Brain activation and hypothalamic functional connectivity during human non-rapid eye movement sleep: an EEG/fMRI study

• Published in: Brain (London, England : 1878) England : 1878), 2006-03, Vol.129 (3), p.655-667
• Main Authors: Kaufmann, C., Wehrle, R., Wetter, T. C., Holsboer, F., Auer, D. P., Pollmächer, T., Czisch, M.
• Format: Article
• Language: English
• Subjects: ACC = anterior cingulate cortex; Adult; BA = Brodmann area; Biological and medical sciences; BOLD = blood oxygenation level dependent; Brain - physiology; brain imaging; Brain Mapping - methods; EEG; Electrodiagnosis. Electric activity recording; Electroencephalography; Female; fMRI; fMRI = functional MRI; Human viral diseases; Humans; Hypothalamus - physiology; IFG = inferior frontal gyrus; Infectious diseases; Investigative techniques, diagnostic techniques (general aspects); IPL = inferior parietal lobule; Magnetic Resonance Imaging; Male; MedFG = medial frontal gyrus; Medical sciences; MFG = middle frontal gyrus; Nervous system; Neurology; NREM = non-rapid eye movement; NREM sleep; Oxygen - blood; S1/2/3/4 = sleep stages 1–4; SFG = superior frontal gyrus; Signal Processing, Computer-Assisted; sleep; Sleep Deprivation - physiopathology; Sleep Stages - physiology; SPM = statistical parametric mapping; STG = superior temporal gyrus; SWS = slow-wave sleep; Viral diseases; Viral diseases of the lymphoid tissue and the blood. Aids; Wakefulness - physiology
• ISSN: 0006-8950; 1460-2156
• DOI: 10.1093/brain/awh686

Regional differences in sleep EEG dynamics indicate that sleep-related brain activity involves local brain processes with sleep stage specific activity patterns of neuronal populations. Macroscopically, it is not fully understood which cerebral brain regions are involved in the successive discontinuation of wakefulness. We simultaneously used EEG and functional MRI on 9 subjects (6 female: mean = 24.1 years, 3 male: mean = 26.0 years) and analyzed local blood oxygenation level dependent signal changes linked to the transition from wakefulness to different non-rapid eye movement (NREM) sleep stages (according to Rechtschaffen and Kales) of the first sleep cycles after 36 h of total sleep deprivation. Several brain regions throughout the cortex, the limbic lobe, the thalamus, the caudate nucleus, as well as midbrain structures, such as the mammillary body/hypothalamus, showed reduced activity during NREM sleep across all sleep stages. Additionally, we found deactivation patterns specific to NREM sleep stages compared with wakefulness suggesting that a synchronized sleeping state can be established only if these regions interact in a well-balanced way. Sleep stage 2, which is usually linked to the loss of self-conscious awareness, is associated with signal decreases comprising thalamic and hypothalamic regions, the cingulate cortex, the right insula and adjacent regions of the temporal lobe, the inferior parietal lobule and the inferior/middle frontal gyri. The hypothalamic region known to be of particular importance in the regulation of the sleep–wake cycle shows specific temporally correlated network activity with the cortex while the system is in the sleeping state, but not during wakefulness. We describe a specific pattern of decreased brain activity during sleep and suggest that this pattern must be synchronized for establishing and maintaining sleep.