Cortical network functional connectivity in the descent to sleep

Abstract

Descent into sleep is accompanied by disengagement of the conscious brain from the external world. It follows that this process should be associated with reduced neural activity in regions of the brain known to mediate interaction with the environment. We examined blood oxygen dependent (BOLD) signal functional connectivity using conventional seed-based analyses in 3 primary sensory and 3 association networks as normal young adults transitioned from wakefulness to light sleep while lying immobile in the bore of a magnetic resonance imaging scanner. Functional connectivity was maintained in each network throughout all examined states of arousal. Indeed, correlations within the dorsal attention network modestly but significantly increased during light sleep compared to wakefulness. Moreover, our data suggest that neuronally mediated BOLD signal variance generally increases in light sleep. These results do not support the view that ongoing BOLD fluctuations primarily reflect unconstrained cognition. Rather, accumulating evidence supports the hypothesis that spontaneous BOLD fluctuations reflect processes that maintain the integrity of functional systems in the brain.default network ͉ fMRI ͉ neuroimaging ͉ non-rapid eye movement sleep T here is a physiologically distinct change in the state of the brain during sleep in comparison to wakefulness that is manifest subjectively as altered awareness and objectively as reduced responsiveness to environmental stimuli. The electrophysiological correlates of sleep are sufficiently pronounced and characteristic as to be defining (1, 2). Thus, natural sleep is characterized by a sequence of electroencephalographically defined stages that may be broadly divided into nonrapid eye movement (NREM) and rapid eye movement (REM) that cyclically alternate throughout the sleep period.Over the past decade, PET studies have shown that throughout NREM sleep cerebral blood flow and metabolism are reduced in cortical association areas (3-7), as well as in the brainstem, thalamus, basal ganglia, and basal forebrain (3, 4, 7). NREM sleep is accompanied by reduced responsiveness to stimuli in regions involved in executive function, attention, and perceptual processing (5,7,8). The deepest NREM sleep states are characterized by low frequency oscillations in the EEG during which cognition is thought to be greatly reduced (9-13). During REM, cerebral blood flow and metabolism remain decreased in prefrontal and parietal regions but are increased in paralimbic areas, anterior cingulate, and thalamus (3,7,14), a pattern consistent with the emotionality and reduced logicality notable in during dreaming (7,15,16). REM sleep is also marked by atonia in skeletal muscles, reducing the ability to overtly respond to external stimulation. Thus, the transitions from wakefulness to successively deeper stages of NREM and then REM sleep progressively disengage the self from the environment.It is now well-established that slow (Ͻ0.1 Hz) spontaneous fluctuations of the blood oxygen dependent (BOLD) signal show ph...

Principal components of functional connectivity: A new approach to study dynamic brain connectivity during rest

“…These networks of regions with coherent activity during rest are consistent across subjects and closely resemble the brain's functional organization of evoked responses (Damoiseaux et al, 2006;Fox and Raichle, 2007;Laird et al, 2011;Smith et al, 2009). Coherent BOLD activity persists during sleep and in anesthetized monkeys, suggesting that it reflects a fundamental property of the brain's functional organization (Larson-Prior et al, 2009;Vincent et al, 2007).…”

“…These networks of regions with coherent activity during rest are consistent across subjects and closely resemble the brain's functional organization of evoked responses (Damoiseaux et al, 2006;Fox and Raichle, 2007;Laird et al, 2011;Smith et al, 2009). Coherent BOLD activity persists during sleep and in anesthetized monkeys, suggesting that it reflects a fundamental property of the brain's functional organization (Larson-Prior et al, 2009;Vincent et al, 2007).Coherent BOLD activity, known as "functional connectivity" (FC), is modulated by learning (Bassett et al, 2011), cognitive and affective states (Cribben et al, 2012;Ekman et al, 2012;Eryilmaz et al, 2011;Richiardi et al, 2011;Shirer et al, 2012) and also spontaneously Chang and Glover, 2010; Kitzbichler et al, 2009). Chang andGlover (2010) showed that FC between the posterior cingulate cortex, a key region of the default mode network, and various other brain regions was highly dynamic over time.…”

As we fall asleep we forget about the future: A quantitative linguistic analysis of mentation reports from hypnagogia

“…What further supports the prediction of the AIM model for sleep onset is that general blood-oxygenlevel dependent (BOLD) activity has been shown to decrease from waking to sleep onsetnotably, amongst others, in the frontal lobes and limbic structures, including the hippocampus as well as the occipital lobes (Kaufmann et al, 2006). However, BOLD signal functional connectivity does not decrease within sleep onset, and functional connectivity within the dorsal attention network even increases slightly in light sleep (Larson-Priora et al, 2009). …”

“…to exhibit decreased functional connectivity between its components) in sleep (Picchioni, Duyn, & Horovitz, 2013). While the connectivity between the DMN nodes is strongest in wakeful rest, connectivity has been reported to undergo only small changes (Horovitz et al, 2008;Larson-Priora et al, 2009), or no changes at all (Sämann et al, 2011), in sleep onset. In sleep stage 2, the functional connectivity between the posterior cingulate cortex and medial prefrontal cortex is reduced, and decreases further in sleep stage 3 (Sämann et al, 2011;Wu et al, 2012).…”

Mesoscale infraslow spontaneous membrane potential fluctuations recapitulate high-frequency activity cortical motifs

“…From its early description as 'infraslow' 4 , spontaneous or resting-state activity at this very low-frequency domain (o0.1 Hz) has been observed as a consistent feature of ongoing brain activity across different species [4][5][6][7] and across different brain states 5,[8][9][10] , though its precise function and mechanistic underpinnings remain unclear. In the developing brain, electrophysiological infraslow activity in the form of neuronal activity transients or bursting activity has been linked with the development of neuronal networks 11,12 , whereas in the adult brain, infraslow activity has been demonstrated to synchronize with higher-frequency brain activity 13,14 and to correlate to variability in behavioural performance 15,16 .…”