HYPOGLOSSAL NEURAL ACTIVITY DURING INGESTION AND REJECTION IN THE AWAKE RAT

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 (X(lick) +/- 59 ms; X(gape) +/- 134 ms, means +/- SD), GEN (X(lick) +/- 77 ms; X(gape) +/- 200 ms), and STY (X(lick) +/- 93 ms; X(gape) +/- 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. There was a significant positive correlation between the number of spikes/lick and spikes/swallow but no predictable relationship between either the number of spikes/lick and spikes/gape or between spikes/swallow and spikes/gape. Thus, although the lick-swallow sequence and the gape response have opposite behavioral functions, the magnitude of activity within a single mXII motoneuron during ingestion is not a good predictor of its activity during rejection. 5. Vector plots representing the magnitude and phase of single neuron activity during lick cycles produced a distribution with little overlap between neurons classified as protrudor-related, and those classified as retractor-related. During gape cycles, many mXII neurons exhibited a phase shift in their peak firing relative to AD. This produced a distribution of neurons in the vector plot that corresponded to the three-phase sequence of lingual coactivation (phase I), protrusion (phase II), and retraction (phase III). 6. Although all of the mXII cells that were recorded in the present study were active during rhythmic licking, only subsets of cells responded differentially during swallows and gapes. The central pattern generators for generating lick cycles and swallows are located in the brain stem and share a common final pathway that include the oromotor nuclei. The switch in the motor program from ingestion to rejection involves both excitation and suppression of subsets of mXII cells as well as a shift in the firing patterns to produce the proper sequencing of lingual muscle activation to expel unwanted fluid from the oral cavity.