Extracellular activity of swallowing neurons (SN) in the region of the hypoglossal (XIIth) motor nucleus was studied in sheep anesthetized with halothane. Eighty six SN exhibited a discharge closely linked to swallowing electromyographic (EMG) activity of the geniohyoΓ―d (GH) muscle induced by stimulation of the superior laryngeal nerve. Swallowing activation persisted after motor paralysis, indicating that this activity did not result from sensory feedback. SN were classified into two groups. Group I SN (N = 66) discharged a burst of up to 12 spikes for 50-300 ms during the response of GH. Mean frequencies ranged from 10 to 60 Hz, peak instantaneous frequencies from 10 to 100 Hz. Thirty two SN were antidromically activated by stimulating the XIIth nerve. Mean latencies of antidromic spikes were 2.6 ms and 2.4 ms for SN sending their axons in the medial and lateral branches respectively of XIIth nerve, corresponding to conduction velocities of 50.4 m/s and 53.7 m/s. The other 34 group I SN were located at sites with large antidromic field potentials obscuring the identification of unitary antidromic spikes. Thirty group I SN, 16 antidromically activated and 14 in areas with large field potentials, were histologically located in the XIIth motor nucleus between the transverse planes 1 mm caudal to 2 mm rostral to the obex. Group I SN are likely motoneurons supplying GH and tongue musculature. Group II SN (N = 20) were never antidromically activated by XIIth nerve stimulation, and were all located in the reticular formation adjacent to the lateral edge of the XIIth motor nucleus, particularly in transverse planes within 1 mm of the obex.(ABSTRACT TRUNCATED AT 250 WORDS)