Slow Oscillations during Sleep Coordinate Interregional Communication in Cortical Networks

Abstract

Large-amplitude sleep slow oscillations group faster neuronal oscillations and are of functional relevance for memory performance. However, relatively little is known about the impact of slow oscillations on functionally coupled networks. Here, we provide a comprehensive view on how human slow oscillatory dynamics influence various measures of brain processing. We demonstrate that slow oscillations coordinate interregional cortical communication, as assessed by phase synchrony in the sleep spindle frequency range and cross-frequency coupling between spindle and beta activity. Furthermore, we show that the organizing role of slow oscillations is restricted to circumscribed topographical areas. These findings add importantly to our basic understanding of the orchestrating role of slow oscillations. In addition, they are of considerable relevance for accounts of sleep-dependent memory reprocessing and consolidation.

Sleep to Remember

“…In this way, spindles are nested within the slow oscillations Cox et al, 2014). A recent study confirmed the coupling of spindles with the slow oscillation and further showed that the timing of the spindles in relation to the slow oscillation was important for memory consolidation.…”

“…Indeed, presenting specific cues associated with the original learning during subsequent SWS can facilitate memory performance upon awakening, for the auditory modality in rodents (Bendor and Wilson, 2012) and humans (Creery et al, 2015). In the olfactory modality, odors that were part of the learning context, when presented during SWS, memory retention of paired associate learning in humans (Rasch et al, 2007).…”

Phase-clustering bias in phase–amplitude cross-frequency coupling and its removal

“…This "nesting" of oscillations has been shown to occur in both humans and animals (Jensen and Colgin, 2007;McGinn and Valiante, 2014), and to relate to various task-related processes (Canolty et al, 2006), including perception (Händel and Haarmeier, 2009;Voytek et al, 2010;Gross et al, 2013), cognitive control (Cohen et al, 2009;Dürschmid et al, 2013), memory (Sauseng et al, 2008;Tort et al, 2009;Axmacher et al, 2010;Belluscio et al, 2012), and emotional processing (Popov et al, 2012). Crossfrequency coupling has also been related to spontaneous activity during sleep (Cox et al, 2014) and "default-mode" resting state (Foster and Parvizi, 2012). In general, cross-frequency coupling is proposed to reflect a common, fundamental principle of how neurophysiological processes in the brain can be temporally organized across different frequency bands (Lisman, 2005;Canolty and Knight, 2010), and thus, different time scales.…”

“…Recently, we introduced a simple modification to the PAC metric in an analysis of spindle-beta coupling (11-16 Hz and 20-25 Hz, respectively) in human electrophysiological sleep data (Cox et al, 2014). This method entails a linear removal of the phase clustering bias, resulting in debiased PAC (dPAC).…”

Coordination of Slow Waves With Sleep Spindles Predicts Sleep-Dependent Memory Consolidation in Schizophrenia

“…We determined whether these parameters --SW phase at spindle peak and consistency --differed by group and, to test our main hypothesis, we correlated them with sleep dependent memory consolidation. (C) As a secondary analysis to confirm timing results we used the standard technique, phase amplitude coupling (PAC) [40][41][42] , which uses all spindle time points to identify the SW phase at which sigma amplitude is maximal and tests the significance of this coupling.…”