An essential question raised after the observation of highly variable bursting activity in individual neurons of Central Pattern Generators (CPGs) is how an assembly of such cells can cooperatively act to produce regular signals to motor systems. It is well known that some neurons in the lobster stomatogastric ganglion have a highly irregular spiking-bursting behavior when they are synaptically isolated from any connection in the CPG. Experimental recordings show that periodic stimuli on a single neuron can regulate its firing activity. Other evidence demonstrates that specific chemical and/or electrical synapses among neurons also induce the regularization of the rhythms. In this paper we present a modeling study in which a slow subcellular dynamics, the exchange of calcium between an intracellular store and the cytoplasm, is responsible for the origin and control of the irregular spiking-bursting activity. We show this in simulations of single cells under periodic driving and in minimal networks where the cooperative activity can induce regularization. While often neglected in the description of realistic neuron models, subcellular processes with slow dynamics may play an important role in information processing and short-term memory of spiking-bursting neurons.