Pulmonary C-fiber receptor activation abolishes uncoupled facial nerve activity from phrenic bursting during positive end-expired pressure in the rat

Abstract

Phasic respiratory bursting in the facial nerve (FN) can be uncoupled from phrenic bursting by application of 9 cmH(2)O positive end-expired pressure (PEEP). This response reflects excitation of expiratory-inspiratory (EI) and preinspiratory (Pre-I) facial neurons during the Pre-I period and inhibition of EI neurons during inspiration (I). Because activation of pulmonary C-fiber (PCF) receptors can inhibit the discharge of EI and Pre-I neurons, we hypothesized that PCF receptor activation via capsaicin would attenuate or abolish uncoupled FN bursting with an increase from 3 cmH(2)O (baseline) to 9 cmH(2)O PEEP. Neurograms were recorded in the FN and phrenic nerve in anesthetized, ventilated, vagally intact adult Wistar rats. Increasing PEEP to 9 cmH(2)O resulted in a persistent rhythmic discharge in the FN during phrenic quiescence (i.e., uncoupled bursting). Combination of PEEP with intrajugular capsaicin injection severely attenuated or eliminated uncoupled bursting in the FN (P < 0.05). Additional experiments examined the pattern of facial motoneuron (vs. neurogram) bursting during PEEP application and capsaicin treatment. These single-fiber recordings confirmed that Pre-I and EI (but not I) neurons continued to burst during PEEP-induced phrenic apnea. Capsaicin treatment during PEEP substantially inhibited Pre-I and EI neuron discharge. Finally, analyses of FN and motoneuron bursting across the respiratory cycle indicated that the inhibitory effects of capsaicin were more pronounced during the Pre-I period. We conclude that activation of PCF receptors can inhibit FN bursting during PEEP-induced phrenic apnea by inhibiting EI and I facial motoneuron discharge.

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).…”