Excitation of dorsal and ventral respiratory group neurons by phrenic nerve afferents

Speck, D. F.; Revelette, W. R.

doi:10.1152/jappl.1987.62.3.946

Cited by 32 publications

(20 citation statements)

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“…However, in a few supplemental experiments, we could not detect any rapid (i.e., within 1-3 breaths) changes in the EMG activity of the contralateral hemidiaphragm or external intercostal muscles following phrenicotomy. Phrenic afferents are also capable of exerting excitatory effects on supraspinal respiratory neurons (44). Consistent with this notion, we noted that phrenicotomy induced immediate changes in respiratory frequency in uninjured rats.…”

Section: Discussionsupporting

confidence: 86%

Contribution of the spontaneous crossed-phrenic phenomenon to inspiratory tidal volume in spontaneously breathing rats

Dougherty

Lee

Lane

et al. 2012

Journal of Applied Physiology

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Dougherty BJ, Lee KZ, Lane MA, Reier PJ, Fuller DD. Contribution of the spontaneous crossed-phrenic phenomenon to inspiratory tidal volume in spontaneously breathing rats. J Appl Physiol 112: 96-105, 2012. First published October 27, 2011 doi:10.1152/japplphysiol.00690.2011Spinal cord hemisection at C2 (C2HS) severs bulbospinal inputs to ipsilateral phrenic motoneurons causing transient hemidiaphragm paralysis. The spontaneous crossed-phrenic phenomenon (sCPP) describes the spontaneous recovery of ipsilateral phrenic bursting following C2HS. We reasoned that the immediate (next breath) changes in tidal volume (VT) induced by ipsilateral phrenicotomy during spontaneous breathing would provide a quantitative measure of the contribution of the sCPP to postinjury VT. Using this approach, we tested the hypothesis that the sCPP makes more substantial contributions to VT when respiratory drive is increased. Pneumotachography was used to measure VT in anesthetized, spontaneously breathing adult male rats at intervals following C2HS. A progressive increase in VT (ml/breath) occurred over an 8 wk period following C2HS during both poikilocapnic baseline breathing and hypercapnic respiratory challenge (7% inspired CO2). The sCPP did not impact baseline breathing at 1-3 days postinjury since VT was unchanged after ipsilateral phrenicotomy. However, by 2 wk post-C2HS, baseline phrenicotomy caused a 16 Ϯ 2% decline in VT; a comparable 16 Ϯ 4% decline occurred at 8 wk. Contrary to our hypothesis, the phrenicotomy-induced declines in VT (%) during hypercapnic respiratory stimulation did not differ from the baseline response at any postinjury time point (all P Ͼ 0.11). We conclude that by 2 wk post-C2HS the sCPP makes a meaningful contribution to VT that is similar across different levels of respiratory drive. plasticity; hemisection; phrenicotomy; cervix SEVERING IPSILATERAL BULBOSPINAL inputs to phrenic motoneurons via lateral hemisection of the C2 spinal cord (C2HS) transiently paralyzes the hemidiaphragm (22,23,27,48). However, a partial return of ipsilateral phrenic motoneuron inspiratory bursting occurs over a period of weeks to months following C2HS (14,15,20,37). This response has been termed the spontaneous crossed-phrenic phenomenon (sCPP; Refs. 22,28,40). The sCPP provides an important experimental model of neuroplasticity and associated functional recovery (i.e., phrenic bursting) after spinal cord injury (22,28,40). However, the functional contribution of the sCPP to ventilation (V E) has not been definitively established. In other words, it is unclear if the relatively small amount of electrical activity that has been measured in the ipsilateral phrenic nerve after chronic C2HS is sufficient to alter inspiratory tidal volume (V T ). Thus it is unknown if C2HS-induced, spontaneous neuroplastic changes associated with the sCPP (22, 23) have a meaningful impact on the respiratory system (20).The functional impact of the sCPP has been examined to a limited extent (14,15,20). Correlations between phrenic nerve activity ...

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Section: Discussionsupporting

confidence: 86%

Contribution of the spontaneous crossed-phrenic phenomenon to inspiratory tidal volume in spontaneously breathing rats

Dougherty

Lee

Lane

et al. 2012

Journal of Applied Physiology

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“…Since 5-HT does not cross the blood-brain barrier [26], increase in central inspiratory drive cannot be ascribed to any direct action of this agent on medullary respiratory neurons. Diaphragmatic afferents were still present in all animals of the present study, and some observations in cats [25] and dogs [10] have shown that their activation by the increase in strength of diaphragmatic contraction, as produced by resistive loading, exerts facilitatory influences on the respiratory centers.…”

Section: Changes In Central Inspiratory Drivesupporting

confidence: 53%

Comparisons among external resistive loading, drug-induced bronchospasm, and dense gas breathing in cats: Roles of vagal and spinal afferents

