CNS innervation of airway-related parasympathetic preganglionic neurons: a transneuronal labeling study using pseudorabies virus

Haxhiu, Musa A.; Jansen, A.S.P.; Cherniack, Neil S.; Loewy, A.

doi:10.1016/0006-8993(93)90435-p

Cited by 161 publications

(106 citation statements)

References 86 publications

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“…The results of the present study showed that retrogradely labeled AVPNs do not express NADPH diaphorase reaction. However, strongly positive NADPH diaphorase neurons were observed in other medullary regions, including the nucleus tractus solitarius and ventral portion of the gigantocellular nucleus that provide afferent innervation to AVPNs (21,27). In the present study, comparable results were obtained using NADPH-diaphorase staining and NOS immunoreactivity, which indicates that NADPH-diaphorase staining reflects the presence of neuronal NOS (25,60).…”

Section: Discussionsupporting

confidence: 83%

“…Recent studies indicate that the iNANC system employs vasoactive intestinal peptide (VIP) (7,16,22,38,47,57), nitric oxide (NO) (4, 30, 36, 44, 51), or both (6, 14 -16, 64) to elicit ASM relaxation. However, the preganglionic origin of neurons containing these relaxing molecules has not been established.The preganglionic motor innervation of the airways arises from the nucleus ambiguus and from the most rostral part of the dorsal motor nucleus of the vagus (DMV) (21,23,27,29,34). Inputs from these preganglionic neurons are carried by the vagal fibers that are thought to synapse with airway ganglionic cells, which in turn modify and distribute central parasympathetic outflow to the effector organs of the airways and lungs (54, 59).…”

mentioning

confidence: 99%

“…The preganglionic motor innervation of the airways arises from the nucleus ambiguus and from the most rostral part of the dorsal motor nucleus of the vagus (DMV) (21,23,27,29,34). Inputs from these preganglionic neurons are carried by the vagal fibers that are thought to synapse with airway ganglionic cells, which in turn modify and distribute central parasympathetic outflow to the effector organs of the airways and lungs (54, 59).…”

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Chemical profile of vagal preganglionic motor cells innervating the airways in ferrets: the absence of noncholinergic neurons

Mayer

Haxhiu

2004

Journal of Applied Physiology

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Kc, Prabha, Catherine A. Mayer, and Musa A. Haxhiu. Chemical profile of vagal preganglionic motor cells innervating the airways in ferrets: the absence of noncholinergic neurons. J Appl Physiol 97: 1508 -1517, 2004; 10.1152/japplphysiol.00282.2004.-In ferrets, we investigated the presence of choline acetyltransferase (ChAT), vasoactive intestinal peptide (VIP), and markers for nitric oxide synthase (NOS) in preganglionic parasympathetic neurons innervating extrathoracic trachea and intrapulmonary airways. Cholera toxin ␤-subunit, a retrograde axonal transganglionic tracer, was used to identify airway-related vagal preganglionic neurons. Double-labeling immunohistochemistry and confocal microscopy were employed to characterize the chemical nature of identified airway-related vagal preganglionic neurons at a single cell level. Physiological experiments were performed to determine whether activation of the VIP and ChAT coexpressing vagal preganglionic neurons plays a role in relaxation of precontracted airway smooth muscle tone after muscarinic receptor blockade. The results showed that 1) all identified vagal preganglionic neurons innervating extrathoracic and intrapulmonary airways are acetylcholine-producing cells, 2) cholinergic neurons innervating the airways coexpress ChAT and VIP but do not contain NOS, and 3) chemical stimulation of the rostral nucleus ambiguus had no significant effect on precontracted airway smooth muscle tone after muscarinic receptor blockade. These studies indicate that vagal preganglionic neurons are cholinergic in nature and coexpress VIP but do not contain NOS; their stimulation increases cholinergic outflow, without activation of inhibitory nonadrenergic, noncholinergic ganglionic neurons, stimulation of which induces airway smooth muscle relaxation. Furthermore, these studies do not support the possibility of direct inhibitory innervation of airway smooth muscle by vagal preganglionic fibers that contain VIP.central nervous system control of the airways; parasympathetic preganglionic neurons; choline acetyl transferase; vasoactive intestinal peptide; nitric oxide synthase; nucleus ambiguus; airway constriction; airway dilation IN MANY SPECIES, INCLUDING HUMANS, airway smooth muscle (ASM) tone critically relies on the balance between central excitatory cholinergic control (3,19,33,49) and the inhibitory nonadrenergic, noncholinergic (iNANC) influences (2,12,17,47,56). Activation of cholinergic preganglionic neurons produces airway constriction, submucosal gland secretion and increased blood flow using acetylcholine as a neurotransmitter (23,25,26). In the presence of cholinergic and sympathetic blockade, stimulation of vagal nerves, either by electrical current or via neural reflex pathways, elicits relaxation of preconstricted ASM cells via activation of iNANC pathways (2,12,17,56). Recent studies indicate that the iNANC system employs vasoactive intestinal peptide (VIP) (7,16,22,38,47,57), nitric oxide (NO) (4, 30, 36, 44, 51), or both (6, 14 -16, 64) to elicit ASM relaxation. Ho...

