Modification in activity of medullary respiratory-related neurons for vocalization and swallowing

1. The medullary ventral respiratory group (VRG) in and near the nucleus ambiguous contains neurons related to respiration. Also found here are neurons related to vocalization and swallowing as well as motoneurons of laryngeal, pharyngeal, palatal, and esophageal muscles. Previous reports in anesthetized animals have characterized discharge properties of neurons as they relate to a single behavior, e.g., respiration. Relatively few studies have documented discharge properties during more than one behavior, e.g., respiration and swallowing. Neurons were recorded extracellularly from awake Macaca nemestrina monkeys engaged in a vocalization task. The present paper describes how respiratory-related neurons (RRNs) modify their discharge during vocalization and swallowing. 2. The temporal relation between vocalization, subglottal pressure (SP), and diaphragm electromyogram (EMG) was established from recordings in anesthetized monkeys. Vocalization was elicited by electrical stimulation of the midbrain periaqueductal gray (PAG). Vocalization is preceded by deep inspiration and a brief pause in diaphragm EMG and begins with a rapid increase in positive SP. 3. Extracellularly recorded neural potentials from the VRG in three awake monkeys were related to respiration by correlating their discharge with EMGs from the posterior cricoarytenoid or intercostal muscles during quiet respiration. Neurons were classified as inspiratory (INSP; N = 27), phase spanning (PS; N = 20), or expiratory (N = 6) on this basis. 4. A fourth category of cells was defined as a subgroup of INSP cells on the basis of their discharge during vocalization. This group, inspiratory-pause (INSP-PS; N = 10), paused for ~100 ms just before vocalization and resumed their activity during vocalization. 5. Of 63 fully analyzed RRNs, 40 (63%) also modulated their activity with vocalization and 3 (5%) with swallowing. Thirteen (21%) RRNs modulated with vocalization, respiration, and swallowing. Seven (11%) cells were modulated only with respiration. 6. Most cells demonstrated a shorter period of activity and a higher discharge rate associated with vocalization in comparison with quiet respiration. Six (30%) of the PS cells demonstrated an augmenting discharge pattern before vocalization, which was different from the other PS cells and different from their pattern during quiet respiration. Thirteen RRNs showed a pause in activity during vocal fold closure associated with swallowing, whereas three cells gave a burst at this time. 7. The higher discharge rate and shorter burst duration preceding vocalization, compared with quiet respiration, may be related to the greater positive SP necessary to support vocalization. 8. The pause in the activity of the INSP-PS cells appears to be part of a coordinated pattern related to cessation of inspiration and vocal fold adduction accompanying vocalization. 9. RRNs that pause during swallowing may be related to inhibition of other RRNs during the swallow. RRNs that burst during swallowing may receive inputs from laryngeal afferents or may be related to contraction of pharyngeal muscles during the swallow. 10. The augmenting pattern of PS cells before vocalization is similar to patterns of midbrain PAG cells before vocalization. Medullary PS cells, as well as other medullary RRNs modulating with vocalization, may be influenced by PAG projections.