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Acoustic oddball during NREM sleep: a combined EEG/fMRI study.

Czisch M, Wehrle R, Stiegler A, Peters H, Andrade K, Holsboer F, Sämann PG - PLoS ONE (2009)

Bottom Line: Our main results were: (1) Other than in wakefulness, rare tones did not induce a blood oxygenation level dependent (BOLD) signal increase in the auditory pathway but a strong negative BOLD response in motor areas and the amygdala. (2) Stratification of rare tones by the presence of evoked KCs detected activation of the auditory cortex, hippocampus, superior and middle frontal gyri and posterior cingulate only for rare tones followed by a KC. (3) The typical high frontocentral EEG deflections of KCs were not paralleled by a BOLD equivalent.We interpret this as a sleep protective mechanism to delimit motor responses and to reduce the sensitivity of the amygdala towards further incoming stimuli.The KC itself is not reflected by increased metabolic demand in BOLD based imaging, arguing that evoked KCs result from increased neural synchronicity without altered metabolic demand.

View Article: PubMed Central - PubMed

Affiliation: Max Planck Institute of Psychiatry, Munich, Germany. czisch@mpipsykl.mpg.de

ABSTRACT

Background: A condition vital for the consolidation and maintenance of sleep is generally reduced responsiveness to external stimuli. Despite this, the sleeper maintains a level of stimulus processing that allows to respond to potentially dangerous environmental signals. The mechanisms that subserve these contradictory functions are only incompletely understood.

Methodology/principal findings: Using combined EEG/fMRI we investigated the neural substrate of sleep protection by applying an acoustic oddball paradigm during light NREM sleep. Further, we studied the role of evoked K-complexes (KCs), an electroencephalographic hallmark of NREM sleep with a still unknown role for sleep protection. Our main results were: (1) Other than in wakefulness, rare tones did not induce a blood oxygenation level dependent (BOLD) signal increase in the auditory pathway but a strong negative BOLD response in motor areas and the amygdala. (2) Stratification of rare tones by the presence of evoked KCs detected activation of the auditory cortex, hippocampus, superior and middle frontal gyri and posterior cingulate only for rare tones followed by a KC. (3) The typical high frontocentral EEG deflections of KCs were not paralleled by a BOLD equivalent.

Conclusions/significance: We observed that rare tones lead to transient disengagement of motor and amygdala responses during light NREM sleep. We interpret this as a sleep protective mechanism to delimit motor responses and to reduce the sensitivity of the amygdala towards further incoming stimuli. Evoked KCs are suggested to originate from a brain state with relatively increased stimulus processing, revealing an activity pattern resembling novelty processing as previously reported during wakefulness. The KC itself is not reflected by increased metabolic demand in BOLD based imaging, arguing that evoked KCs result from increased neural synchronicity without altered metabolic demand.

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Differences in activation patterns dependent on evoked K-complexes.(A) Comparison of activation for rare tones followed by a KC against rare tones not evoking a KC response. Axial slices are indicated with MNI z-coordinates. FMRI data are thresholded at puncorr<0.001, cluster extent>10 voxels. (B) Evoked potentials for the Fz, Cz and Pz derivation. Green: frequent tones; red: rarew/oKC tones; black: rareKC tones. Surface mapping of EEG amplitudes for selected components is inserted.
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pone-0006749-g002: Differences in activation patterns dependent on evoked K-complexes.(A) Comparison of activation for rare tones followed by a KC against rare tones not evoking a KC response. Axial slices are indicated with MNI z-coordinates. FMRI data are thresholded at puncorr<0.001, cluster extent>10 voxels. (B) Evoked potentials for the Fz, Cz and Pz derivation. Green: frequent tones; red: rarew/oKC tones; black: rareKC tones. Surface mapping of EEG amplitudes for selected components is inserted.

Mentions: Electrode×trial type interactions were found for all analyzed components, reflecting generally higher sensitivity for the more anterior electrodes for amplitude differences (Figure 2B).


