Pulmonary Smooth Muscle in Vertebrates: A Comparative Review of Structure and Function

Abstract

Although the airways of vertebrates are diverse in shape, complexity, and function, they all contain visceral smooth muscle. The morphology, function, and innervation of this tissue in airways is reviewed in actinopterygians, lungfish, amphibians, non-avian reptiles, birds, and mammals. Smooth muscle was likely involved in tension regulation ancestrally, and may serve to assist lung emptying in fishes and aquatic amphibians, as well as maintain internal lung structure. In certain non-avian reptiles and anurans antagonistic smooth muscle fibers may contribute to intrapulmonary gas mixing. In mammals and birds, smooth muscle regulates airway caliber, and may be important in controlling the distribution of ventilation at rest and exercise, or during thermoregulatory and vocal hyperventilation. Airway smooth muscle is controlled by the autonomic nervous system: cranial cholinergic innervation generally causes excitation, cranial non-adrenergic, non-cholinergic innervation causes inhibition, and spinal adrenergic (SA) input causes species-specific, often heterogeneous contractions and relaxations.

Structure and function of small airways in asthma patients revisited

“…These are only two of the many roles proposed for the contractile function of the ASM [100,102,103]. In a review published by CIERI [107], it has been suggested that ASM in the terminal bronchiole of mammals plays an important role in keeping the alveoli inflated at low lung volumes and that ASM might attenuate ventilation-perfusion heterogeneity by constricting airways in either the apex or base in different situations. Furthermore, the ASM is assigned an important role in the production of cytokines, chemokines, growth factors and ECM components [108].…”

Asthma: A Loss of Post-natal Homeostatic Control of Airways Smooth Muscle With Regression Toward a Pre-natal State

“…Air is actively forced into the primitive lungs by muscles in the upper airways while emptying is also an active process driven by largely the smooth muscle of the lower airway (159)(160)(161)(162)(163)(164). Of note, much of the control mechanisms via the vagus nerve appears to have been established at the very earliest stages in the evolution of the lung and air breathing, while surfactants also date back to the earliest lungs and swim bladders (165)(166)(167)(168)(169)(170)(171). The evolution of the diaphragm, present only in mammals, and a separate relatively rigid thoracic cavity, together with robust elastic recoil provided for a much more efficient means of filling and emptying the lungs (dinosaurs, birds, and reptiles developed completely different mechanisms for filling and emptying their lungs).…”

“…Emptying alveoli helps to both protect these fragile structures from barotrauma and prevent nitrogen narcosis. Surfactants appear to help unstick the closed alveoli, a role they probably served in the earliest rudimentary lungs (165,166).…”

“…However, in the case of the human respiratory tract, sympathetic innervation is sparse and predominantly supplies blood vessels and submucosal glands. In contrast to humans, spinal adrenergic sympathetic nerves supply ASM in some mammals such as guinea pigs, cats and dogs (165,264,265). In humans it is the cranial parasympathetic nervous system that predominantly controls the ASM through extensive plexuses.…”

“…Nitric oxide [NO] and vasoactive intestinal peptide (VIP) act as the principle transmitters in the mammalian NANC parasympathetic bronchodilating system with the former predominating in humans (though to date there is no direct evidence that NO gas is released during these responses). It appears that parasympathetic mediated relaxations of ASM requires higher frequency of stimulation than those needed to evoke parasympathetic cholinergic contractions (165,264,265).…”