Phase-amplitude coupling supports phase coding in human ECoG

eLife

Volumn 4, Issue AUGUST2015, 2015, Pages

  Watrous, Andrew J ^a   Deuker, Lorena ^a,b   Fell, Juergen ^a   Axmacher, Nikolai ^c,d  

^a UNIVERSITY OF BONN   (Germany)

^b RADBOUD UNIVERSITY   (Netherlands)

^c GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^d RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; CLINICAL ARTICLE; DRUG RESISTANT EPILEPSY; ELECTROCORTICOGRAPHY; EXCITATION CONTRACTION COUPLING; FEMALE; FREQUENCY MODULATION; HIPPOCAMPUS; HUMAN; MALE; MICROELECTRODE; PHASE AMPLITUDE COUPLING; POSTSYNAPTIC POTENTIAL SUMMATION; STEREOTACTIC PROCEDURE; BRAIN; ELECTROENCEPHALOGRAM; PATHOPHYSIOLOGY; PHOTOSTIMULATION; PHYSIOLOGY;

BRAIN; BRAIN WAVES; DRUG RESISTANT EPILEPSY; ELECTROCORTICOGRAPHY; HUMANS; PHOTIC STIMULATION;

EID: 84943779814     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.07886     Document Type: Article

References (66)

1. Aru J, Aru J, Priesemann V, Wibral M, Lana L, Pipa G, Singer W, Vicente R. 2015. Untangling cross-frequency coupling in neuroscience. Current Opinion in Neurobiology 31:51–61. doi: 10.1016/j.conb.2014.08.002.
2. Axmacher N, Elger CE, Fell J. 2008. Ripples in the medial temporal lobe are relevant for human memory consolidation. Brain 131:1806–1817. doi: 10.1093/brain/awn103.
3. Axmacher N, Henseler MM, Jensen O, Weinreich I, Elger CE, Fell J. 2010. Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proceedings of the National Academy of Sciences of USA 107:3228–3233. doi: 10.1073/pnas.0911531107.
4. Belitski A, Gretton A, Magri C, Murayama Y, Montemurro MA, Logothetis NK, Panzeri S. 2008. Low-frequency local field potentials and spikes in primary visual cortex convey independent visual information. Journal of Neuroscience 28:5696–5709.
5. Belitski A, Panzeri S, Magri C, Logothetis N, Kayser C. 2010. Sensory information in local field potentials and spikes from visual and auditory cortices: time scales and frequency bands. Journal of Computational Neuroscience 29:533–545. doi: 10.1007/s10827-010-0230-y.
6. Berens P. 2009. Circstat: a matlab toolbox for circular statistics. Journal of Statistical Software 31.
7. Bragin A, Jando´ G, Nádasdy Z, Hetke J, Wise K, Buzsáki G. 1995. Gamma (40–100 Hz) oscillation in the hippocampus of the behaving rat. Journal of Neuroscience 15:47–60.
8. Burke JF, Ramayya AG, Kahana MJ. 2015. Human intracranial high-frequency activity during memory processing: neural oscillations or stochastic volatility. Current Opinion in Neurobiology 31:104–110. doi: 10.1016/j.conb.2014.09.003.
9. Buzsaki G. 2010. Neural syntax: cell assemblies, synapsembles, and readers. Neuron 68:362–385. doi: 10.1016/j.neuron.2010.09.023.
10. Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, Berger MS, Barbaro NM, Knight RT. 2006. High gamma power is phase-locked to theta oscillations in human neocortex. Science 313:1626–1628. doi: 10.1126/science.1128115.
11. Canolty RT, Knight RT. 2010. The functional role of cross-frequency coupling. Trends in Cognitive Sciences 14:506–515. doi: 10.1016/j.tics.2010.09.001.
12. Chan A, Baker J, Eskandar E, Schomer D, Ulbert I, Marinkovic K, Cash S, Halgren E. 2011. First-pass selectivity for semantic categories in human anteroventral temporal lobe. Journal of Neuroscience 31:18119–18129. doi: 10.1523/JNEUROSCI.3122-11.2011.
13. Cichy RM, Pantazis D, Oliva A. 2014. Resolving human object recognition in space and time. Nature Neuroscience 17:455–462. doi: 10.1038/nn.3635.
14. Cohen MX. 2014. Fluctuations in oscillation frequency control spike timing and coordinate neural networks. Journal of Neuroscience 34:8988–8998. doi: 10.1523/JNEUROSCI.0261-14.2014.
