Sleep deprivation reduces default mode network connectivity and anti-correlation during rest and task performance

Abstract

Sleep deprivation (SD) can alter extrinsic, task-related fMRI signal involved in attention, memory and executive function. However, its effects on intrinsic low-frequency connectivity within the Default Mode Network (DMN) and its related anti-correlated network (ACN) have not been well characterized. We investigated the effect of SD on functional connectivity within the DMN, and on DMN-ACN anti-correlation, both during the resting state and during performance of a visual attention task (VAT). 26 healthy participants underwent fMRI twice: once after a normal night of sleep in rested wakefulness (RW) and once following approximately 24 h of total SD. A seed-based approach was used to examine pairwise correlations of low-frequency fMRI signal across different nodes in each state. SD was associated with significant selective reductions in DMN functional connectivity and DMN-ACN anti-correlation. This was congruent across resting state and VAT analyses, suggesting that SD induces a robust alteration in the intrinsic connectivity within and between these networks.

Introduction

A single night of total sleep deprivation (SD) can result in behavioral deficits with accompanying alterations in neural activation patterns (Chee and Chuah, 2008, Goel et al., 2009). To date, the focus of most research has been on delineating the regional effects of SD on attention (Chee et al., 2008, Lim and Dinges, 2008, Tomasi et al., 2009), short-term memory (Chee and Chuah, 2007) and executive function (Nilsson et al., 2005). In contrast, far less is known about the effect of sleep deprivation on intrinsic low-frequency connectivity within the Default Mode Network (DMN) and its anti-correlated network (ACN).

The DMN is a network of brain regions that consistently deactivates in response to externally oriented tasks (Raichle et al., 2001, Shulman et al., 1997) and activates in response to numerous tasks involving internally oriented cognition (Bar, 2007, Binder et al., 2009, D'Argembeau et al., 2005, Hassabis and Maguire, 2007). The main DMN nodes—the posterior cingulate cortex (PCC), precuneus and retrosplenial cortex, the dorsal and ventral medial prefrontal cortex (MPFC), inferior parietal lobule (IPL), lateral temporal cortex (LTC), and hippocampal formation (Buckner et al., 2008)—show correlated low-frequency BOLD signal fluctuations, suggesting functional connectivity (Greicius et al., 2003).

Interestingly, these low-frequency signals are anti-correlated with several regions normally activated as a group by externally oriented tasks (Fox et al., 2005). This anti-correlated network (ACN) includes the frontal eye fields (FEF), intraparietal sulcus (IPS), middle temporal region (MT), supplementary motor area (SMA), inferior parietal lobule (also referred to as the temporoparietal junction (TPJ; Corbetta and Shulman, 2002), dorsolateral prefrontal cortex (DLPFC), and Insula (Fox et al., 2005). Switching between externally and internally oriented cognition is thought to be mediated via a competitive relationship between the ACN and DMN (Fox and Raichle, 2007, Fox et al., 2005).

Relevant to the current work, DMN connectivity and anti-correlation is diminished in many neurological and psychiatric disorders (Broyd et al., 2009, Buckner et al., 2008). Functional connectivity within the DMN is also diminished when healthy persons enter deep sleep (Horovitz et al., 2009). Both DMN functional connectivity and anti-correlation are reduced subsequent to general anesthesia (Boveroux et al., 2010, Deshpande et al., 2010), leading to the notion that diminished DMN connectivity and anti-correlation can index disrupted brain function in a variety of contexts. This motivated us to investigate if DMN connectivity and anti-correlation is altered in healthy persons undergoing a night of total SD, given the association of this state with aforementioned alterations in cognitive function.

Several SD studies evaluating short-term memory (Chee and Choo, 2004, Chee and Chuah, 2007, Choo et al., 2005) have revealed reduction in task-related deactivation across several nodes of the DMN. However, a recent study evaluating working memory reported reduced deactivation in the MPFC along with increased precuneus deactivation (Gujar et al., 2010), suggesting altered functional connectivity between DMN nodes during SD. Indeed, recent work involving partial SD reported such reductions in DMN functional connectivity, along with reduced anti-correlation between the DMN and ACN (Sämann et al., 2010).

Functional connectivity involving the DMN has typically been evaluated using resting state data, but data acquired while participants perform tasks has also been used (Fair et al., 2007, Fransson, 2006, Greicius et al., 2003, Greicius and Menon, 2004). One approach is to regress out task-related activity before evaluating DMN functional connectivity (Fair et al., 2007). Although some studies suggest that this approach generates results comparable to those obtained from resting state data (Arfanakis et al., 2000, Fair et al., 2007), others suggest otherwise (Esposito et al., 2006, Esposito et al., 2009, Fransson, 2006).

In the present study, we evaluated the effect of SD on functional connectivity within the DMN and anti-correlation between the DMN and ACN, both during resting state and while volunteers performed a visual attention task (VAT). This comparison is important in SD studies because sleepiness increases in the supine position (Caldwell et al., 2003) and is expected to be accentuated following sleep deprivation, particularly in the absence of task performance. As such, it might be useful to assess changes in network connectivity while a person is engaged in a task to reduce the likelihood of volunteers falling asleep.