Cerebrospinal fluid-contacting neurons (CSF-cNs) are a distinct medullospinal population strategically located around the central canal. In zebrafish, they sense spinal curvature and CSF composition, but their role in CNS circuitry of tetrapods remains unclear. In this work, we mapped the CSF-cNs network using Pkd2l1Cre mice to selectively label their cell bodies, axons and synaptic terminals. We confirm their presence along the brainstem central canal, extending up to the fourth ventricle. Their axons project to several brainstem areas, including the hypoglossal (nXII) and Roller nucleus. CSF-cN axons wrap around the nXII in a remarkably precise manner, while also innervate the core of the Roller. XII motoneurons modulate tongue movement and are output of the rhythmic network that control breathing. Opposing, Roller nucleus has been poorly studied. The analysis of genetic Synaptophysin-Tomato puncta identified that CSF-cNs form profuse GABAergic synapses onto ventral nXII motoneurons and Dbx1-derived Roller neurons. Moreover, optogenetic stimulation of CSF-cNs evoked inhibitory postsynaptic currents in Roller neurons, confirming functional connections. We propose that CSF-cNs may regulate respiratory activity through these nuclei, according to CSF homeostasis. Altogether, our results uncover a novel connectivity map of CSF-cNs in the mammalian brainstem, enlightening previously unknown circuits that modulate autonomic functions.