Sleep Deprivation Impairs Object-Selective Attention: A View from the Ventral Visual Cortex

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.