Hemodynamic cerebral correlates of sleep spindles during human non-rapid eye movement sleep

Abstract

In humans, some evidence suggests that there are two different types of spindles during sleep, which differ by their scalp topography and possibly some aspects of their regulation. To test for the existence of two different spindle types, we characterized the activity associated with slow (11-13 Hz) and fast (13-15 Hz) spindles, identified as discrete events during non-rapid eye movement sleep, in non-sleepdeprived human volunteers, using simultaneous electroencephalography and functional MRI. An activation pattern common to both spindle types involved the thalami, paralimbic areas (anterior cingulate and insular cortices), and superior temporal gyri. No thalamic difference was detected in the direct comparison between slow and fast spindles although some thalamic areas were preferentially activated in relation to either spindle type. Beyond the common activation pattern, the increases in cortical activity differed significantly between the two spindle types. Slow spindles were associated with increased activity in the superior frontal gyrus. In contrast, fast spindles recruited a set of cortical regions involved in sensorimotor processing, as well as the mesial frontal cortex and hippocampus. The recruitment of partially segregated cortical networks for slow and fast spindles further supports the existence of two spindle types during human non-rapid eye movement sleep, with potentially different functional significance.H uman sleep is associated with a profound modification of consciousness and the emergence of distinct sleep oscillations. In the early stages of non-rapid eye movement (NREM) sleep, electroencephalographic recordings show characteristic spindle oscillations. In humans, spindles consist of waxing-and-waning 11-to 15-Hz oscillations, lasting 0.5-3 sec. At the cellular level, spindles are associated with substantial neuronal activity. Spindles arise from cyclic inhibition of thalamo-cortical (TC) neurons by reticular thalamic neurons. Postinihibitory rebound spike bursts in TC cells entrain cortical populations in spindle oscillations (1). These neuronal mechanisms, which involve large TC populations, are thought to shape the processing of information during light NREM sleep and participate in the alteration of consciousness that characterizes this stage of sleep.Little is known on the cerebral correlates of human spindles. Early positron emission tomography studies reported a negative relationship between thalamic cerebral blood flow and the power spectrum in the spindle frequency band (2). However, the low temporal resolution of positron emission tomography did not allow for a fine-grained characterization of the cerebral correlates of human spindles. In addition, two kinds of spindles are described in humans. Slow spindles (Ͻ13 Hz) predominate over frontal, whereas fast spindles (Ͼ13 Hz) prevail over centro-parietal areas. The difference in spindle scalp topography is also reflected by profound functional differences. These two spindling activities differ by their circadian and homeostatic regul...

Effects of fluctuating physiological rhythms during prolonged EEG-fMRI studies

“…These results are difficult to compare to those of the literature because cerebral correlates of spindles were mostly indirectly studied by sleep studies that encompassed all NREM or stage 2. Only one recent paper by Schabus et al (2007) reported hemodynamic modifications related specifically to spindles. They also showed a common positive correlation with BOLD in the lateral part of the thalami.…”

“…With respect to the other rhythms related to sleep, such as theta (Laufs et al, 2003b;Scheeringa et al, 2007), beta (Moosmann et al, 2003;Laufs et al, 2006), delta rhythms and sleep spindles (Schabus et al, 2007), the literature is not as rich and the impact of their modulation on the BOLD signal is not as clear. However, methods used in all these studies did not distinguish the BOLD effect of each specific rhythm.…”

“…Moreover, the analysis of spindles was restricted over a region-of-interest (ROI) encompassing the thalami and putamen because, in group analyses over the whole brain, BOLD responses in small structures even consistently observed in every individual can be non significant due to smoothing (Worsley et al, 2002). According to studies demonstrating the role of putamen and thalami in spindle generation (Steriade and Llinás, 1988;Steriade and Amzica, 1998;Schabus et al, 2007), we restricted the group analysis to this ROI.…”

Regional neocortical gray matter structure and sleep fragmentation in older adults

“…Moreover, sleep spindles 11 and slow waves 14 are associated with transient activation of specific cortical regions. Therefore, it is plausible that atrophy or dysfunction of specific cortical regions may have an effect on sleep continuity and depth.…”

“…The cerebral cortex plays an important role in the generation of sleep spindles, 11 K-complexes, 12,13 and slow waves, 14 electroencephalography features that may play an important role in maintaining the continuity and depth of natural sleep. Moreover, sleep spindles 11 and slow waves 14 are associated with transient activation of specific cortical regions.…”