HYPOGLOSSAL NEURAL ACTIVITY DURING INGESTION AND REJECTION IN THE AWAKE RAT

1. The activity of 34 hypoglossal (mXII) neurons was characterized dur ing the ingestion and rejection of gustatory stimuli in the awake rat. Intraoral infusions of water, sucrose, sodium chloride, or hydrochlor ic acid initiated ingestion responses; infusions of quinine monohydroc hloride initiated rejection responses. Electromyographic (EMG) activit y from three oropharyngeal muscles monitored the occurrence of lick cy cles and swallows (ingestion) and gape cycles (rejection). In addition , the orofacial region was videotaped to provide an independent assess ment of lingual and jaw movements in relation to neural activity. 2. E MG activity during lick and gape cycles was quantified by calculating the duration, magnitude, and peak time of muscle contractions. Lick an d gape cycles produced highly differentiated patterns of activity from jaw-opener (anterior digastric, AD), lingual protrudor (geniohyoid, G EN), and lingual retractor (styloglossus, STY) muscles. Lick cycles we re characterized by an alternating two-phase sequence of protrusion-re traction; gape cycles by an initial coactivation of both lingual muscl es (phase I), followed by a sequence of protrusion (phase II)and retra ction (phase III). Contraction durations were significantly longer dur ing gape cycles compared with lick cycles for the AD (X(lick) +/- 59 m s; 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 p rotrudor- 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 cl assifications were largely consistent with the results from an analysi s 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 deter mining the mean number of spikes per lick, gape, and swallow for each neuron. Five out of 14 (36%) protrudor-related and 10/17 (59%) retract or-related cells had significant increases in activity during gape res ponses compared with the number of spikes per lick cycle. This increas ed activity of mXII neurons was consistent with the more robust lingua l motor activity during the gape response. Two protrudor-related and t hree retractor-related neurons showed significant decreases in activit y 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 spi kes/lick and spikes/swallow but no predictable relationship between ei ther the number of spikes/lick and spikes/gape or between spikes/swall ow and spikes/gape. Thus, although the lick-swallow sequence and the g ape response have opposite behavioral functions, the magnitude of acti vity within a single mXII motoneuron during ingestion is not a good pr edictor 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. Duri ng gape cycles, many mXII neurons exhibited a phase shift in their pea k firing relative to AD. This produced a distribution of neurons in th e 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 pres ent study were active during rhythmic licking, only subsets of cells r esponded 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 i nvolves both excitation and suppression of subsets of mXII cells as we ll as a shift in the firing patterns to produce the proper sequencing of lingual muscle activation to expel unwanted fluid from the oral cav ity.