Sleep spindle-related reactivation of category-specific cortical regions after learning face-scene associations

NeuroImage

Volumn 59, Issue 3, 2012, Pages 2733-2742

  Bergmann, Til O ^a,b   Mölle, Matthias ^c   Diedrichs, Jens ^a   Born, Jan ^c,d   Siebner, Hartwig R ^a,e,f  

^a UNIVERSITY OF KIEL   (Germany)

^b RADBOUD UNIVERSITY   (Netherlands)

^c UNIVERSITY OF LÜBECK   (Germany)

^d UNIVERSITY OF TÜBINGEN   (Germany)

^e HVIDOVRE HOSPITAL   (Denmark)

^f UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

EEG fMRI; Fusiform face area (FFA); Hippocampus; Paired associate learning; Parahippocampal place area (PPA)

Indexed keywords

ADULT; ARTICLE; BRAIN CORTEX; BRAIN FUNCTION; BRAIN REGION; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HIPPOCAMPUS; HUMAN; HUMAN EXPERIMENT; MALE; MEMORY; MOTOR CONTROL; NONREM SLEEP; NORMAL HUMAN; PAIRED ASSOCIATE LEARNING; PARAHIPPOCAMPAL PLACE AREA; PATTERN RECOGNITION; PRIORITY JOURNAL; RECALL; SLEEP SPINDLE; STIMULUS RESPONSE; TASK PERFORMANCE; VISUAL CORTEX; VISUOMOTOR COORDINATION;

ADULT; CEREBRAL CORTEX; ELECTROENCEPHALOGRAPHY; FACE; FEMALE; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; MEMORY; NEOCORTEX; PAIRED-ASSOCIATE LEARNING; PARAHIPPOCAMPAL GYRUS; PSYCHOMOTOR PERFORMANCE; SLEEP; SPACE PERCEPTION; THALAMUS; YOUNG ADULT;

EID: 84855452291     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.10.036     Document Type: Article

References (77)

