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. 2011 Sep 13;108(37):15438-43.
doi: 10.1073/pnas.1112503108. Epub 2011 Sep 6.

Interplay between spontaneous and induced brain activity during human non-rapid eye movement sleep

Thien Thanh Dang-Vu  1 , Maxime Bonjean, Manuel Schabus, Mélanie Boly, Annabelle Darsaud, Martin Desseilles, Christian Degueldre, Evelyne Balteau, Christophe Phillips, André Luxen, Terrence J Sejnowski, Pierre Maquet
Affiliations

Interplay between spontaneous and induced brain activity during human non-rapid eye movement sleep

Thien Thanh Dang-Vu et al. Proc Natl Acad Sci U S A. .

Abstract

Humans are less responsive to the surrounding environment during sleep. However, the extent to which the human brain responds to external stimuli during sleep is uncertain. We used simultaneous EEG and functional MRI to characterize brain responses to tones during wakefulness and non-rapid eye movement (NREM) sleep. Sounds during wakefulness elicited responses in the thalamus and primary auditory cortex. These responses persisted in NREM sleep, except throughout spindles, during which they became less consistent. When sounds induced a K complex, activity in the auditory cortex was enhanced and responses in distant frontal areas were elicited, similar to the stereotypical pattern associated with slow oscillations. These data show that sound processing during NREM sleep is constrained by fundamental brain oscillatory modes (slow oscillations and spindles), which result in a complex interplay between spontaneous and induced brain activity. The distortion of sensory information at the thalamic level, especially during spindles, functionally isolates the cortex from the environment and might provide unique conditions favorable for off-line memory processing.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Experimental protocol. (A) Timeline of experimental procedure. After a 4-d constant sleep schedule, volunteers were recorded with EEG/fMRI during the experimental night. (B) Experimental night. Sessions of continuous wakefulness (light blue) as well as S2-3 of NREM sleep (orange) with corresponding fMRI time series were selected for analysis. S1 and S4 of NREM sleep, depicted in light brown, were not used for analysis. (C) Events of interest included the tones categorized according to their occurrence during S2-3 within (TS, red squares) or outside (TN, blue squares) spindles.
Fig. 2.
Fig. 2.
Brain regions activated in relation to tones during waking (TW), NREM sleep (outside spindles; TN), and spindles (TS). (A) Significant responses associated with tones presented during waking. (B) Significant responses associated with tones presented during S2-3 NREM sleep, in the absence of ongoing spindles. These responses are located in the thalamus, primary auditory cortex, brainstem, cerebellum, middle frontal gyrus, precuneus, and posterior cingulate gyrus. The brainstem response encompasses areas compatible with the cochlear nuclear groups (peak voxel), the trapezoid bodies, and the superior olivary complex. (C) Significant responses associated with tones presented within spindles in S2-3 NREM sleep. In this area of the brainstem (arrow, Inset), neural populations that process sound are found in the nuclei of the lateral lemniscus. Functional results are displayed on an individual structural image (display at P < 0.001, uncorrected), at different levels of the x, y, and z axes as indicated for each section. (D and E) Fitted responses in the thalamus (x = −12, y = −22, z = −6; D) and the auditory cortex (x = 58, y = −14, z = 6; E) associated with sounds delivered with (red, TS) or without (blue, TN) ongoing spontaneous spindle. The curves correspond to the mean and the shaded areas to the SEM. Coordinates of the thalamus and auditory cortex were derived from the peak voxels in these areas during wakefulness (TW).
Fig. 3.
Fig. 3.
Difference in responses to TN and TS. (A) Brain areas showing significant responses for tones presented during NREM sleep outside spindles (TN) and not to tones presented during spindles (TS). Functional results are displayed on an individual structural image (display at P < 0.001, uncorrected). (B) Mean parameter estimates (arbitrary units ± SEM) for TN and TS in the right Heschl's gyrus. *P ≤ 0.05.
Fig. 4.
Fig. 4.
Brain regions activated in relation to tones during NREM sleep (outside spindles), followed (TNK) or not followed (TN0) by a K complex. (A) Significant responses associated with tones presented during S2-3 NREM sleep, in the absence of ongoing spindles, and when tones were followed by a K complex (TNK). (B) Significant responses associated with tones presented during S2-3 NREM sleep, in the absence of ongoing spindles, and when tones were not followed by a K complex (TN0). (C Top and Middle) Brain areas showing larger activations for TNK compared with TN0. Although responses to both TNK and TN0 overlap with areas recruited by TN, responses to TNK are significantly larger than those to TN0 in the primary auditory cortex and inferior frontal gyrus. (Bottom) Mean parameter estimates (arbitrary units ± SEM) for TNK and TN0 in the right Heschl's gyrus. *P ≤ 0.05. Functional results are displayed on an individual structural image (display at P < 0.001, uncorrected) at different levels of the x, y, and z axes as indicated for each section.
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