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The Third Nervous System in the Lung

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The Third Nervous System in the Lung Thorax: first published as 10.1136/thx.39.8.561 on 1 August 1984. Downloaded from Thorax 1984;39:561-567 Editorial The third nervous system in the lung: physiology and clinical perspectives The autonomic nervous system controls many are neither adrenergic nor cholinergic were aspects of pulmonary function' and, until recently, it described by Campbell in 1971.4 Since then NANC was thought that this was achieved entirely by means nerves which relax airway smooth muscle have been of classical cholinergic and adrenergic mechanisms. found in several species, including man.55 In these This view has recently been challenged by the studies airway strips are mounted in an organ bath demonstration of a third nervous system in the air- and stimulated by an electrical current that selec- ways (fig). Although the identities of the neuro- tively activates nerves. In guinea pig tracheal strips transmitters in this newly recognised nervous system electrical field stimulation produces an initial con- are not certain, there is increasing evidence that they traction that is blocked by the anticholinergic drug are peptides. This third nervous system is of particu- atropine and therefore due to acetylcholine release lar interest as it is the predominant inhibitory nerv- from cholinergic nerves. The initial contraction is ous pathway to human airway smooth muscle and followed by a relaxation, which is only partially this raises the possibility that a functional defect in inhibited by ,3 adrenergic blockers.56 Thus, although this nervous system might underlie bronchial hyper- a component of the inhibitory response is reactivity in asthma. The recognition that a third adrenergic, there is a component that is non- component of the autonomic nervous system regu- adrenergic. The nerve toxin tetrodotoxin abolishes lates airway smooth muscle tone and other aspects these responses to field stimulation and proves that copyright. of lung physiology has stimulated great interest, they are mediated by nerves (which must be post- since it may provide new insights into diseases such ganglionic), and not due to a direct effect on smooth as asthma and chronic obstructive lung disease, and muscle. Thus guinea pig trachea appears to have may also lead to novel therapeutic approaches. excitatory cholinergic nerves and inhibitory nerves which are both adrenergic and non-adrenergic. In http://thorax.bmj.com/ A third component of the autonomic nervous system similar studies on human airway smooth muscle a cholinergic contractile component is also demon- The existence of a nervous system in the gastrointes- strable, but the inhibitory response is unaffected by tinal tract which is neither adrenergic nor adrenergic blockade.78 This indicates, rather surpris- cholinergic has been established for many years. ingly, that there is no functional sympathetic inner- Non-adrenergic, non-cholinergic (NANC) nerves vation of human airway smooth muscle and that control gut motility and secretions and have been inhibitory nerves are non-adrenergic. The absence demonstrated in vertebrates from fish to man.23 of sympathetic nerves in human airway smooth Indeed, the presence of NANC nerves in primitive muscle is supported by histological studies showing on September 30, 2021 by guest. Protected vertebrates indicates that this nervous system an absence of adrenergic nerve terminals within developed early in evolution. The third nervous sys- smooth muscle,79 by studies showing a lack of effect tem has also been demonstrated in the urogenital of cocaine (a neuronal uptake inhibitor) on norad- tract, the eye, and the cardiovascular system.3 renaline dose-response curves,'0 and by the lack of Because the airways develop embroyologically from effect of tyramine (which directly releases norad- the foregut it is not surprising to find that NANC renaline from nerve terminals) on airway function in nerves are also present in the lung. man." There are, of course, adrenergic receptors in airway smooth muscle,'2 and these are presumably NANC nerves in the airways regulated by circulating adrenaline.'3 NANC nerves appear to be the only neural inhibitory pathway in Inhibitory nerves which relax toad lungs and which human airway smooth muscle from the trachea to the smallest bronchi,7 and for this reason there is Address for reprint requests: Dr Peter J Barnes, Department of particular interest in their physiological role and Medicine (Respiratory Division), Royal Postgraduate Medical regulation. School, Hammersmith Hospital, London W12 OHS. NANC nerves have also been demonstrated in 561 Thorax: first published as 10.1136/thx.39.8.561 on 1 August 1984. Downloaded from 562 NON-ADRENERG IC, ADRENERGIC CHOLINERGIC NON-CHOLINERGIC