We measured a low-threshold, inactivating K⁺ current, i.e., A-current (I_A), in respiratory neurons of the preBötzinger Complex (preBötC) in rhythmically active slice preparations from neonatal C57BL/6 mice. The majority of inspiratory neurons (21/34 = 61.8%), but not expiratory neurons (1/8 = 12.5%), expressed I_A. In whole cell and somatic outside-out patches I_A activated at –60 mV (half-activation voltage measured –16.3 mV) and only fully inactivated above –40 mV (half-inactivation voltage measured –85.6 mV), indicating that I_A can influence membrane trajectory at baseline voltages during respiratory rhythm generation in vitro. 4-Aminopyridine (4-AP, 2 mM) attenuated I_A in both whole cell and somatic outside-out patches. In the context of rhythmic network activity, 4-AP caused irregular respiratory-related motor output on XII nerves and disrupted rhythmogenesis as detected with whole-cell and field recordings in the preBötC. Whole-cell current-clamp recordings showed that 4-AP changed the envelope of depolarization underlying inspiratory bursts (i.e., inspiratory drive potentials) from an incrementing pattern to a decrementing pattern during rhythm generation and abolished current pulse-induced delayed excitation. These data suggest that I_A opposes excitatory synaptic depolarizations at baseline voltages of approximately –60 mV and influences the inspiratory burst pattern. We propose that I_A promotes orderly recruitment of constituent rhythmogenic neurons by minimizing the activity of these neurons until they receive massive coincident synaptic input, which reduces the periodic fluctuations of inspiratory activity.