Slow EEG rhythms and inter-hemispheric synchronization across sleep and wakefulness in the human hippocampus

NeuroImage

Volumn 60, Issue 1, 2012, Pages 497-504

  Moroni, Fabio ^a,b   Nobili, Lino ^c,d   De Carli, Fabrizio ^d   Massimini, Marcello ^e   Francione, Stefano ^c   Marzano, Cristina ^a   Proserpio, Paola ^c   Cipolli, Carlo ^b   De Gennaro, Luigi ^a   Ferrara, Michele ^f  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF BOLOGNA   (Italy)

^c OSPEDALE NIGUARDA CA GRANDA   (Italy)

^d CNR   (Italy)

^e UNIVERSITY OF MILAN   (Italy)

^f UNIVERSITY OF L'AQUILA   (Italy)

Author keywords

Consolidation; Delta waves; Memory; Oscillation; Sleep function; Synchronization

Indexed keywords

ANTICONVULSIVE AGENT;

ADULT; ARTICLE; BRAIN DEPTH RECORDING; CASE REPORT; CORTICAL SYNCHRONIZATION; DELTA RHYTHM; FOCAL EPILEPSY; HIPPOCAMPUS; HUMAN; INTERHEMISPHERIC TRANSFER; LEFT HEMISPHERE; MALE; MEMORY CONSOLIDATION; NEUROIMAGING; NIGHT SLEEP; NONREM SLEEP; NUCLEAR MAGNETIC RESONANCE IMAGING; OSCILLATION; POWER SPECTRUM; PRIORITY JOURNAL; REM SLEEP; RIGHT HEMISPHERE; SLEEP PATTERN; SLEEP WAKING CYCLE; SLOW BRAIN WAVE; SLOW WAVE SLEEP; WAKEFULNESS;

ADULT; ELECTROENCEPHALOGRAPHY; ELECTROENCEPHALOGRAPHY PHASE SYNCHRONIZATION; HIPPOCAMPUS; HUMANS; MALE; SLEEP; WAKEFULNESS; YOUNG ADULT;

EID: 84856105927     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.11.093     Document Type: Article

References (74)

