Dreams are internally generated experiences that occur independently of current sensory input. Here we argue, based on cortical anatomy and function, that dream experiences are tightly related to the workings of a specific part of cortical pyramidal neurons, the apical integration zone (AIZ). The AIZ receives and processes contextual information from diverse sources and could constitute a major switch point for transitioning from externally to internally generated experiences such as dreams. We propose that during dreams the output of certain pyramidal neurons is mainly driven by input into the AIZ. We call this mode of functioning "apical drive". Our hypothesis is based on the evidence that the cholinergic and adrenergic arousal systems, which show different dynamics between waking, slow wave sleep, and rapid eye movement sleep, have specific effects on the AIZ. We suggest that apical drive may also contribute to waking experiences, such as mental imagery. Future studies, investigating the different modes of apical function and their regulation during sleep and wakefulness are likely to be richly rewarded.