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The consummatory components of ingestion and rejection, organized in the caudal brainstem, include licking, swallowing, and the oral phase of rejection (gaping). Studies employing electrical-stimulation induced motor activity have localized interneurons controlling these complex motor patterns to the medullary reticular formation (RF), but the characteristics of these neurons during more naturally induced behavior are unknown. The purpose of the present study was to record the activity profiles of RF neurons during licking, swallowing, and oral rejection in response to gustatory stimulation. Two-hundred and two neurons recorded from awake, freely moving rats were broadly classified as orally related (67%) or non-orally related (33%). Orally related neurons included a large number that were rhythmically active during licking (n = 76; 38%). These "lick-rhythmic" neurons were widely distributed in the RF, but were concentrated in the caudal medullary reticular formation adjacent to the hypoglossal nucleus (Probst's region) and further rostral in the intermediate zone (IRt) of the RF. An analysis of autocorrelations determined that lick-rhythmic neurons in these regions were more closely coupled to licking than to lick-rhythmic neurons more lateral in the parvocellular RF (PCRt). In addition to neurons with weak lick-rhythmic activity, the PCRt also contained a disproportionate number of neurons with orosensory or mixed oro-sensorimotor properties. These data provide evidence for functional specialization within different regions of the medullary RF. A high proportion of lick-rhythmic neurons also showed differential activity associated with swallowing (41%) and/or gaping (75%), further suggesting that the different components of ingestion and rejection share brainstem substrates instead of being produced by unique subsets of interneurons.

1. 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)