Fine-tuned coupling between human parahippocampal ripples and sleep spindles

European Journal of Neuroscience

Volumn 33, Issue 3, 2011, Pages 511-520

  Clemens, Zsófia ^a   Mölle, Matthias ^b   Eross, Loránd ^a   Jakus, Rita ^a   Rásonyi, György ^a   Halász, Péter ^c   Born, Jan ^b,d  

^a NATIONAL INSTITUTE OF NEUROSURGERY   (Hungary)

^b UNIVERSITY OF LÜBECK   (Germany)

^c PÁZMÁNY PÉTER CATHOLIC UNIVERSITY   (Hungary)

^d UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Epilepsy; Hippocampus; Ripples; Sleep; Spindles

Indexed keywords

ADULT; ARTICLE; CELL POLARITY; CLINICAL ARTICLE; CONTROLLED STUDY; ELECTRIC POTENTIAL; ELECTRODE; ELECTROENCEPHALOGRAM; FEMALE; FRONTAL CORTEX; HIPPOCAMPUS; HUMAN; MALE; MEMORY CONSOLIDATION; NEOCORTEX; NONREM SLEEP; OSCILLATION; PARIETAL CORTEX; PRIORITY JOURNAL; REM SLEEP; SEIZURE; SLEEP SPINDLE; SLOW WAVE SLEEP; TEMPORAL LOBE EPILEPSY;

ADULT; ELECTROENCEPHALOGRAPHY; EPILEPSY; HIPPOCAMPUS; HUMANS; MEMORY; MIDDLE AGED; NEOCORTEX; SLEEP;

EID: 79251564916     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07505.x     Document Type: Article

References (49)