1. Achermann P., Borbely A.A. Low-frequency (< 1 Hz) oscillations in the human sleep electroencephalogram. Neuroscience 1997, 81:213-222.
2. Adolphs R., Spezio M. Role of the amygdala in processing visual social stimuli. Prog. Brain Res. 2006, 156:363-378.
3. Allen P.J., Polizzi G., Krakow K., Fish D.R., Lemieux L. Identification of EEG events in the MR scanner: the problem of pulse artifact and a method for its subtraction. Neuroimage 1998, 8:229-239.
4. Allen P.J., Josephs O., Turner R. A method for removing imaging artifact from continuous EEG recorded during functional MRI. Neuroimage 2000, 12:230-239.
5. Andrade K.C., Spoormaker V.I., Dresler M., Wehrle R., Holsboer F., Samann P.G., Czisch M. Sleep spindles and hippocampal functional connectivity in human NREM sleep. J. Neurosci. 2011, 31:10331-10339.
6. Astafiev S.V., Snyder A.Z., Shulman G.L., Corbetta M. Comment on "modafinil shifts human locus coeruleus to low-tonic, high-phasic activity during functional MRI" and "homeostatic sleep pressure and responses to sustained attention in the suprachiasmatic area". Science 2010, 328:309. (author reply 309).
7. Buzsaki G. The hippocampo-neocortical dialogue. Cereb. Cortex 1996, 6:81-92.
8. Clemens Z., Fabo D., Halasz P. Overnight verbal memory retention correlates with the number of sleep spindles. Neuroscience 2005, 132:529-535.
9. Clemens Z., Fabo D., Halasz P. Twenty-four hours retention of visuospatial memory correlates with the number of parietal sleep spindles. Neurosci. Lett. 2006, 403:52-56.
10. Clemens Z., Mölle M., Eross L., Barsi P., Halasz P., Born J. Temporal coupling of parahippocampal ripples, sleep spindles and slow oscillations in humans. Brain 2007, 130:2868-2878.
11. Clemens Z., Mölle M., Eross L., Jakus R., Rasonyi G., Halasz P., Born J. Fine-tuned coupling between human parahippocampal ripples and sleep spindles. Eur. J. Neurosci. 2010, 33:511-520.
12. Contreras D., Destexhe A., Steriade M. Intracellular and computational characterization of the intracortical inhibitory control of synchronized thalamic inputs in vivo. J. Neurophysiol. 1997, 78:335-350.
13. Dang-Vu T.T., Schabus M., Desseilles M., Albouy G., Boly M., Darsaud A., Gais S., Rauchs G., Sterpenich V., Vandewalle G., Carrier J., Moonen G., Balteau E., Degueldre C., Luxen A., Phillips C., Maquet P. Spontaneous neural activity during human slow wave sleep. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:15160-15165.
14. Debener S., Ullsperger M., Siegel M., Engel A.K. Single-trial EEG-fMRI reveals the dynamics of cognitive function. Trends Cogn. Sci. 2006, 10:558-563.
15. Diekelmann S., Born J. The memory function of sleep. Nat. Rev. Neurosci. 2010, 11:114-126.
16. Ego-Stengel V., Wilson M.A. Disruption of ripple-associated hippocampal activity during rest impairs spatial learning in the rat. Hippocampus 2009, 20:1-10.
17. Eichenbaum H. A cortical-hippocampal system for declarative memory. Nat. Rev. Neurosci. 2000, 1:41-50.
18. Epstein R., Kanwisher N. A cortical representation of the local visual environment. Nature 1998, 392:598-601.
19. Eschenko O., Sara S.J. Learning-dependent, transient increase of activity in noradrenergic neurons of locus coeruleus during slow wave sleep in the rat: brain stem-cortex interplay for memory consolidation?. Cereb. Cortex 2008, 18:2596-2603.
20. Eschenko O., Mölle M., Born J., Sara S.J. Elevated sleep spindle density after learning or after retrieval in rats. J. Neurosci. 2006, 26:12914-12920.
21. Fogel S.M., Smith C.T. Learning-dependent changes in sleep spindles and Stage 2 sleep. J. Sleep Res. 2006, 15:250-255.
22. Frankland P.W., Bontempi B. The organization of recent and remote memories. Nat. Rev. Neurosci. 2005, 6:119-130.
23. Gais S., Mölle M., Helms K., Born J. Learning-dependent increases in sleep spindle density. J. Neurosci. 2002, 22:6830-6834.
24. Gauthier I., Tarr M.J., Moylan J., Skudlarski P., Gore J.C., Anderson A.W. The fusiform "face area" is part of a network that processes faces at the individual level. J. Cogn. Neurosci. 2000, 12:495-504.
25. Girardeau G., Benchenane K., Wiener S.I., Buzsaki G., Zugaro M.B. Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci. 2009, 12:1222-1223.
26. Glover G.H., Li T.Q., Ress D. Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR. Magn. Reson. Med. 2000, 44:162-167.
27. Hoddes E., Zarcone V., Smythe H., Phillips R., Dement W.C. Quantification of sleepiness: a new approach. Psychophysiology 1973, 10:431-436.