1. Achermann P., Borbély A.A. Temporal evolution of coherence and power in the human sleep electroencephalogram. J. Sleep Res. 1998, 7:36-41.
2. Arnolds D.E., Lopes da Silva F.H., Aitink J.W., Kamp A., Boeijinga P. The spectral properties of hippocampal EEG related to behaviour in man. Electroencephalogr. Clin. Neurophysiol. 1980, 50:324-328.
3. Arzy S., Allali G., Brunet D., Michel C.M., Kaplan P.W., Seeck M. Antiepileptic drugs modify power of high EEG frequencies and their neural generators. Eur. J. Neurol. 2010, 17:1308-1312.
4. Axmacher N., Mormann F., Fernández G., Elger C.E., Fell J. Memory formation by neuronal synchronization. Brain Res. Rev. 2006, 52:170-182.
5. Babiloni C., Vecchio F., Mirabella G., Buttiglione M., Sebastiano F., Picardi A., Di Gennaro G., Quarato P.P., Grammaldo L.G., Buffo P., Esposito V., Manfredi M., Cantore G., Eusebi F. Hippocampal, amygdala, and neocortical synchronization of theta rhythms is related to an immediate recall during Rey auditory verbal learning test. Hum. Brain Mapp. 2009, 30:2077-2089.
6. Besser R., Hornung K., Theisohn M., Rothacher G., Kramer G. EEG changes in patients during the introduction of carbamazepine. Electroencephalogr. Clin. Neurophysiol. 1992, 83:19-23.
7. Bland B.H. The physiology and pharmacology of hippocampal formation theta rhythms. Prog. Neurobiol. 1986, 26:1-54.
8. Bódizs R., Kantor S., Szabo G., Szucs A., Eross L., Halász P. Rhythmic hippocampal slow oscillation characterizes REM sleep in humans. Hippocampus 2001, 11:747-753.
9. Born J., Rasch B., Gais S. Sleep to remember. Neuroscientist 2006, 12:410-424.
10. Brazier M.A. Studies of the EEG activity of limbic structures in man. Electroencephalogr. Clin. Neurophysiol. 1968, 25:309-318.
11. Buzsáki G. Hippocampal sharp waves: their origin and significance. Brain Res. 1986, 398:242-252.
12. Buzsáki G. Two-stage model of memory trace formation: a role for "noisy" brain states. Neuroscience 1989, 31:551-570.
13. Buzsáki G. Memory consolidation during sleep: a neurophysiological perspective. J. Sleep Res. 1998, 7:17-23.
14. Buzsáki G. Theta oscillations in the hippocampus. Neuron 2002, 33:325-340.
15. Buzsáki G. Rhythms of the Brain 2006, Oxford University Press, New York.
16. Buzsáki G., Czopf J., Kondakor I., Kellenyi L. Laminar distribution of hippocampal rhythmic slow activity (RSA) in the behaving rat: current source density analysis, effects of urethane and atropine. Brain Res. 1986, 365:125-137.
17. Cantero J.L., Atienza M., Stickgold R., Kahana M.J., Madsen J.R., Kocsis B. Sleep-dependent theta oscillations in the human hippocampus and neocortex. J. Neurosci. 2003, 23:10897-10903.
18. Caplan J.B., Glaholt M.G. The roles of EEG oscillations in learning relational information. NeuroImage 2007, 38:604-616.
19. Caplan J.B., Madsen J.R., Raghavachari S., Kahana M.J. Distinct patterns of brain oscillations underlie two basic parameters of human maze learning. J. Neurophysiol. 2001, 86:368-380.
20. Caplan J.B., Madsen J.R., Schulze-Bonhage A., Aschenbrenner-Scheibe R., Newman E.L., Kahana M.J. Human theta oscillations related to sensorimotor integration and spatial learning. J. Neurosci. 2003, 23:4726-4736.
21. Carr M.F., Jadhav S.P., Frank L.M. Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval. Nat. Neurosci. 2011, 14:147-153.
22. Clemens Z., Mölle M., Eross L., Barsi P., Halász P., Born J. Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain 2007, 130:2868-2878.
23. Clemens Z., Weiss B., Szucs A., Eross L., Rásonyi G., Halász P. Phase coupling between rhythmic slow activity and gamma characterizes mesiotemporal rapid-eye-movement sleep in humans. Neuroscience 2009, 163:388-396.
24. Clemens Z., Mölle M., Eross L., Jakus R., Rásonyi G., Halász P., Born J. Fine-tuned coupling between human parahippocampal ripples and sleep spindles. Eur. J. Neurosci. 2011, 33:511-520.
25. Cossu M., Cardinale F., Colombo N., Mai R., Nobili L., Sartori I., Lo Russo G. Stereoelectroencephalography in the presurgical evaluation of children with drug-resistant focal epilepsy. J. Neurosurg. 2005, 103:333-343.
26. Diekelmann S., Born J. The memory function of sleep. Nat. Rev. Neurosci. 2010, 11:114-126.
