The neurons and mechanisms involved in mammalian spinal cord networks that produce rhythmic locomotor activity remain largely undefined. Hb9 interneurons, a small population of discretely localized interneurons in the mouse spinal cord, are conditionally bursting neurons (Wilson et al., 2005). Here we applied potassium channel blockers with the aim of increasing neuronal excitability and observed that under these conditions, postnatal Hb9 interneurons exhibited bursts of action potentials with underlying voltage-independent spikelets. The bursts were insensitive to antagonists to fast chemical synaptic transmission, and the bursting and spikelets were blocked by tetrodotoxin. Calcium imaging studies using 2-photon excitation in the spinal cord slice revealed that clustered Hb9 interneurons exhibited synchronous, and occasional asynchronous, calcium transients that were also insensitive to fast synaptic transmission blockade. All transients were blocked by the gap junction blocker carbenoxolone. Paired whole cell patch clamp recordings of Hb9 interneurons in the late postnatal mouse revealed common chemical synaptic inputs but no evidence of direct current transfer (i.e. electrotonic coupling) between the neurons. However, we found evidence that Hb9 and a previously defined population of non-Hb9 interneurons were electrotonically coupled. In the whole spinal cord preparation, 2-photon excitation calcium imaging in the absence of fast chemical transmission revealed bursting activity of Hb9 interneurons synchronous with rhythmic ventral root output. Thus, Hb9 interneurons are both endogenous bursters and rhythmically active within a heterogeneous electrotonically coupled network. A network with these properties could produce the wide range of stable rhythms necessary for locomotor activity.