The physiological motor patterns produced by neurons in the nucleus retroambiguus in the rat and their modulation by vagal, peripheral chemosensory, and nociceptive stimulation

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The nucleus retroambiguus (NRA) is a neuronal cell group in the ventrolateral tegmental field, rostrocaudally between the obex and the first cervical spinal segment (Holstege, 1989; 1991; Holstege, Kerstens, Moes, & Vanderhorst, 1997). NRA‐neurons maintain direct bilateral fiber projections via a contralateral pathway to the motoneurons innervating soft palate, pharynx, larynx, intercostal, diaphragm, abdominal, and pelvic floor muscles (de Almeida and Kirkwood, 2013; Holstege, 1989; Holstege, Graveland, Bijker‐Biemond, & Schuddeboom, 1983; Holstege & Tan, 1987; Holstege, van Neerven, & Evertse, 1987). These muscles determine the pharyngeal, laryngeal, intrathoracic, intra‐abdominal, and intrapelvic pressure. In many studies, the NRA is thought to be part of the caudal respiratory group (Ellenberger & Feldman, 1990; Ezure, Manabe, & Yamada, 1988; Jones, Saad, Lewis, & Merrill, 1970; Jones, Stanic, & Dutschmann, 2015; Subramanian, & Dutschmann, 2012), but the NRA not only controls respiration (Subramanian & Holstege, 2009) but also vomiting (Miller, Nonaka, Siniaia, & Jakus, 1995), parturition and all other motor activities which need changes in the thoracic, abdominal, and pelvic pressure (Holstege, 2014; Holstege & Subramanian, 2016; Subramanian & Holstege, 2009). Moreover, the NRA‐premotor interneurons also project to motoneurons in the lumbosacral spinal cord involved in generating the posture necessary for mating in cat (Boers et al., 2005; Holstege, 2014; Vanderhorst & Holstege, 1995), hamster (Gerrits & Holstege, 1999), and monkey (Vanderhorst, Terasawa, Ralston, & Holstege, 2000a).
The periaqueductal gray (PAG) also uses the NRA premotor interneurons to generate vocalization in the cat (Holstege, 1989; Subramanian & Holstege, 2009; Zhang, Bandler, & Davis, 1995), monkey (Jürgens, 2009), and in the songbird (Schmidt & Wild, 2014). In humans, the PAG‐NRA pathway represents the sound part of human speech (Holstege & Subramanian, 2016), which includes changes in respiration frequency (Subramanian, Balnave, & Holstege, 2008; Subramanian & Holstege, 2009).
To understand the physiology of individual NRA neurons, it is necessary to know how the multiple NRA motor systems operate. In an earlier study in cat, Subramanian and Holstege (2009) showed how the NRA is involved in respiratory and laryngeal modulation during vocal behavior. In the current study, we investigated the single activity patterns of NRA neurons and the NRA neuronal responses to afferent feedback loops via vagal, peripheral chemosensory and nociceptive pathways. In addition, we examined the functional topography within the NRA for the respiratory, laryngeal and pelvic floor control systems. With this comprehensive approach, we aim to establish not only the evolutionary perspectives of the NRA across species but also data for using the rat as a model for future investigations of the PAG‐NRA pathway within the emotional motor system (Holstege, 1992).
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