Sleep deprivation in youth has garnered international attention in recent years, as correlational studies have demonstrated significant relationships between lack of sleep and detrimental behavioral and academic outcomes. However, no study to date has systematically examined the neurophysiological consequences of a single night of sleep restriction (i.e., 4 h) in adolescents using ultra-high field functional neuroimaging. Much of what we know regarding the neural consequences of sleep deprivation has come from the adult literature, and among those studies, the majority use region of interest (ROI) approaches, thus disregarding the dynamic mechanisms that may subserve the behavioral effects of sleep restriction. Leveraging a crossover within-subjects design, we demonstrate that pivotal brain regions involved in the default mode and limbic regulatory centers have disrupted functioning following a night of restricted sleep compared to a night of “normal sleep”. Specifically, a normal night (i.e., 8 h) of sleep led to increased global and local efficiency of bilateral amygdala, and less efficiency in the posterior cingulate, as measured by graph theory, compared to a night of sleep restriction. Furthermore, aberrant functional connectivity patterns were identified in key fronto-limbic circuitry, suggesting a potential pathophysiological mechanism underlying the widespread effects of sleep deprivation in youth.