27. Duncan J.S., Smith S.J., Forster A. Effects of the removal of phenytoin, carbamazepine and vaplroate on the encephalogram. Epilepsia 1989, 30:590-596.
28. Eichenbaum H. Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 2004, 44:109-120.
29. Ekstrom A.D., Caplan J.B., Ho E., Shattuck K., Fried I., Kahana M.J. Human hippocampal theta activity during virtual navigation. Hippocampus 2005, 15:881-889.
30. Fell J., Axmacher N. The role of phase synchronization in memory processes. Nat. Rev. Neurosci. 2011, 12:105-118.
31. Fell J., Klaver P., Lehnertz K., Grunwald T., Schaller C., Elger C.E., Fernández G. Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nat. Neurosci. 2001, 4:1259-1264.
32. Fell J., Klaver P., Elfadil H., Schaller C., Elger C.E., Fernández G. Rhinal hippocampal theta coherence during declarative memory formation: interaction with gamma synchronization?. Eur. J. Neurosci. 2003, 17:1082-1088.
33. Fell J., Fernández G., Klaver P., Axmacher N., Mormann F., Haupt S., Elger C.E. Rhinal-hippocampal coupling during declarative memory formation: dependence on item characteristics. Neurosci. Lett. 2006, 407:37-41.
34. Gais S., Born J. Declarative memory consolidation: mechanisms acting during human sleep. Learn. Mem. 2004, 11:679-685.
35. Gais S., Plihal W., Wagner U., Born J. Early sleep triggers memory for early visual discrimination skills. Nat. Neurosci. 2000, 3:1335-1339.
36. Giuditta A., Ambrosini M.V., Montagnese P., Mandale P., Cotugno M., Grassi Zucconi G., Vescia S. The sequential hypothesis of the function of sleep. Behav. Brain Res. 1995, 69:157-166.
37. Green J.D., Arduini A.A. Hippocampal electrical activity in arousal. J. Neurophysiol. 1954, 17:533-557.
38. Jacobs J., Kahana M.J., Ekstrom A.D., Fried I. Brain oscillations control timing of single-neuron activity in humans. J. Neurosci. 2007, 27:3839-3844.
39. Kahana M.J., Sekuler R., Caplan J.B., Kirschen M., Madsen J.R. Human theta oscillations exhibit task dependence during virtual maze navigation. Nature 1999, 399:781-784.
40. Le Van Quyen M., Staba R., Bragin A., Dickson C., Valderrama M., Fried I., Engel J. Large-scale microelectrode recordings of high-frequency gamma oscillations in human cortex during sleep. J. Neurosci. 2010, 30:7770-7782.
41. Lee A.K., Wilson M.A. Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 2002, 36:1183-1194.
42. Lega B.C., Jacobs J., Kahana M. Human hippocampal theta oscillations and the formation of episodic memories. Hippocampus 2011, 10.1002/hipo.20937.
43. Louie K., Wilson M.A. Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 2001, 29:145-156.
44. Malow B.A., Carney P.R., Kushwaha R., Bowes R.J. Hippocampal sleep spindles revisited: physiologic or epileptic activity?. Clin. Neurophysiol. 1999, 110:687-693.
45. Marciani M.G., Spanedda F., Mattia D. Neurophysiologic and neuropsychologic profiles of lamotrigine in epilepsy. Clin. Neuropharmacol. 1999, 22:159-163.
46. Marzano C., Ferrara M., Mauro F., Moroni F., Gorgoni M., Tempesta D., Cipolli C., De Gennaro L. Recalling and forgetting dreams: theta and alpha oscillations during sleep predict subsequent dream recall. J. Neurosci. 2011, 31:6674-6683.
47. Massimini M., Huber R., Ferrarelli F., Hill S., Tononi G. The sleep slow oscillation as a traveling wave. J. Neurosci. 2004, 24:6862-6870.
48. Meador K.J., Loring D.W., Abney O.L., Allen M.E., Moore E.E., Zamrini E.Y., King D.W. Effects of carbamazepine and phenytoin on EEG and memory in healthy adults. Epilepsia 1993, 34:153-157.
49. Mecarelli O., Piacenti A., Pultino P., Vicenzini E., Rizzo C., Rinalduzzi S., de Feo M.R., Accornero N. Clinical and electroencephalographic effects of topiramate in patients with epilepsy and healthy volunteers. Clin. Neuropharmacol. 2001, 5:284-289.
50. Mölle M., Marshall L., Gais S., Born J. Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep. J. Neurosci. 2002, 22:10941-10947.
51. Mölle M., Yeshenko O., Marshall L., Sara S.J., Born J. Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep. J. Neurophysiol. 2006, 96:62-70.
52. Montplaisir J., Leduc L., Laverdière M., Walsh J., Saint-Hilaire J.M. Sleep spindles in the human hippocampus: normal or epileptic activity?. Sleep 1981, 4:423-428.
