It has been postulated that the brain operates in a self-organized critical state that brings multiple benefits, such as optimal sensitivity to input. Thus far, self-organized criticality has typically been depicted as a one-dimensional process, where one parameter is tuned to a critical value. However, the number of adjustable parameters in the brain is vast, and hence critical states can be expected to occupy a high-dimensional manifold inside a high-dimensional parameter space. Here, we show that adaptation rules inspired by homeostatic plasticity drive a neuro-inspired network to drift on a critical manifold, where the system is poised between inactivity and persistent activity. During the drift, global network parameters continue to change while the system remains at criticality.