The activity of 34 hypoglossal (mXII) neurons was characterized during the ingestion and rejection of gustatory stimuli in the awake rat. Intraoral infusions of water, sucrose, sodium chloride, or hydrochloric acid initiated ingestion responses; infusions of quinine monohydrochloride initiated rejection responses. Electromyographic (EMG) activity from three oropharyngeal muscles monitored the occurrence of lick cycles and swallows (ingestion) and gape cycles (rejection). In addition, the orofacial region was videotaped to provide an independent assessment of lingual and jaw movements in relation to neural activity. 2. EMG activity during lick and gape cycles was quantified by calculating the duration, magnitude, and peak time of muscle contractions. Lick and gape cycles produced highly differentiated patterns of activity from jaw-opener (anterior digastric, AD), lingual protrudor (geniohyoid, GEN), and lingual retractor (styloglossus, STY) muscles. Lick cycles were characterized by an alternating two-phase sequence of protrusion-retraction; gape cycles by an initial coactivation of both lingual muscles (phase I), followed by a sequence of protrusion (phase II) and retraction (phase III). Contraction durations were significantly longer during gape cycles compared with lick cycles for the AD (Xlick +/- 59 ms; Xgape +/- 134 ms, means +/- SD), GEN (Xlick +/- 77 ms; Xgape +/- 200 ms), and STY (Xlick +/- 93 ms; Xgape +/- 220 ms) muscles. 3. Thirty-one out of 34 mXII neurons were functionally classified as protrudor- or retractor-related by cross-correlating anterior digastric EMG activity with neural activity during licking. Fourteen out of 34 neurons were protrudor-related, 17/34 were retractor-related. These classifications were largely consistent with the results from an analysis of a subset of cells (n = 14) that directly compared neural activity with videotaped records of visible tongue movements. 4. The magnitude of mXII activity during ingestion and rejection was compared by determining the mean number of spikes per lick, gape, and swallow for each neuron. Five out of 14 (36%) protrudor-related and 10/17 (59%) retractor-related cells had significant increases in activity during gape responses compared with the number of spikes per lick cycle. This increased activity of mXII neurons was consistent with the more robust lingual motor activity during the gape response. Two protrudor-related and three retractor-related neurons showed significant decreases in activity during gape responses. Although a similar proportion of mXII neurons exhibited decreases in activity during swallows compared with licks (3 protrudor- and 1 retractor-related), fewer mXII neurons (1 protrudor- and 1 retractor-related) showed increased activity during swallows.(ABSTRACT TRUNCATED AT 400 WORDS)