Original Research ARTICLE
The fate of incoming stimuli during NREM sleep is determined by spindles and the phase of the slow oscillation
- 1 Cyclotron Research Centre, University of Liège, Liège, Belgium
- 2 Laboratory for Sleep and Consciousness Research, University of Salzburg, Salzburg, Austria
The present study aimed at identifying the neurophysiological responses associated with auditory stimulation during non-rapid eye movement (NREM) sleep using simultaneous electroencephalography (EEG)/functional magnetic resonance imaging (fMRI) recordings. It was reported earlier that auditory stimuli produce bilateral activation in auditory cortex, thalamus, and caudate during both wakefulness and NREM sleep. However, due to the spontaneous membrane potential fluctuations cortical responses may be highly variable during NREM. Here we now examine the modulation of cerebral responses to tones depending on the presence or absence of sleep spindles and the phase of the slow oscillation. Thirteen healthy young subjects were scanned successfully during stage 2–4 NREM sleep in the first half of the night in a 3 T scanner. Subjects were not sleep-deprived and sounds were post hoc classified according to (i) the presence of sleep spindles or (ii) the phase of the slow oscillation during (±300 ms) tone delivery. These detected sounds were then entered as regressors of interest in fMRI analyses. Interestingly wake-like responses – although somewhat altered in size and location – persisted during NREM sleep, except during present spindles (as previously published in Dang-Vu et al., 2011) and the negative going phase of the slow oscillation during which responses became less consistent or even absent. While the phase of the slow oscillation did not alter brain responses in primary sensory cortex, it did modulate responses at higher cortical levels. In addition EEG analyses show a distinct N550 response to tones during the presence of light sleep spindles and suggest that in deep NREM sleep the brain is more responsive during the positive going slope of the slow oscillation. The presence of short temporal windows during which the brain is open to external stimuli is consistent with the fact that even during deep sleep meaningful events can be detected. Altogether, our results emphasize the notion that spontaneous fluctuations of brain activity profoundly modify brain responses to external information across all behavioral states, including deep NREM sleep.
Keywords: AEP, sleep, spindles, spontaneous activity, slow-wave phase, EEG/fMRI, fMRI, EEG
Citation: Schabus M, Dang-Vu TT, Heib DPJ, Boly M, Desseilles M, Vandewalle G, Schmidt C, Albouy G, Darsaud A, Gais S, Degueldre C, Balteau E, Phillips C, Luxen A and Maquet P (2012) The fate of incoming stimuli during NREM sleep is determined by spindles and the phase of the slow oscillation. Front. Neur. 3:40. doi: 10.3389/fneur.2012.00040
Received: 14 November 2011; Paper pending published: 15 December 2011;
Accepted: 02 March 2012; Published online: 05 April 2012.
Edited by:Michael Czisch, Max Planck Institute of Psychiatry, Germany
Reviewed by:Renate Wehrle, University Clinic Regensburg, Germany
Kátia C. Andrade, Brain Institute/Federal University of Rio Grande do Norte, Brazil
Copyright: © 2012 Schabus, Dang-Vu, Heib, Boly, Desseilles, Vandewalle, Schmidt, Albouy, Darsaud, Gais, Degueldre, Balteau, Phillips, Luxen and Maquet. This is an open-access article distributed under the terms of the Creative Commons Attribution Non Commercial License, which permits non-commercial use, distribution, and reproduction in other forums, provided the original authors and source are credited.
*Correspondence: Manuel Schabus, Department of Psychology, University of Salzburg, Hellbrunnerstr.34, 5020 Salzburg, Austria. e-mail: email@example.com; Pierre Maquet, Cyclotron Research Centre (B30), University of Liège, Sart Tilman, 4000 Liège, Belgium. e-mail: firstname.lastname@example.org