Uncoupling of upper airway motor activity from phrenic bursting by positive end-expired pressure in the rat

Abstract

Lee K-Z, Fuller DD, Tung L-C, Lu I-J, Ku L-C, Hwang J-C. Uncoupling of upper airway motor activity from phrenic bursting by positive end-expired pressure in the rat. J Appl Physiol 102: [878][879][880][881][882][883][884][885][886][887][888][889] 2007. First published November 2, 2006; doi:10.1152/japplphysiol.00934.2006.-Phasic bursting in the hypoglossal nerve can be uncoupled from phrenic bursting by application of positive end-expired pressure (PEEP). We wished to determine whether similar uncoupling can also be induced in other respiratory-modulated upper airway (UAW) motor outputs. Discharge of the facial, hypoglossal, superior laryngeal, recurrent laryngeal, and phrenic nerves was recorded in anesthetized, ventilated rats during stepwise changes in PEEP with a normocapnic, hyperoxic background. Application of 3-to 6-cmH 2O PEEP caused the onset inspiratory (I) UAW nerve bursting to precede the phrenic burst but did not uncouple bursting. In contrast, application of 9-to 12-cmH2O PEEP uncoupled UAW neurograms such that rhythmic bursting occurred during periods of phrenic quiescence. Single-fiber recording experiments were conducted to determine whether a specific population of UAW motoneurons is recruited during uncoupled bursting. The data indicate that expiratory-inspiratory (EI) motoneurons remained active, while I motoneurons did not fire during uncoupled UAW bursting. Finally, we examined the relationship between motoneuron discharge rate and PEEP during coupled UAW and phrenic bursting. EI discharge rate was linearly related to PEEP during preinspiration, but showed no relationship to PEEP during inspiration. Our results demonstrate that multiple UAW motor outputs can be uncoupled from phrenic bursting, and this response is associated with bursting of EI nerve fibers. The relationship between PEEP and EI motoneuron discharge rate differs during preinspiratory and I periods; this may indicate that bursting during these phases of the respiratory cycle is controlled by distinct neuronal outputs. uncoupled activity; motoneurons; expiratory-inspiratory; preinspiratory THE MAMMALIAN UPPER AIRWAY (UAW) consists of the airflow passages extending from the trachea to the external nares and is thus composed of the nasal cavity, pharynx, and larynx (34). The compliance and geometry of this region are influenced by a number of skeletal muscles. Among them are the alae nasi, tongue, and laryngeal muscles, which are innervated by the facial (FN), hypoglossal (HN) and superior (SLN), and recurrent laryngeal nerves (RLN), respectively (1,26,41).Many studies have shown that the inspiratory (I) discharge of the HN precedes the phrenic I burst (5,6,13,17,23,33). This preinspiratory (Pre-I) activity has been suggested to benefit UAW patency by dilating and stiffening the UAW before the onset of I airflow (30). Similar to the HN, the onset of FN, SLN, and RLN I bursting occurs before the onset of phrenic bursting (16,25).The respiratory-related discharge of the UAW muscles is influenced by various chemical and mechanical ...

Hypoxia-induced short-term potentiation of respiratory-modulated facial motor output in the rat

“…Based on bursting patterns relative to I phrenic output, Hwang and colleagues categorized VII motoneurons as Pre-I, I, expiratory (E), inspiratory-expiratory (I-E), expiratory-inspiratory (E-I), and tonic (Hwang and St John, 1988; Lee et al, 2008; Lee et al, 2007). The relative contribution of intrinsic neuronal properties (e.g.…”

“…It is clear, however, that Pre-I and I VII motor outputs can respond differently to peripheral inputs. For example, Pre-I and I bursting can be differentially modulated by positive end-expired pressure (PEEP) (Lee et al, 2007) and pulmonary C-fiber activation (Lee et al, 2008). High levels of PEEP eliminates I VII bursting although rhythmic Pre-I VII activity persists (Lee et al, 2007).…”

“…The general procedures have been described previously (Lee and Fuller, 2010; Lee et al, 2008; Lee et al, 2007; Lee et al, 2009). The phrenic nerve was accessed via a ventral approach; the VII nerve was isolated between the nares and the mandible.…”

“…During breathing, VII activity includes both phasic and tonic components (Hwang et al, 1988; Hwang and St John, 1988; Lee et al, 2008; Lee et al, 2007; Onimaru et al, 2006), although this designation may depend on the recording conditions (Bailey et al, 2007). Phasic VII activity can be further categorized as either pre-inspiratory (Pre-I), inspiratory (I), or post-inspiratory (Post-I) based on when bursting occurs in relation to phrenic motor activity (Lee et al, 2008; Lee et al, 2007).…”

“…Phasic VII activity can be further categorized as either pre-inspiratory (Pre-I), inspiratory (I), or post-inspiratory (Post-I) based on when bursting occurs in relation to phrenic motor activity (Lee et al, 2008; Lee et al, 2007). Although hypoxia-induced neuroplasticity of I phrenic and hypoglossal motor activity has been extensively investigated (see (Mitchell et al, 2001; Mitchell and Johnson, 2003) for review), the potential for plasticity in upper airway Pre-I bursting has received relatively little attention (Lee and Fuller, 2010).…”