Acoustic oddball during NREM sleep: a combined EEG/fMRI study.

Czisch M, Wehrle R, Stiegler A, Peters H, Andrade K, Holsboer F, Sämann PG - PLoS ONE (2009)

Differences in activation patterns dependent on evoked K-complexes.(A) Comparison of activation for rare tones followed by a KC against rare tones not evoking a KC response. Axial slices are indicated with MNI z-coordinates. FMRI data are thresholded at puncorr<0.001, cluster extent>10 voxels. (B) Evoked potentials for the Fz, Cz and Pz derivation. Green: frequent tones; red: rarew/oKC tones; black: rareKC tones. Surface mapping of EEG amplitudes for selected components is inserted.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2727699&req=5

pone-0006749-g002: Differences in activation patterns dependent on evoked K-complexes.(A) Comparison of activation for rare tones followed by a KC against rare tones not evoking a KC response. Axial slices are indicated with MNI z-coordinates. FMRI data are thresholded at puncorr<0.001, cluster extent>10 voxels. (B) Evoked potentials for the Fz, Cz and Pz derivation. Green: frequent tones; red: rarew/oKC tones; black: rareKC tones. Surface mapping of EEG amplitudes for selected components is inserted.
Mentions: Electrode×trial type interactions were found for all analyzed components, reflecting generally higher sensitivity for the more anterior electrodes for amplitude differences (Figure 2B).

Bottom Line: Our main results were: (1) Other than in wakefulness, rare tones did not induce a blood oxygenation level dependent (BOLD) signal increase in the auditory pathway but a strong negative BOLD response in motor areas and the amygdala. (2) Stratification of rare tones by the presence of evoked KCs detected activation of the auditory cortex, hippocampus, superior and middle frontal gyri and posterior cingulate only for rare tones followed by a KC. (3) The typical high frontocentral EEG deflections of KCs were not paralleled by a BOLD equivalent.We interpret this as a sleep protective mechanism to delimit motor responses and to reduce the sensitivity of the amygdala towards further incoming stimuli.The KC itself is not reflected by increased metabolic demand in BOLD based imaging, arguing that evoked KCs result from increased neural synchronicity without altered metabolic demand.

View Article: PubMed Central - PubMed

Affiliation: Max Planck Institute of Psychiatry, Munich, Germany. czisch@mpipsykl.mpg.de

ABSTRACT

Background: A condition vital for the consolidation and maintenance of sleep is generally reduced responsiveness to external stimuli. Despite this, the sleeper maintains a level of stimulus processing that allows to respond to potentially dangerous environmental signals. The mechanisms that subserve these contradictory functions are only incompletely understood.

Methodology/principal findings: Using combined EEG/fMRI we investigated the neural substrate of sleep protection by applying an acoustic oddball paradigm during light NREM sleep. Further, we studied the role of evoked K-complexes (KCs), an electroencephalographic hallmark of NREM sleep with a still unknown role for sleep protection. Our main results were: (1) Other than in wakefulness, rare tones did not induce a blood oxygenation level dependent (BOLD) signal increase in the auditory pathway but a strong negative BOLD response in motor areas and the amygdala. (2) Stratification of rare tones by the presence of evoked KCs detected activation of the auditory cortex, hippocampus, superior and middle frontal gyri and posterior cingulate only for rare tones followed by a KC. (3) The typical high frontocentral EEG deflections of KCs were not paralleled by a BOLD equivalent.

Conclusions/significance: We observed that rare tones lead to transient disengagement of motor and amygdala responses during light NREM sleep. We interpret this as a sleep protective mechanism to delimit motor responses and to reduce the sensitivity of the amygdala towards further incoming stimuli. Evoked KCs are suggested to originate from a brain state with relatively increased stimulus processing, revealing an activity pattern resembling novelty processing as previously reported during wakefulness. The KC itself is not reflected by increased metabolic demand in BOLD based imaging, arguing that evoked KCs result from increased neural synchronicity without altered metabolic demand.

Show MeSH