53. Mormann F., Osterhage H., Andrzejak R.G., Weber B., Fernández G., Fell J., Elger C.E., Lehnertz K. Independent delta/theta rhythms in the human hippocampus and entorhinal cortex. Front. Hum. Neurosci. 2008, 2:3.
54. Moroni F., Nobili L., Curcio G., De Carli F., Fratello F., Marzano C., De Gennaro L., Ferrillo F., Cossu M., Francione S., Lo Russo G., Bertini M., Ferrara M. Sleep in the human hippocampus: a stereo-EEG study. PLoS One 2007, 2:e867.
55. Moroni F., Nobili L., Curcio G., De Carli F., Tempesta D., Marzano C., De Gennaro L., Mai R., Francione S., Lo Russo G., Ferrara M. Procedural learning and sleep hippocampal low frequencies in humans. NeuroImage 2008, 42:911-918.
56. Neufeld M.Y., Kogan E., Chistik V., Korczyn A.D. Comparison of the effects of vigabatrin, lamotrigine and topiramate on quantitative EEGs in patients with epilepsy. Clin. Neuropharmacol. 1999, 22:80-86.
57. Niedermeyer E., Lopes da Silva F. Electroencephalography of the Walking Adult 1999, Lippincott Williams and Wilkins, Philadelphia.
58. Nir Y., Mukamel R., Dinstein I., Privman E., Harel M., Fisch L., Gelbard-Sagiv H., Kipervasser S., Andelman F., Neufeld M.Y., Kramer U., Arieli A., Fried I., Malach R. Interhemispheric correlations of slow spontaneous neuronal fluctuations revealed in human sensory cortex. Nat. Neurosci. 2008, 11:1100-1108.
59. Picchioni D., Horovitz S.G., Fukunaga M., Carr W.S., Meltzer J.A., Balkin T.J., Duyn J.H., Braun A.R. Infraslow EEG oscillations organize large scale cortical-subcortical interactions during sleep: a combined EEG/fMRI study. Brain Res. 2011, 1374:63-72.
60. Placidi F., Tombini M., Romigi A., Bianchi L., Izzi F., Sperli F., Mattia D., Cervellino A., Marciani M.G. Topiramate: effect on EEG interictal abnormalities and background activity in patients affected by focal epilepsy. Epilepsy Res. 2004, 58:43-52.
61. Raghavachari S., Kahana M.J., Rizzato D.S., Caplan J.B., Kirschen M.P., Bourgeois B., Madsen J.R., Lisman J.E. Gating of human theta oscillations by a working memory task. J. Neurosci. 2001, 21:3175-3183.
62. Rechtschaffen A., Kales A. A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects. NIH Publication No. 204, US Government Printing Office 1968, Public Health Service, Washington DC.
63. Rutishauser U., Ross I.B., Mamelak A.N., Schuman E.M. Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 2010, 464:903-907.
64. Sederberg P.B., Kahana M.J., Howard M.W., Donner E.J., Madsen J.R. Theta and gamma oscillations during encoding predict subsequent recall. J. Neurosci. 2003, 23:10809-10814.
65. Skaggs W.E., McNaughton B.L. Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science 1996, 271:1870-1873.
66. Tononi G., Girelli C. Sleep function and synaptic homeostasis. Sleep Med. Rev. 2006, 10:49-62.
67. Vanderwolf C.H. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr. Clin. Neurophysiol. 1969, 26:407-418.
68. Veauthier J., Haettig H., Meencke H.J. Impact of levetiracetam add-on therapy on different EEG occipital frequencies in epileptic patients. Seizure 2009, 18:392-395.
69. Wagner T., Axmacher N., Lehnertz K., Elger C.E., Fell J. Sleep-dependent directional coupling between human neocortex and hippocampus. Cortex 2010, 46:56-63.
70. Watrous A.J., Fried I., Ekstrom A.D. Behavioral correlates of human hippocampal delta and theta oscillations during navigation. J. Neurophysiol. 2011, 105:1747-1755.
71. Weiss S., Rappelsberger P. Long-range EEG synchronization during word encoding correlates with successful memory performance. Cogn. Brain Res. 2000, 2000(9):299-312.
72. Whitten T.A., Hughes A.M., Dickson C.T., Caplan J.B. A better oscillation detection method robustly extracts EEG rhythms across brain state changes: the human alpha rhythm as a test case. NeuroImage 2011, 54:860-874.
73. Wilson M.A., McNaughton B.L. Reactivation of hippocampal ensemble memories during sleep. Science 1994, 265:676-679.
74. Zaveri H.P., Duckrow R.B., de Lanerolle N.C., Spencer S.S. Distinguishing subtypes of temporal lobe epilepsy with background hippocampal activity. Epilepsia 2001, 42:725-730.