Breathing is a vital rhythmic motor behavior incessant from the first to our last breath. Increasingly refined anatomical, physiological, and genetic methods identified critical neuronal structures for breathing in a rostro-caudally aligned column of discrete functional nuclei with distinct neuron types that constitute the Ventral Respiratory Column (VRC). However, the concept of such compartmentalized organization must be reconciled with the considerable neuronal heterogeneity distributed along the entire VRC. Using Neuropixel probes we record simultaneously from hundreds of neurons across the entire VRC in anesthetized, but otherwise intact, freely breathing mice. Combined with optogenetic tagging techniques, and 3D histological reconstruction we create a functional, anatomic, and genetic map of over 13,000 neurons in the VRC with single-unit and millisecond resolution. By applying recent neural population analyses we uncover that a highly constrained rotational latent dynamical mode governs normal breathing. Our data reveal that the offset of inspiration forms an attractor that resets the respiratory rhythm, suggesting that the respiratory cycle begins not at the onset of an inspiration, but its cessation. These trajectories are sensitive to metabolic and pharmacological manipulations. Opioid administration alters the latent timing, while hypoxia-induced gasping results in a discrete reconfiguration from rotational to ballistic dynamics. These data provide a novel look at an old problem. They conceptualize the constitutive components of respiratory neural activity not as being composed of the average activity of homogenous genetic cell-classes or single nuclei, but of the underlying low dimensional neural activity patterns (neural modes) which may be distributed across cells of a given genotype and/or anatomical location.