I c2 v vagus sympathetic nerve cholinergic efferent ik adrenal medulla non -adrenergic, mnt afferent ACh NVIP smooth muscle copyright. epithelium Im *M ef Xa * X 0* * 0 a 0-Gre). a% lm )JI/Millil IIIIIIIIII)nfliff/ I)IIJImill a airway lumen http://thorax.bmj.com/ Innervation ofhuman airway smooth muscle: the three components ofthe autonomic nervous system. In addition to classical adrenergic and cholinergic pathways, there is a third component to the autonomic nervous system, shown by the dashed lines. The non-cholinergic, non-adrenergic pathway is inhibitory to airway smooth muscle, the neurotransmitter of which is likely to be vasoactive intestinal peptide (VIP). There may also be an excitatory non-cholinergic pathway, which may consist ofcollateral branches ofafferent nerves which release substance P. Specific receptors for these neurotransmitters present on airway smooth muscle cells: 3,-8 adrenergic, M-muscarnic cholinergic, V-VIP, and P-substance on September 30, 2021 by guest. Protected P receptors. ACh-acety1choline. cats and guinea pigs in vivo by electrical stimulation promotes mucus secretion in cat trachea, which is of the vagus nerve after cholinergic and adrenergic reduced but not abolished by cholinergic and blockade.'4-'6 Stimulation of this pathway produces adrenergic blockers"; and electrical field stimula- pronounced and long lasting bronchodilatation. This tion of ferret tracheal segments in vitro also indi- response can be inhibited by ganglion blockers, sug- cates that NANC nerves stimulate mucus secre- gesting that these NANC nerves are preganglionic tion.'8 NANC nerves may also mediate relaxation of as well as postganglionic.'4 It has not yet been poss- pulmonary blood vessels.'9 ible to establish whether NANC nerves mediate bronchodilation in human airways in vivo, although The search for the neurotransmitter such studies should be possible with pharmacologi- cal blockade and reflex stimulation. Although it has been possible to demonstrate the NANC nerves also regulate secretion of airway existence of NANC nerves in the lung both in vitro mucus in animals. Stimulation of the vagus nerves and in vivo, it is difficult to investigate the physio- Thorax: first published as 10.1136/thx.39.8.561 on 1 August 1984. Downloaded from 563 logical role of this nervous system until the neuro- ised to neurones and nerve terminals in airway transmitter has been identified and a specific blocker smooth muscle (particularly in the upper airways), developed. Burnstock originally proposed that the around submucosal glands, beneath airway epi- neurotransmitter might be a purine nucleotide such thelial cells, and in bronchial and pulmonary as adenosine triphosphate (ATP) or adenosine, vessels. 273132 In addition, VIP is localised in airway since in the gut these purines are released on nerve ganglia in both neurones and preganglionic nerve stimulation and both exogenous ATP and adenosine terminals (CB Basbaum, PJ Barnes, unpublished mimic some of the effects of NANC nerve stimula- observations). VIP produces prolonged relaxation tion.2 These nerves were therefore termed of airway smooth muscle in vitro, which is unaf- purinergic. The evidence is, however, against a fected by adrenergic or cholinergic blockers.2'2230 purine as the neurotransmitter of NANC nerves in Moreover, VIP mimics the electrophysiological the airways. Although ATP relaxes isolated guinea changes in airway smooth muscle produced by pig airway smooth muscle,202' its antagonist NANC nerve stimulation.2' 22 In vivo inhaled VIP quinidine does not block NANC relaxation either in protects against histamine induced bronchoconstric- vitro or in vivo,202223 nor does the purine uptake tion in dogs'9 and guinea pigs,33 and infused VIP inhibitor dipyridamole enhance non-adrenergic reverses serotonin induced bronchoconstriction in bronchodilation.2'22 cats.34 In isolated human airways VIP has a small More recent studies suggest that the neurotrans- relaxant effect8 and inhaled VIP has only a weak mitter may be a regulatory peptide, so that NANC protective effect against histamine induced bron- nerves are probably "peptidergic." There is now choconstriction compared with a /8 agonist.35 VIP rather convincing evidence that several regulatory given by infusion has a small bronchodilator effect peptides may be neurotransmitters or and protects against histamine induced wheeze in neuromodulators in the gut.24 Electron microscopy asthmatics,36 although the cardiovascular actions of has revealed different types of neurosecretory the infused peptide may have accounted for these granules in autonomic nerve terminals in the gut25: effects. The relative lack of effect of VIP in human small clear vesicles which contain acetylcholine and airways by no means excludes it as a possible small dense granules containing catecholamines
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