15. Crone NE, Miglioretti DL, Gordon B, Lesser RP. 1998. Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. Brain 121:2301–2315. doi: 10.1093/brain/121.12.2301.
16. Daitch AL, Sharma M, Roland JL, Astafiev SV, Bundy DT, Gaona CM, Snyder AZ, Shulman GL, Leuthardt EC, Corbetta M. 2013. Frequency-specific mechanism links human brain networks for spatial attention. Proceedings of the National Academy of Sciences of USA 110:19585–19590. doi: 10.1073/pnas.1307947110.
17. Delorme A, Makeig S. 2004. EEGLAB: an open source toolbox for analysis of single- trial EEG dynamics including independent component analysis. Journal of Neuroscience Methods 134:9–21. doi: 10.1016/j.jneumeth.2003.10.009.
18. Destexhe A, Hughes SW, Rudolph M, Crunelli V. 2007. Are corticothalamic ‘up’ states fragments of wakefulness? Trends in Neuroscience 30:334–342. doi: 10.1016/j.tins.2007.04.006.
19. Dvorak D, Fenton AA. 2014. Toward a proper estimation of phase-amplitude coupling in neural oscillations. Journal of Neuroscience Methods 225:42–56. doi: 10.1016/j.jneumeth.2014.01.002.
20. Ekstrom A, Viskontas I, Kahana M, Jacobs J, Upchurch K, Bookheimer S, Fried I. 2007. Contrasting roles of neural firing rate and local field potentials in human memory. Hippocampus 17:606–617. doi: 10.1002/hipo.20300.
21. Fell J, Ludowig E, Rosburg T, Axmacher N, Elger CE. 2008. Phase-locking within human mediotemporal lobe predicts memory formation. Neuroimage 43:410–419. doi: 10.1016/j.neuroimage.2008.07.021
22. Fontolan L, Morillon B, Liegeouis-Chauvel C, Giraud AL. 2014. The contribution of frequency-specific activity to hierarchical information processing in the human auditory cortex. Nature Communications 5:4694. doi: 10.1038/ncomms5694.
23. Freudenburg ZV, Gaona CM, Sharma M, Bundy DT, Breshears JD, Pless RB, Leuthardt EC. 2014. Fast-scale network dynamics in human cortex have specific spectral covariance patterns. Proceedings of the National Academy of Sciences of USA 111:4602–4607. doi: 10.1073/pnas.1311716111.
24. Friese U, Köster M, Hassler U, Martens U, Trujillo-Barreto N, Gruber T. 2013. Successful memory encoding is associated with increased cross-frequency coupling between frontal theta and posterior gamma oscillations in human scalp-recorded EEG. Neuroimage 66:642–647. doi: 10.1016/j.neuroimage.2012.11.002.
25. Jacobs J, Kahana M. 2009. Neural representations of individual stimuli in humans revealed by gamma-band electrocorticographic activity. Journal of Neuroscience 29:10203–10214. doi: 10.1523/JNEUROSCI.2187-09.2009.
26. Jacobs J, Kahana M, Ekstrom A, Fried I. 2007. Brain oscillations control timing of single-neuron activity in humans. Journal of Neuroscience 27:3839–3844. doi: 10.1523/JNEUROSCI.4636-06.2007.
27. Jacobs J, Lega B, Anderson C. 2012. Explaining how brain stimulation can evoke memories. Journal of Cognitive Neuroscience 24:553–563. doi: 10.1162/jocn_a_00170.
28. Jensen O, Gips B, Bergmann TO, Bonneford M. 2014. Temporal coding organized by coupled alpha and gamma oscillations prioritize visual processing. Trends in Neurosciences 37:357–369. doi: 10.1016/j.tins.2014.04.001.
29. Kayser C, Ince RA, Panzeri S. 2012. Analysis of slow (theta) oscillations as a potential temporal reference frame for information coding in sensory cortices. PLOS Computational Biology 8:e1002717. doi: 10.1371/journal.pcbi.1002717.
30. Kayser C, Montemurro M, Logothetis N, Panzeri S. 2009. Spike-phase coding boosts and stabilizes information carried by spatial and temporal spike patterns. Neuron 61:597–608. doi: 10.1016/j.neuron.2009.01.008.
31. Kendrick KM, Zhan Y, Fischer H, Nicol AU, Zhang X, Feng J. 2011. Learning alters theta amplitude, theta-gamma coupling and neuronal synchronization in inferotemporal cortex. BMC Neuroscience 12:55. doi: 10.1186/1471–2202-12–55.