28. Horovitz S.G., Braun A.R., Carr W.S., Picchioni D., Balkin T.J., Fukunaga M., Duyn J.H. Decoupling of the brain's default mode network during deep sleep. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:11376-11381.
29. Johnson L.A., Euston D.R., Tatsuno M., McNaughton B.L. Stored-trace reactivation in rat prefrontal cortex is correlated with down-to-up state fluctuation density. J. Neurosci. 2010, 30:2650-2661.
30. Kandel A., Buzsaki G. Cellular-synaptic generation of sleep spindles, spike-and-wave discharges, and evoked thalamocortical responses in the neocortex of the rat. J. Neurosci. 1997, 17:6783-6797.
31. Kanwisher N., McDermott J., Chun M.M. The fusiform face area: a module in human extrastriate cortex specialized for face perception. J. Neurosci. 1997, 17:4302-4311.
32. Keren N.I., Lozar C.T., Harris K.C., Morgan P.S., Eckert M.A. In vivo mapping of the human locus coeruleus. Neuroimage 2009, 47:1261-1267.
33. Larson-Prior L.J., Zempel J.M., Nolan T.S., Prior F.W., Snyder A.Z., Raichle M.E. Cortical network functional connectivity in the descent to sleep. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:4489-4494.
34. Lepage M., Habib R., Tulving E. Hippocampal PET activations of memory encoding and retrieval: the HIPER model. Hippocampus 1998, 8:313-322.
35. Lestienne R., Herve-Minvielle A., Robinson D., Briois L., Sara S.J. Slow oscillations as a probe of the dynamics of the locus coeruleus-frontal cortex interaction in anesthetized rats. J. Physiol. Paris 1997, 91:273-284.
36. Maquet P. The role of sleep in learning and memory. Science 2001, 294:1048-1052.
37. Maquet P., Laureys S., Peigneux P., Fuchs S., Petiau C., Phillips C., Aerts J., Del Fiore G., Degueldre C., Meulemans T., Luxen A., Franck G., Van Der Linden M., Smith C., Cleeremans A. Experience-dependent changes in cerebral activation during human REM sleep. Nat. Neurosci. 2000, 3:831-836.
38. Marshall L., Born J. The contribution of sleep to hippocampus-dependent memory consolidation. Trends Cogn. Sci. 2007, 11:442-450.
39. McClelland J.L., McNaughton B.L., O'Reilly R.C. 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. 1995, 102:419-457.
40. Minzenberg M.J., Watrous A.J., Yoon J.H., Ursu S., Carter C.S. Modafinil shifts human locus coeruleus to low-tonic, high-phasic activity during functional MRI. Science 2008, 322:1700-1702.
41. Minzenberg M.J., Watrous A.J., Yoon J.H., La C., Ursu S., Carter C.S. Response to comment on "modafinil shifts human locus coeruleus to low-tonic, high-phasic activity during functional MRI". Science 2010, 328:309.
42. Mölle M., Born J. Hippocampus whispering in deep sleep to prefrontal cortex - for good memories?. Neuron 2009, 61:496-498.
43. 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.
44. 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.
45. Mölle M., Eschenko O., Gais S., Sara S.J., Born J. The influence of learning on sleep slow oscillations and associated spindles and ripples in humans and rats. Eur. J. Neurosci. 2009, 29:1071-1081.
46. Orban P., Rauchs G., Balteau E., Degueldre C., Luxen A., Maquet P., Peigneux P. Sleep after spatial learning promotes covert reorganization of brain activity. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:7124-7129.
47. Peigneux P., Laureys S., Fuchs S., Collette F., Perrin F., Reggers J., Phillips C., Degueldre C., Del Fiore G., Aerts J., Luxen A., Maquet P. Are spatial memories strengthened in the human hippocampus during slow wave sleep?. Neuron 2004, 44:535-545.
48. Peyrache A., Khamassi M., Benchenane K., Wiener S.I., Battaglia F.P. Replay of rule-learning related neural patterns in the prefrontal cortex during sleep. Nat. Neurosci. 2009, 12:919-926.
49. Poldrack R.A., Mumford J.A. Independence in ROI analysis: where is the voodoo?. Soc. Cogn. Affect. Neurosci. 2009, 4:208-213.
50. Poldrack R.A., Rodriguez P. How do memory systems interact? Evidence from human classification learning. Neurobiol. Learn. Mem. 2004, 82:324-332.
51. Rasch B., Born J. Maintaining memories by reactivation. Curr. Opin. Neurobiol. 2007, 17:698-703.
52. Rechtschaffen A., Kales A. A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects 1968, United States Government Printing Office, Washington, DC.
53. Sämann P.G., Wehrle R., Hoehn D., Spoormaker V.I., Peters H., Tully C., Holsboer F., Czisch M. Development of the Brain's default mode network from wakefulness to slow wave sleep. Cereb. Cortex 2011, 21:2082-2093.
