Sleep deprivation rapidly disrupts cognitive function, and in the long term contributes to neurological disease. Why sleep deprivation has such profound effects on cognition is not well understood. Here, we use simultaneous fast fMRI-EEG to test how sleep deprivation modulates cognitive, neural, and fluid dynamics in the human brain. We demonstrate that after sleep deprivation, sleep-like pulsatile cerebrospinal fluid (CSF) flow events intrude into the awake state. CSF flow is coupled to attentional function, with high flow during attentional impairment. Furthermore, CSF flow is tightly orchestrated in a series of brain-body changes including broadband neuronal shifts, pupil constriction, and altered systemic physiology, pointing to a coupled system of fluid dynamics and neuromodulatory state. The timing of these dynamics is consistent with a vascular mechanism regulated by neuromodulatory state, in which CSF begins to flow outward when attention fails, and flow reverses when attention recovers. The attentional costs of sleep deprivation may thus reflect an irrepressible need for neuronal rest periods and widespread pulsatile fluid flow.