In Aplysia, mutually antagonistic ingestive and egestive behaviors are produced by the same multifunctional central pattern generator (CPG) circuit. Interestingly, higher-order inputs that activate the CPG do not directly specify whether the resulting motor program is ingestive or egestive, because the slow dynamics of the network intervene. One input, the command-like cerebral-buccal interneuron 2 (CBI-2), slowly drives the motor output towards ingestion. While another input, the esophageal nerve (EN), drives the motor output towards egestion. When the input is switched from EN to CBI-2, the motor output does not switch immediately, and remains egestive. Here, we investigated how these slow dynamics are implemented on the interneuronal level. We found that activity of two CPG interneurons, B20 and B40, tracked the motor output regardless of the input, while activity of another CPG interneuron, B65, tracked the input regardless of the motor output. Furthermore, we show that the slow dynamics of the network are implemented, at least in part, in the slow dynamics of the interaction between the input-representing and the output-representing neurons. We conclude that 1) a population of CPG interneurons, recruited during a particular motor program, simultaneously encodes both the input that is used to elicit the motor program, and the output elicited by this input; and, 2) activity of the input-representing neurons may serve to bias the future motor programs.