Sleep deprivation impairs object-selective attention: a view from the ventral visual cortex

Abstract

Background: Most prior studies on selective attention in the setting of total sleep deprivation (SD) have focused on behavior or activation within fronto-parietal cognitive control areas. Here, we evaluated the effects of SD on the top-down biasing of activation of ventral visual cortex and on functional connectivity between cognitive control and other brain regions.

Methodology/principal findings: Twenty-three healthy young adult volunteers underwent fMRI after a normal night of sleep (RW) and after sleep deprivation in a counterbalanced manner while performing a selective attention task. During this task, pictures of houses or faces were randomly interleaved among scrambled images. Across different blocks, volunteers responded to house but not face pictures, face but not house pictures, or passively viewed pictures without responding. The appearance of task-relevant pictures was unpredictable in this paradigm. SD resulted in less accurate detection of target pictures without affecting the mean false alarm rate or response time. In addition to a reduction of fronto-parietal activation, attending to houses strongly modulated parahippocampal place area (PPA) activation during RW, but this attention-driven biasing of PPA activation was abolished following SD. Additionally, SD resulted in a significant decrement in functional connectivity between the PPA and two cognitive control areas, the left intraparietal sulcus and the left inferior frontal lobe.

Conclusions/significance: SD impairs selective attention as evidenced by reduced selectivity in PPA activation. Further, reduction in fronto-parietal and ventral visual task-related activation suggests that it also affects sustained attention. Reductions in functional connectivity may be an important additional imaging parameter to consider in characterizing the effects of sleep deprivation on cognition.

Figure 1. Schematic of the object-selective attention task.

Three faces and three houses were presented during every task block. Inter-stimulus intervals varied randomly after each scrambled image, and were held constant at 2000 ms following each target. Subjects performed 6 task runs during each scanning session. AF  =  attend and respond to faces; AH  =  attend and respond to houses; OBS  =  passive observation of houses and faces.

Figure 2. Effect of selective attention task on brain activation.

Brain regions showing significant activation in the conjunction of Attend House (AH) vs. baseline and Attend Face (AF) vs. baseline conditions (p<.001, uncorrected). The top panel depicts activation during rested wakefulness (RW), and the bottom panel depicts activation after approximately 24 h of total sleep deprivation (SD).

Figure 3. Parameter estimates of activation for the house conditions in areas associated with arousal and attention.

Parameter estimates for each condition and state associated with the left inferior frontal gyrus (IFG), left intraparietal sulcus (IPS), anterior cingulate cortex (ACC), and left thalamus. Significant state-related differences were observed in the left IFG and IPS, but not in ACC or the thalamus.

Figure 4. Effect of sleep deprivation on activation associated with selective attention for houses.

Brain regions that showed a significant effect of state on activation in the Attend House (AH) vs. baseline contrast (p<.001 uncorrected; in orange). This finding was similar to the main effect of state obtained using an ANOVA analysis. For comparison, the regions showing the effect of task are overlaid in green and the overlap between regions showing task and state effects are in an intermediate color. IPS  =  intraparietal sulcus; IFG  =  inferior frontal gyrus.

Figure 5. Effects of sleep deprivation and attention on parahippocampal place area (PPA) activation.

In the rested (RW) state, attention to houses (AH) resulted in significantly greater PPA activation compared to ignoring (IH) or observing (OH) houses. However, this attention biasing was lost during SD.

Figure 6. Psychophysiological interaction (PPI) in the rested and sleep deprived state.

Connectivity analysis was performed using seeds in the left intraparietal sulcus (IPS; Talairach co-ordinates: −27, −58, 37) and left inferior frontal regions (Talairach co-ordinates: −36, 11, 4) (seed regions represented by green squares). Each map represents the conjunction of regions showing significant PPI in the Attend House (AH) vs. Ignore House (IH) and AH vs. Observe House (OH) conditions (threshold p<.05).