32. Kopell N, Kramer MA, Malerba P, Whittington MA. 2010. Are different rhythms good for different functions? Frontiers in Human Neuroscience 4:1–9. doi: 10.3389/fnhum.2010.00187.
33. Kovatch CK, Tsuchiya N, Kawasaki H, Oya H, Howard MA, Adolphs R. 2011. Manifestation of ocular-muscle EMG contamination in human intracranial recordings. Neuroimage 54:213–233. doi: 10.1016/j.neuroimage.2010.08.002.
34. Kraskov A, Quiroga R, Reddy L, Fried I, Koch C. 2007. Local field potentials and spikes in the human medial temporal lobe are selective to image category. Journal of Cognitive Neuroscience 19:479–492. doi: 10.1162/jocn.2007.19.3.479.
35. Lakatos P, Shah AS, Knuth KH, Ulbert I, Karmos G, Schroeder CE. 2005. An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. Journal of Neurophysiology 94:1904–1911. doi: 10.1152/jn.00263.2005.
36. Lega B, Burke J, Jacobs J, Kahana MJ. 2014. Slow-theta-to-gamma phase-amplitude coupling in human hippocampus supports the formation of new episodic memories. Cerebral Cortex. doi: 10.1093/cercor/bhu232.
37. Lisman JE, Jensen O. 2013. The theta-gamma neural code. Neuron 77:1002–1016. doi: 10.1016/j.neuron.2013.03.007.
38. Lopour B, Tavassoli A, Fried I, Ringach D. 2013. Coding of information in the phase of local field potentials within human medial temporal lobe. Neuron 79:594–606. doi: 10.1016/j.neuron.2013.06.001.
39. Majima K, Matsuo T, Kawasaki K, Kawai K, Saito N, Hasegawa I, Kamitani Y. 2014. Decoding visual object categories from temporal correlations of ECoG signals. Neuroimage 90:74–83. doi: 10.1016/j.neuroimage.2013.12.020.
40. Manning JR, Jacobs J, Fried I, Kahana MJ. 2009. Broadband shifts in local field potential power spectra are correlated with single-neuron spiking in humans. Journal of Neuroscience 29:13613–13620. doi: 10.1523/JNEUROSCI.2041-09.2009.
41. Maris E, van Vugt M, Kahana M. 2011. Spatially distributed patterns of oscillatory coupling between highfrequency amplitudes and low-frequency phases in human iEEG. Neuroimage 54:836–850. doi: 10.1016/j.neuroimage.2010.09.029.
42. McGinn RJ, Valiante TA. 2014. Phase-amplitude coupling and interlaminar synchrony are correlated in human neocortex. The Journal of Neuroscience 34:15923–15930. doi: 10.1523/JNEUROSCI.2771-14.2014.
43. Mormann F, Kornblith S, Quiroga RQ, Kraskov A, Cerf M, Fried I, Koch C. 2008. Latency and selectivity of single neurons indicate hierarchical processing in the human medial temporal lobe. The Journal of Neuroscience 28:8865–8872. doi: 10.1523/JNEUROSCI.1640-08.2008.
44. Miller KJ, Honey CJ, Hermes D, Rao R, denNijs M, Ojemann JG. 2014. Broadband changes in the cortical surface potential track activation of functionally diverse neuronal populations. Neuroimage 85:711–720. doi: 10.1016/j.neuroimage.2013.08.070.
45. Ng B, Logothetis N, Kayser C. 2013. EEG phase patterns reflect the selectivity of neural firing. Cerebral Cortex 23:389–398. doi: 10.1093/cercor/bhs031.
46. O’Keefe J, Recce ML. 1993. Phase relationship between hippocampal place units and the EEG theta rhythm. Hippocampus 3:317–330. doi: 10.1002/hipo.450030307.
47. Ray S, Crone NE, Niebur PJ, Franaszczuk SS, Hsiao SS. 2008. Neural correlates of high-gamma oscillations (60–200 Hz) in macaque local field potentials and their potential implications in electrocorticography. Journal of Neuroscience 28:11526–11536. doi: 10.1523/JNEUROSCI.2848-08.2008.
48. Rey HG, Fried I, Quian Quiroga R. 2014. Timing of single-neuron and local field potential responses in the human medial temporal lobe. Current Biology 24:299–304. doi: 10.1016/j.cub.2013.12.004.
