-induced anaesthesia. J Comput Neurosci 37: 417-437. CrossRef Medline
26. Hutt A, Bestehorn M, Wennekers T (2003) Pattern formation in intracortical neuronal fields. Network 14: 351-368. CrossRef Medline
27. Jadi MP, Sejnowski TJ (2014) Cortical oscillations arise from contextual interactions that regulate sparse coding. Proc Natl Acad Sci U S A 111: 6780-6785. CrossRef Medline
28. Jensen MH, Bak P, Bohr T (1983) Complete devil's staircase, fractal dimension and universality of mode-locking structure in the circle map. Phys Rev Lett 50: 1637-1639. CrossRef
29. Kajikawa Y, Schroeder CE (2015) Generation of field potentials and modulation of their dynamics through volume integration of cortical activity. J Neurophysiol 113: 339-351. CrossRef Medline
30. Klimesch W (1999) EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis. Brain Res Rev 29: 169-195. CrossRef Medline
31. Koch C (1999) Biophysics of computation. Oxford: OUP.
32. Lakatos P, Karmos G, Mehta AD, Ulbert I, Schroeder CE (2008) Entrainment of neuronal oscillations as a mechanism of attentional selection. Science 320: 110-113. CrossRef Medline
33. Lefebvre J, Hutt A (2013) Additive noise quenches delay-induced oscillations. Europhys Lett 102:60003.
34. Lefebvre J, Longtin A, LeBlanc VG (2011) Neural adaptation facilitates oscillatory responses to static inputs in a recurrent network of ON and OFF cells. J Comput Neurosci 31: 73-86. CrossRef Medline
35. Lefebvre J, Hutt A, Knebel JF, Whittingstall K, MurrayMM (2015) Stimulus statistics shape oscillations in nonlinear recurrent neural networks. J Neurosci 35: 2895-2903. CrossRef Medline
36. Lindén H, Pettersen KH, Einevoll GT (2010) Intrinsic dendritic filtering gives low-pass power spectra of local field potentials. J Comput Neurosci 29: 423-444. CrossRef Medline
37. Lorincz ML, Kékesi KA, Juhász G, Crunelli V, Hughes SW (2009) Temporal framing of thalamic relay-mode firing by phasic inhibition during the alpha rhythm. Neuron 63: 683-696. CrossRef Medline
38. Mazzoni A, Lindén H, Cuntz H, Lansner A, Panzeri S, Einevoll GT (2015) Computing the local field potential (LFP) from integrate-and-fire network models. PLoS Comput Biol 11:e1004584. CrossRef Medline
39. Neuling T, Rach S, Herrmann CS (2013) Orchestrating neuronal networks: sustained after-effects of transcranial alternating current stimulation depend upon brain states. Front Hum Neurosci 7: 161. CrossRef Medline
40. Notbohm A, Kurths J, Herrmann CS (2016) Modification of brain oscillations via rhythmic light stimulation provides evidence for entrainment but not for superposition of event-related responses. Front Hum Neurosci 10: 10. CrossRef Medline
41. Podvalny E, Noy N, Harel M, Bickel S, Chechik G, Schroeder CE, Mehta AD, Tsodyks M, Malach R (2015) A unifying principle underlying the extracellular field potential spectral responses in the human cortex. J Neurophysiol 114: 505-519. CrossRef Medline
42. Prescott SA, Sejnowski TJ (2008) Spike-rate coding and spike-time coding are affected oppositely by different adaptation mechanisms. J Neurosci 28: 13649-13661. CrossRef Medline
43. Press WH, Teukolsky SA, Vetterling WT, Flannery BP (2007) Numerical recipes: the art of scientific computing, Ed 3. Cambridge: Cambridge University.
44. Reato D, Rahman A, Bikson M, Parra LC (2010) Low-intensity electrical stimulation affects network dynamics by modulating population rate and spike timing. J Neurosci 30: 15067-15079. CrossRef Medline
45. Roberts JA, Robinson PA (2012) Quantitative theory of driven nonlinear brain dynamics. Neuroimage 62: 1947-1955. CrossRef Medline
46. Romei V, Driver J, Schyns PG, Thut G (2011) Rhythmic TMS over Parietal cortex links distinct brain frequencies to global versus local visual processing. Curr Biol 21: 334-337. CrossRef Medline
47. Samaha J, Postle BR (2015) The speed of alpha-band oscillations predicts the temporal resolution of visual perception. Curr Biol 25: 2985-2990. CrossRef Medline
48. Samaha J, Bauer P, Cimaroli S, Postle BR (2015) Top-down control of the phase of alpha-band oscillations as a mechanism for temporal prediction. Proc Natl Acad Sci U S A 112: 8439-8444. CrossRef Medline
49. Siegel M, Donner TH, Engel AK (2012) Spectral fingerprints of large-scale neuronal interactions. Nat Rev Neurosci 13: 121-134. CrossRef
50. Singer W, GrayCM (1995) Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18: 555-586. CrossRef Medline
51. Strüber D, Rach S, Neuling T, Herrmann CS (2015) On the possible role of stimulation duration for after-effects of transcranial alternating current stimulation. Front Cell Neurosci 9: 311. CrossRef Medline
52. Thut G, Schyns PG, Gross J (2011) Entrainment of perceptually relevant brain oscillations by non-invasive rhythmic stimulation of the human brain. Front Psychol 2: 170. CrossRef Medline
53. Thut G, Miniussi C, Gross J (2012) The functional importance of rhythmic activity in the brain. Curr Biol 22:R658-R663. CrossRef Medline
54. Varela F, Lachaux J-P, Rodriguez E, Martinerie J. The brainweb: phase synchronization and large-scale integration. Nat Rev Neurosci 2:229-239.
55. Vlahou EL, Thurm F, Kolassa IT, SchleeW (2014) Resting-state slow-wave power, healthy aging and cognitive performance. Sci Rep 4: 5101. CrossRef Medline
56. Wang XJ, Buzsáki G (1996) Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J Neurosci 16: 6402-6413. Medline
57. Whittington MA, Traub RD, Jefferys JG (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373: 612-615. CrossRef Medline
58. Witkowski M, Garcia-Cossio E, Chander BS, Braun C, Birbaumer N, Robinson SE, Soekadar SR (2015) Mapping entrained brain oscillations during transcranial alternating current stimulation (tACS). Neuro Image CrossRef