This paper argues that humans possess unique cognitive abilities due to the presence of a functional system that exists in the human brain that is absent in the non-human brain. This system, the frontal feedback system, was born in the hominin brain when the great phylogenetic expansion of the prefrontal cortex relative to posterior sensory regions surpassed a critical threshold. Surpassing that threshold effectively reversed the preferred direction of information flow in the highest association regions of the neocortex, producing the (...) frontal feedback system. This reversal was from the caudo-rostral bias characteristic of non-human, or pre-human, brain dynamics to a rostro-caudal bias characteristic of modern human brain dynamics. The frontal feedback system works through frontal motor routines, or action schemes, manipulating the release and reconstruction of stored sensory memories in posterior sensory areas. As an obligatory feature of frontal feedback, a central character, or self, emerges within this cortical network that manifests itself as agent in these reconstructions as well as in the experience of sensory perceptions. Dynamical-systems modeling of cortical interactions is combined in the paper with recent neuroimaging studies of “resting-state” brain activity to bridge the gap between microscopic and macroscopic levels of cortical behavior. This synthesis is used to support the proposal of an information flow reversal occurring in the hominin brain and also to explain how such a reversal generates the wide variety of cognitive and experiential phenomena that many consider to be uniquely human. (shrink)