Criticality has emerged as a leading dynamical candidate for healthy and pathological neuronal activity. At the heart of criticality in neural systems is the need for parameters to be tuned to specific values or for the existence of self-organizing mechanisms. Existing models lack precise physiological descriptions for how the brain maintains its tuning near a critical point. In this paper we argue that a key ingredient missing from the field is a formulation of reciprocal coupling between neural activity and metabolic resources. We propose that the constraint of optimizing the balance between energy use and activity plays a major role in tuning brain states to lie near criticality. Important recent findings aligned with our viewpoint have emerged from analyses of disorders that involve severe metabolic disturbances and alter scale-free properties of brain dynamics, including burst suppression. Moreover, we argue that average shapes of neuronal avalanches are a signature of scale-free activity that offers sharper insights into underlying mechanisms than afforded by traditional analyses of avalanche statistics. © 2014 Roberts, Iyer, Vanhatalo and Breakspear.