1. Abeles, M. (1982) Quantification, smoothing, and confidence limits for single-units' histograms. J. Neurosci. Methods, 5, 317-325.
2. Asano, E., Mihaylova, T., Juhász, C., Sood, S. & Chugani, H.T. (2007) Effect of sleep on interictal spikes and distribution of sleep spindles on electrocorticography in children with focal epilepsy. Clin. Neurophysiol., 118, 1360-1368.
3. Axmacher, N., Elger, C.E. & Fell, J. (2008) Ripples in the medial temporal lobe are relevant for human memory consolidation. Brain, 131, 1806-1817.
4. Bragin, A., Engel, J. Jr, Wilson, C.L., Fried, I. & Buzsaki, G. (1999a) High-frequency oscillations in human brain. Hippocampus, 9, 137-142.
5. Bragin, A., Engel, J. Jr, Wilson, C.L., Fried, I. & Mathern, G.W. (1999b) Hippocampal and entorhinal cortex high-frequency oscillations (100--500Hz) in human epileptic brain and in kainic acid--treated rats with chronic seizures. Epilepsia, 40, 127-137.
6. Buzsáki, G. (1989) Two-stage model of memory trace formation: a role for "noisy" brain states. Neuroscience, 31, 551-570.
7. Buzsáki, G. (1996) The hippocampo-neocortical dialogue. Cereb. Cortex, 6, 81-92.
8. Buzsáki, G. (2006) Rhythms of the Brain. Oxford University Press, New York, USA.
9. Buzsáki, G. & Draguhn, A. (2004) Neuronal oscillations in cortical networks. Science, 304, 1926-1929.
10. Clemens, Z., Mölle, M., Erõss, L., Barsi, P., Halász, P. & Born, J. (2007) Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain, 130, 2868-2878.
11. Collins, D.R., Lang, E.J. & Paré, D. (1999) Spontaneous activity of the perirhinal cortex in behaving cats. Neuroscience, 89, 1025-1039.
12. De Gennaro, L. & Ferrara, M. (2003) Sleep spindles: an overview. Sleep Med. Rev., 7, 423-440.
13. Diba, K. & Buzsáki, G. (2007) Forward and reverse hippocampal place-cell sequences during ripples. Nat. Neurosci., 10, 1241-1242.
14. Diekelmann, S. & Born, J. (2010) The memory function of sleep. Nat. Rev. Neurosci., 11, 114-126.
15. Doran, S.M. (2003) The dynamic topography of individual sleep spindles. Sleep Res. Online., 5, 133-139.
16. Faber, J. & Vladyka, V. (1984) Nocturnal sleep stereo-electroencephalography and polygraphy in epileptics. Acta Univ. Carol. Med. Monogr., 108, 1-145.
17. Isomura, Y., Sirota, A., Ozen, S., Montgomery, S., Mizuseki, K., Henze, D.A. & Buzsáki, G. (2006) Integration and segregation of activity in entorhinal-hippocampal subregions by neocortical slow oscillations. Neuron, 52, 871-882.
18. Ji, D. & Wilson, M.A. (2007) Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat. Neurosci., 10, 100-107.
19. Kudrimoti, H.S., Barnes, C.A. & McNaughton, B.L. (1999) Reactivation of hippocampal cell assemblies: effects of behavioral state, experience, and EEG dynamics. J. Neurosci., 19, 4090-4101.
20. Malow, B.A., Carney, P.R., Kushwaha, R. & Bowes, R.J. (1999) Hippocampal sleep spindles revisited: physiologic or epileptic activity? Clin. Neurophysiol., 110, 687-693.
21. Marshall, L. & Born, J. (2007) The contribution of sleep to hippocampus-dependent memory consolidation. Trends Cogn Sci., 11, 442-450.
22. McClelland, J.L., McNaughton, B.L. & O'Reilly, R.C. (1995) Why there are complementary learning systems in the hippocampus and neocortex: insights from the successes and failures of connectionist models of learning and memory. Psychol. Rev., 102, 419-457.
23. Mölle, M. & Born, J. (2009) Hippocampus whispering in deep sleep to prefrontal cortex - for good memories? Neuron, 61, 496-498.
24. Mölle, M., Marshall, L., Gais, S. & Born, J. (2002) Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep. J. Neurosci., 22, 10941-10947.
25. Mölle, M., Yeshenko, O., Marshall, L., Sara, S.J. & Born, J. (2006) Hippocampal sharp wave-ripples linked to slow oscillations in rat slow-wave sleep. J. Neurophysiol., 96, 62-70.
26. Mölle, M., Eschenko, O., Gais, S., Sara, S.J. & Born, J. (2009) The influence of learning on sleep slow oscillations and associated spindles and ripples in humans and rats. Eur. J. Neurosci., 29, 1071-1081.
27. Montplaisir, J., Leduc, L., Laverdière, M., Walsh, J. & Saint-Hilaire, J.M. (1981) Sleep spindles in the human hippocampus: normal or epileptic activity? Sleep, 4, 423-428.
28. Nádasdy, Z., Hirase, H., Czurkó, A., Csicsvari, J. & Buzsáki, G. (1999) Replay and time compression of recurring spike sequences in the hippocampus. J. Neurosci., 19, 9497-9507.
29. Paré, D., Steriade, M., Deschênes, M. & Oakson, G. (1987) Physiological characteristics of anterior thalamic nuclei, a group devoid of inputs from reticular thalamic nucleus. J. Neurophysiol., 57, 1669-1685.
30. Rasch, B., Buchel, C., Gais, S. & Born, J. (2007) Odor cues during slow-wave sleep prompt declarative memory consolidation. Science, 315, 1426-1429.
31. Rechtschaffen, A. & Kales, A. (1968) A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects. US Department of Health, Education and Welfare, Bethesda, MD.
32. Rosanova, M. & Ulrich, D. (2005) Pattern-specific associative long-term potentiation induced by a sleep spindle-related spike train. J. Neurosci., 25, 9398-9405.
33. Rosene, D.L. & Van Hoesen, G.W. (1977) Hippocampal efferents reach widespread areas of cerebral cortex and amygdala in the rhesus monkey. Science, 198, 315-317.
34. Schabus, M., Dang-Vu, T.T., Albouy, G., Balteau, E., Boly, M., Carrier, J., Darsaud, A., Degueldre, C., Desseilles, M., Gais, S., Phillips, C., Rauchs, G., Schnakers, C., Sterpenich, V., Vandewalle, G., Luxen, A. & Maquet, P. (2007) Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proc. Natl. Acad. Sci. USA, 104, 13164-13169.
35. Siapas, A.G. & Wilson, M.A. (1998) Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron, 21, 1123-1128.
36. Sirota, A. & Buzsáki, G. (2005) Interaction between neocortical and hippocampal networks via slow oscillations. Thalamus Relat. Syst., 3, 245-259.
37. Sirota, A., Csicsvari, J., Buhl, D. & Buzsáki, G. (2003) Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl. Acad. Sci. U S A, 100, 2065-2069.
38. Sirota, A., Montgomery, S., Fujisawa, S., Isomura, Y., Zugaro, M. & Buzsáki, G. (2008) Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron, 60, 683-697.
39. Staba, R.J., Wilson, C.L., Bragin, A., Fried, I. & Engel, J. Jr (2002) Quantitative analysis of high-frequency oscillations (80-500Hz) recorded in human epileptic hippocampus and entorhinal cortex. J. Neurophysiol., 88, 1743-1752.
40. Staba, R.J., Wilson, C.L., Bragin, A., Jhung, D., Fried, I. & Engel, J. Jr (2004) High-frequency oscillations recorded in human medial temporal lobe during sleep. Ann. Neurol., 56, 108-115.
41. Steriade, M. (1997) Synchronized activities of coupled oscillators in the cerebral cortex and thalamus at different levels of vigilance. Cereb. Cortex, 7, 583-604.
42. Steriade, M. (2006) Grouping of brain rhythms in corticothalamic systems. Neuroscience, 137, 1087-1106.
43. Swanson, L.W. (1981) A direct projection from Ammon's horn to prefrontal cortex in the rat. Brain Res., 217, 150-154.
44. Thierry, A.M., Gioanni, Y., Degenetais, E. & Glowinski, J. (2000) Hippocampo-prefrontal cortex pathway: anatomical and electrophysiological characteristics. Hippocampus, 10, 411-419.
45. Tononi, G. & Cirelli, C. (2006) Sleep function and synaptic homeostasis. Sleep Med. Rev., 10, 49-62.
46. Wierzynski, C.M., Lubenov, E.V., Gu, M. & Siapas, A.G. (2009) State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep. Neuron, 61, 587-596.
47. Wieser, H.G., Elger, C.E. & Stodieck, S.R. (1985) The 'foramen ovale electrode': a new recording method for the preoperative evaluation of patients suffering from mesio-basal temporal lobe epilepsy. Electroencephalogr. Clin. Neurophysiol., 61, 314-322.
48. Wilson, M.A. & McNaughton, B.L. (1994) Reactivation of hippocampal ensemble memories during sleep. Science, 265, 676-679.
49. Zeitlhofer, J., Gruber, G., Anderer, P., Asenbaum, S., Schimicek, P. & Saletu, B. (1997) Topographic distribution of sleep spindles in young healthy subjects. J. Sleep Res., 6, 149-155.