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Section: Discussionsupporting

confidence: 83%

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confidence: 99%

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confidence: 99%

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Chemical profile of vagal preganglionic motor cells innervating the airways in ferrets: the absence of noncholinergic neurons

Mayer

Haxhiu

2004

Journal of Applied Physiology

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“…Bronchial and pulmonary C-fibre afferents terminate in the nucleus tractus solitarius (Kubin et al, 1991) and preganglionic pulmonary vagal motoneurones are found in the nucleus ambiguus and dorsal vagal nucleus (Kalia, 1981). As well as the nucleus tractus solitarius, projections to preganglionic pulmonary vagal neurones also come from the raphe obscurus and ventral lateral medulla (Haxhiu et al, 1993). In addition, chemical stimulation of the ventral surface increases activity in pulmonary vagal motoneurones (Haxhiu et al, 1987).…”

Section: Discussionmentioning

confidence: 99%

Involvement of central 5‐HT_1A receptors in the reflex activation of pulmonary vagal motoneurones by inhaled capsaicin in anaesthetized cats

Bootle

Adcock

Ramage

1996

British J Pharmacology

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1 The aim of the present experiments was to determine whether 5-HTIA receptors play a role in the control of the reflex activation of pulmonary vagal motoneurones. This was carried out by investigating the effects of intracisternal injections (i.c.) of the 5-HTIA receptor ligands, 8-OH-DPAT (50 ,ug kg-'), buspirone (200 ug kg-'), WAY-100635 (100 Mg kg-'), methiothepin (200 Mg kg-') and (-)-pindolol (100 Mg kg-') and the 5-HT2 receptor antagonist, cinanserin (200 ug kg-'), on the reflex bronchoconstriction evoked by inhaled capsaicin aerosol in a-chloralose anaesthetized, neuromuscularly blocked and artificially ventilated cats. Recordings were made of heart rate, blood pressure and upper tracheal pressure.2 Central application of all the 5-HTIA receptor antagonists (methiothepin, WAY-100635 and (-)-pindolol) attenuated the reflex bronchoconstriction in the upper trachea. However, the same dose of WAY-100635 given i.v. had no effect on this reflex bronchoconstriction. The 5-HTlA receptor agonist, 8-OH-DPAT (50 Mg kg-') given i.c., potentiated the capsaicin-evoked reflex bronchoconstriction, whereas buspirone (200 Mg kg-') i.c. had no effect. The 5-HT2 receptor antagonist, cinanserin (200 Mg kg-') also had no effect. 3 It is concluded that the reflex excitation of pulmonary vagal motoneurones by inhaled capsaicin in achloralose anaesthetized cats involves the activation of central 5-HTIA receptors.

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“…In rats (Haxhiu et al, 1993), as in other species (reviewed in Kalia, 1987;Jordan, 2001;Haxhiu et al, 2005), the motor preganglionic component of the network innervating the airways arises mainly from the nucleus ambiguus and to a lesser extent from the dorsal motor nucleus of the vagus (DMV). Of these two groups of neurons, AVPNs within the rostral nucleus ambiguus (rNA) play a greater role in generating cholinergic outflow to airway smooth muscle (Haselton et al, 1992), secretory glands, and blood vessels .…”

Section: Introductionmentioning

confidence: 99%

Airway-related vagal preganglionic neurons express multiple nicotinic acetylcholine receptor subunits

Dehkordi

Balan

et al. 2006

Autonomic Neuroscience

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Nicotine acting centrally increases bronchomotor tone and airway secretion, suggesting that airwayrelated vagal preganglionic neurons (AVPNs) within the rostral nucleus ambiguus (rNA) express nicotinic acetylcholine receptors (nAChRs). In the present study, we examined the three main functionally characterized subtypes of nAChRs in the CNS, the α7 homomeric and α4β2 heteromeric receptors. First, we characterized the expression of these subunits at the message (mRNA) and protein levels in brain tissues taken from the rNA region, the site where AVPNs are located. In addition, double labeling fluorescent immunohistochemistry and confocal laser microscopy were used to define the presence of α7, α4, and β2 nAChRs on AVPNs that were retrogradely labeled with cholera toxin h subunit (CTb), injected into the upper lung lobe (n = 4) or extrathoracic trachea (n = 4). Our results revealed expression of all three studied subunits at mRNA and protein levels within the rNA region. Furthermore, virtually all identified AVPNs innervating intrapulmonary airways express α7 and α4 nAChR subunits. Similarly, a majority of labeled AVPNs projecting to extrathoracic trachea contain α7 and β2 subunits, but less than half of them show detectable α4 nAChR traits. These results suggest that AVPNs express three major nAChR subunits (α7, α4, and β2) that could assemble into functional homologous or heterologous pentameric receptors, mediating fast and sustained nicotinic effects on cholinergic outflow to the airways.

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CNS innervation of airway-related parasympathetic preganglionic neurons: a transneuronal labeling study using pseudorabies virus

Cited by 161 publications

References 86 publications

Chemical profile of vagal preganglionic motor cells innervating the airways in ferrets: the absence of noncholinergic neurons

Chemical profile of vagal preganglionic motor cells innervating the airways in ferrets: the absence of noncholinergic neurons

Involvement of central 5‐HT_1A receptors in the reflex activation of pulmonary vagal motoneurones by inhaled capsaicin in anaesthetized cats

Airway-related vagal preganglionic neurons express multiple nicotinic acetylcholine receptor subunits

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CNS innervation of airway-related parasympathetic preganglionic neurons: a transneuronal labeling study using pseudorabies virus

Cited by 161 publications

References 86 publications

Chemical profile of vagal preganglionic motor cells innervating the airways in ferrets: the absence of noncholinergic neurons

Chemical profile of vagal preganglionic motor cells innervating the airways in ferrets: the absence of noncholinergic neurons

Involvement of central 5‐HT1A receptors in the reflex activation of pulmonary vagal motoneurones by inhaled capsaicin in anaesthetized cats

Airway-related vagal preganglionic neurons express multiple nicotinic acetylcholine receptor subunits

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Involvement of central 5‐HT_1A receptors in the reflex activation of pulmonary vagal motoneurones by inhaled capsaicin in anaesthetized cats