My thesis aimed to elucidate several aspects of motor circuit regulation and its impact on movement. It is well established that a single motor network can produce different output patterns in response to different inputs. However, in most model systems it remains challenging to identify the neurons comprising these networks and determine their role(s) in network operation, including whether each network neuron retains its role(s) when the network generates different output patterns. Also, most work on these circuits has occurred in the isolated nervous system, so little is known about how muscles respond to distinct neural outputs. I therefore aimed to address the cellular and synaptic mechanisms underlying these unresolved issues using the decapod crustacean stomatogastric nervous system. My work focused on a rhythmically active, network-driven motor circuit (central pattern generator [CPG] circuit) called the gastric mill (chewing) CPG in the crab stomatogastric ganglion. This circuit generates the gastric mill rhythm when activated by modulatory projection neurons (e.g. MCN1, CPN2) located in the commissural ganglia, and it is regulated by identified sensory feedback. I addressed and confirmed the hypothesis that, in the isolated nervous system, different extrinsic inputs can drive different gastric mill motor patterns. This enabled me to determine, for the first time in a network-driven motor circuit, that different motor patterns generated by the same motor circuit are paced by the same set of rhythm generator neurons. I further hypothesized and confirmed that these distinct motor patterns are retained at the level of at least some target muscles, and hence likely underlie different behavioral patterns. Lastly, I obtained data supporting the hypothesis that different extrinsic inputs distinctly modify the influence of a sensory feedback pathway on the relevant projection neurons (MCN1, CPN2), enabling the same sensory system to have different effects on different gastric mill rhythms. These results provide among the most detailed comparisons of how motor patterns generated by a single sensorimotor system are selected and regulated. The results thereby provide evidence for several novel cellular and synaptic mechanisms that expand our appreciation of the number of degrees of freedom available to even small sensorimotor systems.