Multifunctional properties of ambiguous neurons identified electrophysiologically during vocalization in the awake monkey

Abstract

1. The nucleus ambiguus (NA) of the medulla contains motoneurons (MNs) for muscles of the larynx, palate, pharynx, and esophagus. Previous studies in anesthetized animals have demonstrated neural discharge correlated closely with respiration, swallowing, and electrical stimulation-elicited vocalization. A preliminary study confirming the above findings was done by recording NA motoneuron extracellular potentials from awake vocalizing monkeys. The present study was undertaken to quantitatively describe discharge properties of a large number of NA neurons recorded from awake, vocalizing monkeys (Macaca nemestrina). 2. In monkeys trained to vocalize for a food reward, extracellular recordings of neurons in and around the nucleus ambiguus were correlated with laryngeal electromyographic activity during vocalization. A nerve cuff electrode on the ipsilateral recurrent laryngeal nerve allowed identification of laryngeal MNs by antidromic activation of laryngeal MNs and the collision test. 3. Most laryngeal MNs became active 100-200 ms before vocalization. They ceased discharging during or immediately after vocalization. Some MNs discharged in close synchrony with bursts of EMG associated with variations in the vocalization. The mean discharge rate of MNs during vocalization was 18 Hz, and the maximum rate in many cells was over 100 Hz. MNs were also active during swallowing. One MN was related only to respiration and one exclusively to swallowing. 4. Some non-motoneurons (Non-MNs) and cells that may possibly be MNs (PossMNs), recorded in and near the NA, showed properties similar to MNs. Many (147) were active only with vocalization, whereas others were active with swallowing (23); respiration (9); vocalization and swallowing (32); vocalization and respiration (40); or vocalization, swallowing, and respiration (17). 5. The present study demonstrates the importance of studying laryngeal MNs in the chronic preparation. Namely, it is shown that both MNs and Non-MNs of the NA are active with more than one activity. Moreover, some Non-MNs are active for only one activity, e.g., vocalization or swallowing. These findings imply the existence of subsets of medullary neurons involved in multiple behaviors for control of generalized laryngeal functions and other subsets related to specific behaviors.