49. Rizzuto DS, Madsen JR, Bromfield EB, Schulze-Bonhage A, Kahana MJ. 2006. Human neocortical oscillations exhibit theta phase differences between encoding and retrieval. Neuroimage 31:1352–1358. doi: 10.1016/j.neuroimage.2006.01.009.
50. Rutishauser U, Ross I, Mamelak A, Schuman E. 2010. Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 464:903–907. doi: 10.1038/nature08860.
51. Schyns P, Thut G, Gross J. 2011. Cracking the code of oscillatory activity. PLOS Biology 9:e1001064. doi: 10.1371/journal.pbio.1001064.
52. Siegel M, Donner TH, Engel AK. 2012. Spectral fingerprints of large-scale neuronal interactions. Nature Reviews Neuroscience 13:121–134. doi: 10.1038/nrn3137.
53. Siegel M, Warden M, Miller E. 2009. Phase-dependent neuronal coding of objects in short-term memory. Proceedings of the National Academy of Sciences of USA 106:21341–21346. doi: 10.1073/pnas.0908193106.
54. Skaggs WE, McNaughton BL, Wilson MA, Barnes CA. 1996. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences. Hippocampus 6:149–172. doi: 10.1002/(SICI)1098-1063(1996)6:2<149::AID-HIPO6>3.0.CO;2-K.
55. Tort AB, Komorowski RW, Manns JR, Kopell NJ, Eichenbaum H. 2009. Theta-gamma coupling increases during the learning of item-context associations. Proceedings of the National Academy of Sciences of USA 106: 20942–20947. doi: 10.1073/pnas.0911331106.
56. van der Meij R, Kahana M, Maris E. 2012. Phase-amplitude coupling in human electrocorticography is spatially distributed and phase diverse. Journal of Neuroscience 32:111–123. doi: 10.1523/JNEUROSCI.4816-11.2012.
57. van Gerven M, Maris E, Sperling M, Sharan A, Litt B, Anderson C, Baltuch G, Jacobs J. 2013. Decoding the memorization of individual stimuli with direct human brain recordings. Neuroimage 70:223–232. doi: 10.1016/j.neuroimage.2012.12.059.
58. Voytek B, Kayser AS, Badre D, Fegen D, Chang EF, Crone NE, Parvizi J, Knight RT, D’Esposito M. 2015. Oscillatory dynamics coordinating human frontal networks in support of goal maintenance. Nature Neuroscience 18: 1318–1324. doi: 10.1038/nn.4071.
59. Watrous AJ, Ekstrom AD. 2014. The spectro-contextual encoding and retrieval theory of episodic memory. Frontiers in Human Neuroscience 8:75. doi: 10.3389/fnhum.2014.00075.
60. Watrous AJ, Fell J, Ekstrom AD, Axmacher N. 2015. More than spikes: common oscillatory mechanisms for content specific neural representations during perception and memory. Current Opinion in Neurobiology 31:33–39. doi: 10.1016/j.conb.2014.07.024.
61. Watrous AJ, Tandon N, Conner CR, Pieters T, Ekstrom AD. 2013. Frequency-specific network connectivity increases underlie accurate spatiotemporal memory retrieval. Nature Neuroscience 16:349–356. doi: 10.1038/nn.3315.
62. Whittingstall K, Logothetis NK. 2009. Frequency-band coupling in surface EEG reflects spiking activity in monkey visual cortex. Neuron 64:281–289. doi: 10.1016/j.neuron.2009.08.016.
63. Womelsdorf T, Valiante TA, Sahin NT, Miller KJ, Tiesinga P. 2014. Dynamic circuit motifs underlying rhythmic gain countrol, gating and integration. Nature Reviews Neuroscience 17:1031–1039. doi: 10.1038/nn.3764.
64. Yaffe RB, Kerr MS, Damera S, Sarma SV, Inati SK, Zaghloul KA. 2014. Reinstatement of distributed cortical oscillations occurs with precise spatiotemporal dynamics during successful memory retrieval. Proceedings of the National Academy of Science of USA 111:18727–18732. doi: 10.1073/pnas.1417017112.
65. Yuval-Greenberg S, Tomer O, Keren AS, Nelken I, Deouell LY. 2008. Transient induced gamma-band responses in EEG as a manifestation of miniature saccades. Neuron 58:429–441. doi: 10.1016/j.neuron.2008.03.027.
66. Zhang H, Fell J, Staresina BP, Weber B, Elger CE, Axmacher N. 2015. Gamma power reductions accompany stimulus-specific representations of dynamic events. Current Biology 25:635–640.