How acute total sleep loss affects the attending brain: a meta-analysis of neuroimaging studies

Abstract

Study objectives: Attention is a cognitive domain that can be severely affected by sleep deprivation. Previous neuroimaging studies have used different attention paradigms and reported both increased and reduced brain activation after sleep deprivation. However, due to large variability in sleep deprivation protocols, task paradigms, experimental designs, characteristics of subject populations, and imaging techniques, there is no consensus regarding the effects of sleep loss on the attending brain. The aim of this meta-analysis was to identify brain activations that are commonly altered by acute total sleep deprivation across different attention tasks.

Design: Coordinate-based meta-analysis of neuroimaging studies of performance on attention tasks during experimental sleep deprivation.

Methods: The current version of the activation likelihood estimation (ALE) approach was used for meta-analysis. The authors searched published articles and identified 11 sleep deprivation neuroimaging studies using different attention tasks with a total of 185 participants, equaling 81 foci for ALE analysis.

Results: The meta-analysis revealed significantly reduced brain activation in multiple regions following sleep deprivation compared to rested wakefulness, including bilateral intraparietal sulcus, bilateral insula, right prefrontal cortex, medial frontal cortex, and right parahippocampal gyrus. Increased activation was found only in bilateral thalamus after sleep deprivation compared to rested wakefulness.

Conclusion: Acute total sleep deprivation decreases brain activation in the fronto-parietal attention network (prefrontal cortex and intraparietal sulcus) and in the salience network (insula and medial frontal cortex). Increased thalamic activation after sleep deprivation may reflect a complex interaction between the de-arousing effects of sleep loss and the arousing effects of task performance on thalamic activity.

Keywords: attention; fmri; fronto-parietal network; meta-analysis; salience network; sleep deprivation; thalamus.

Figure 1

Results from the ALE meta-analysis revealed significantly reduced activation (shown in blue) in the fronto-parietal network (Prefrontal cortex and bilateral Parietal lobe), Insula, and right Parahippocampal cortex (see images at Z = −6, Z = 9, Z = 32, Z = 43, the Z values represent the horizontal coordinates from inferior to superior direction, more negative Z value, more inferior direction and vice versa), but increased activation (shown in yellow and red) in the thalamus (see image at Z = 14) across different attention tasks following total sleep deprivation compared to rested wakefulness. All activations are significant at P < 0.05 corrected for multiple comparisons using the false discovery rate. ALE, activation likelihood estimation; L, left; R, right; B, bilateral.