Barrière¹,

Delpierre²,

Volgo³

et al. 1993

Lung

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In anesthetized cats, breathing spontaneously, increase in lung resistance (RL) was induced by either external resistive loads (ERL) or internal loading produced by dense gas breathing (sulfur hexafluoride, SF6) or serotonin (5-HT)-induced bronchoconstriction. The 3 test agents were used in each animal. Arterial blood gases were maintained in the normal range. Ventilatory and cardiovascular responses were studied in 3 groups of animals: intact, vagotomized, or spinalized at C8 level, a condition that preserved diaphragmatic afferents. In intact or spinal animals, ERL as well as SF6 inhalation lengthened the inspiratory and/or the expiratory periods, whereas 5-HT injections elicited rapid shallow breathing. The changes in ventilatory timing with either type of load were not observed in vagotomized cats. In all animals, ERL breathing or 5-HT injections increased the moving-time average of diaphragmatic EMG measured at constant time (Edi 0.1 and 0.5 secs), but this was not observed during SF6 inhalation, a condition in which the magnitude of RL increase was less than in the 2 other situations. The changes in systemic arterial blood pressure and/or cardiac frequency were mostly associated with 5 HT-induced bronchoconstriction. They persisted in spinalized cats, but were not observed or reversed in vagotomized ones. These observations demonstrate that vagal afferents play a major role in the changes in ventilatory timing and cardiovascular function in response to both external or internal moderate resistive loading. The existence of Edi changes in the 3 groups of cats suggests also that diaphragmatic afferents, preserved in both situations, are involved in this response.

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“…On the other hand, activation of phrenic afferents may stimulate breathing in some cases. Speck and Revellete (64) showed that about one-fourth of dorsal respiratory group respiratory-modulated neurons are excited by phrenic afferents. Based on conduction velocity measurements, they attributed this effect to activation of predominantly small, type III myelinated fibers.…”

Section: Axotomy Of Phrenic Motoneurons and Afferent Neurons: Potentimentioning

confidence: 99%

Phrenicotomy alters phrenic long-term facilitation following intermittent hypoxia in anesthetized rats

Sandhu

Lee

Fregosi

et al. 2010

Journal of Applied Physiology

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Sandhu MS, Lee KZ, Fregosi RF, Fuller DD. Phrenicotomy alters phrenic long-term facilitation following intermittent hypoxia in anesthetized rats. J Appl Physiol 109: 279 -287, 2010. First published April 15, 2010 doi:10.1152/japplphysiol.01422.2009 can induce a persistent increase in neural drive to the respiratory muscles known as long-term facilitation (LTF). LTF of phrenic inspiratory activity is often studied in anesthetized animals after phrenicotomy (PhrX), with subsequent recordings being made from the proximal stump of the phrenic nerve. However, severing afferent and efferent axons in the phrenic nerve has the potential to alter the excitability of phrenic motoneurons, which has been hypothesized to be an important determinant of phrenic LTF. Here we test the hypothesis that acute PhrX influences immediate and long-term phrenic motor responses to hypoxia. Phrenic neurograms were recorded in anesthetized, ventilated, and vagotomized adult male rats with intact phrenic nerves or bilateral PhrX. Data were obtained before (i.e., baseline), during, and after three 5-min bouts of isocapnic hypoxia. Inspiratory burst amplitude during hypoxia (%baseline) was greater in PhrX than in phrenic nerve-intact rats (P Ͻ 0.001). Similarly, burst amplitude 55 min after IH was greater in PhrX than in phrenic nerve-intact rats (175 Ϯ 9 vs. 126 Ϯ 8% baseline, P Ͻ 0.001).In separate experiments, phrenic bursting was recorded before and after PhrX in the same animal. Afferent bursting that was clearly observable in phase with lung deflation was immediately abolished by PhrX. The PhrX procedure also induced a form of facilitation as inspiratory burst amplitude was increased at 30 min post-PhrX (P ϭ 0.01 vs. pre-PhrX). We conclude that, after PhrX, axotomy of phrenic motoneurons and, possibly, removal of phrenic afferents result in increased phrenic motoneuron excitability and enhanced LTF following IH. axotomy; phrenic motoneurons; plasticity EXPOSURE TO INTERMITTENT HYPOXIA (IH) over short periods (e.g., minutes to hours) can evoke a persistent increase in respiratory motor output, termed long-term facilitation (LTF) (35,48,50). LTF has been observed in awake (26, 35) and sleeping humans (53) and in a wide range of animal species (22,46,48). The mechanisms underlying LTF have been studied extensively over the last 10 -15 years, primarily in anesthetized animals (reviewed in Refs. 42,49,50). In anesthetized animals, LTF is typically manifest as an increase in the inspiratory burst amplitude of phrenic (19) and/or hypoglossal (XII) extracellular nerve recordings (20). Recordings of in vivo (19) and in vitro (10) respiratory motor LTF are typically made from cut respiratory muscle nerves. More specifically, the phrenic and/or XII nerves are cut, and subsequent extracellular recordings are made from the central end of the nerve. This procedure can provide stability to the neurophysiological recording procedures, particularly when a dorsal surgical approach is used, but also has the potential to alter respiratory motor output and...

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Excitation of dorsal and ventral respiratory group neurons by phrenic nerve afferents

Cited by 32 publications

References 0 publications

Contribution of the spontaneous crossed-phrenic phenomenon to inspiratory tidal volume in spontaneously breathing rats

Contribution of the spontaneous crossed-phrenic phenomenon to inspiratory tidal volume in spontaneously breathing rats

Comparisons among external resistive loading, drug-induced bronchospasm, and dense gas breathing in cats: Roles of vagal and spinal afferents

Phrenicotomy alters phrenic long-term facilitation following intermittent hypoxia in anesthetized rats

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