The Brain from Inside Out takes a critical look at contemporary brain research and reminds us that theoretical framework does matter. Current technology-driven neuroscience is still largely fueled by an empiricist philosophy assuming that the brain’s goal is to perceive, represent the world, and learn the truth. An inevitable consequence of this framework is the assumption of a decision-making homunculus wedged between our perception and actions. In contrast, The Brain from Inside Out advocates that the brain’s fundamental function is to induce actions and predict the consequences of those actions to support the survival and prosperity of the brain’s host. Brains constantly test their hypotheses by producing actions rather than searching for the veridical objective world. Only actions can provide a second opinion about the relevance of the sensory inputs and provide meaning for and interpretation of those inputs. In this inside-out framework, it is not sensations that teach the brain and build up its circuits. Instead, the brain comes with a preconfigured and self-organized dynamics that constrains how it acts and views the world. Both its anatomical and physiological organizations are characterized by an enormous diversity which spans several orders of magnitude. The two ends of this continuous landscape give rise to apparently distinct qualitative features. A small core of strongly interconnected, highly active neurons provides fast and “good-enough” answers in needy situations by generalizations, whereas detailed and precise solutions rely on the contribution of the more isolated and sluggish majority. In this non-egalitarian organization, preexisting nonsense brain patterns become meaningful through action-based experience. The inside-out framework offers an alternative strategy to investigate how brain operations give rise to our cognitive faculties, as opposed to the outside-in approach that explores how our preconceived ideas map onto brain structures.