54. Sara S.J. The locus coeruleus and noradrenergic modulation of cognition. Nat. Rev. Neurosci. 2009, 10:211-223.
55. Schabus M., Gruber G., Parapatics S., Sauter C., Klosch G., Anderer P., Klimesch W., Saletu B., Zeitlhofer J. Sleep spindles and their significance for declarative memory consolidation. Sleep 2004, 27:1479-1485.
56. Schabus M., Hodlmoser K., Gruber G., Sauter C., Anderer P., Klosch G., Parapatics S., Saletu B., Klimesch W., Zeitlhofer J. Sleep spindle-related activity in the human EEG and its relation to general cognitive and learning abilities. Eur. J. Neurosci. 2006, 23:1738-1746.
57. 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. Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:13164-13169.
58. Schabus M., Hoedlmoser K., Pecherstorfer T., Anderer P., Gruber G., Parapatics S., Sauter C., Kloesch G., Klimesch W., Saletu B., Zeitlhofer J. Interindividual sleep spindle differences and their relation to learning-related enhancements. Brain Res. 2008, 1191:127-135.
59. Schmidt C., Peigneux P., Muto V., Schenkel M., Knoblauch V., Munch M., de Quervain D.J., Wirz-Justice A., Cajochen C. Encoding difficulty promotes postlearning changes in sleep spindle activity during napping. J. Neurosci. 2006, 26:8976-8982.
60. Schmidt C., Collette F., Leclercq Y., Sterpenich V., Vandewalle G., Berthomier P., Berthomier C., Phillips C., Tinguely G., Darsaud A., Gais S., Schabus M., Desseilles M., Dang-Vu T.T., Salmon E., Balteau E., Degueldre C., Luxen A., Maquet P., Cajochen C., Peigneux P. Homeostatic sleep pressure and responses to sustained attention in the suprachiasmatic area. Science 2009, 324:516-519.
61. Schmidt C., Peigneux P., Maquet P., Phillips C. Response to comment on "homeostatic sleep pressure and responses to sustained attention in the suprachiasmatic area". Science 2010, 328:309.
62. Sejnowski T.J., Destexhe A. Why do we sleep?. Brain Res. 2000, 886:208-223.
63. Siapas A.G., Wilson M.A. Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 1998, 21:1123-1128.
64. Sirota A., Csicsvari J., Buhl D., Buzsaki G. Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:2065-2069.
65. Spaniol J., Davidson P.S., Kim A.S., Han H., Moscovitch M., Grady C.L. Event-related fMRI studies of episodic encoding and retrieval: meta-analyses using activation likelihood estimation. Neuropsychologia 2009, 47:1765-1779.
66. Spoormaker V.I., Schroter M.S., Gleiser P.M., Andrade K.C., Dresler M., Wehrle R., Samann P.G., Czisch M. Development of a large-scale functional brain network during human non-rapid eye movement sleep. J. Neurosci. 2010, 30:11379-11387.
67. Steriade M. Grouping of brain rhythms in corticothalamic systems. Neuroscience 2006, 137:1087-1106.
68. Steriade M., Timofeev I. Neuronal plasticity in thalamocortical networks during sleep and waking oscillations. Neuron 2003, 37:563-576.
69. Steriade M., Nunez A., Amzica F. A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components. J. Neurosci. 1993, 13:3252-3265.
70. Sterpenich V., Albouy G., Darsaud A., Schmidt C., Vandewalle G., Dang Vu T.T., Desseilles M., Phillips C., Degueldre C., Balteau E., Collette F., Luxen A., Maquet P. Sleep promotes the neural reorganization of remote emotional memory. J. Neurosci. 2009, 29:5143-5152.
71. Stickgold R. Sleep-dependent memory consolidation. Nature 2005, 437:1272-1278.
72. Sutherland G.R., McNaughton B. Memory trace reactivation in hippocampal and neocortical neuronal ensembles. Curr. Opin. Neurobiol. 2000, 10:180-186.
73. Van Der Werf Y.D., Altena E., Schoonheim M.M., Sanz-Arigita E.J., Vis J.C., De Rijke W., Van Someren E.J. Sleep benefits subsequent hippocampal functioning. Nat. Neurosci. 2009, 12:122-123.
74. van Dongen E.V., Takashima A., Barth M., Fernandez G. Functional connectivity during light sleep is correlated with memory performance for face-location associations. Neuroimage 2011, 57:262-270.
75. Werk C.M., Harbour V.L., Chapman C.A. Induction of long-term potentiation leads to increased reliability of evoked neocortical spindles in vivo. Neuroscience 2005, 131:793-800.
76. Wierzynski C.M., Lubenov E.V., Gu M., Siapas A.G. State-dependent spike-timing relationships between hippocampal and prefrontal circuits during sleep. Neuron 2009, 61:587-596.
77. Yoo S.S., Hu P.T., Gujar N., Jolesz F.A., Walker M.P. A deficit in the ability to form new human memories without sleep. Nat. Neurosci. 2007, 10:385-392.