Tension and stretch receptors in gastrointestinal smooth muscle: re-evaluating vagal mechanoreceptor electrophysiology

Electrophysiological and morphological analyses of vagal mechanoreceptors i n the gut wall suggest conflicting conclusions. Electrophysiology has disti nguished a single general class of ending in smooth muscle, one characteriz ed as an 'in series' tension receptor. Morphology, in contrast, has charact erized two distinct specializations of vagal afferent endings in the muscle wall of the gastrointestinal (GI) tract. These two structures differ in te rms of their target tissues, terminal architectures and regional distributi ons; they also develop on different ontogenetic timetables and depend on di fferent trophic support in the muscle wall. On the basis of these features, we have proposed that one of the putative mechanoreceptors, the intragangl ionic laminar ending (IGLE), has characteristics of a tension receptor and the other, the intramuscular array (IMA), has features of a stretch or leng th receptor. In a functional analogy with striated muscle proprioceptors, I GLEs should have similarities to Golgi tendon organs, whereas IMAs should h ave equivalencies with muscle spindle afferents. The present survey re-exam ines the recording analyses in light of the structural observations. This r eview indicates that previous electrophysiological studies are too inconclu sive to refute the inference that the vagus supplies two distinct types of mechanoreceptors to the muscle wall of the GI tract. Multiple methodologica l constraints and sources of variance have limited the resolution of electr ophysiological experiments. Specifically, these experiments have convention ally used distension stimuli that confound tension and stretch. In addition , sampling strategies have biased recording experiments towards a focus on one type of ending, the IGLE. Furthermore, putative functional properties ( e.g., broad tuning) of vagal mechanoreceptors suggest that distinguishing t wo recording patterns will require exacting protocols. Combining a recognit ion of the methodological difficulties Chat have limited electrophysiologic al analyses with an understanding of the structural features of the endings , however, suggests several critical electrophysiological experiments with the resolution to distinguish two classes of response profiles. Until such experiments can be conducted, sensory physiology's axiom that 'function Var ies with form', taken together with a re-assessment of the existing data, s uggests that the vagus nerve supplies stretch receptors as well as tension receptors to the wall of the GI tract. (C) 2000 Elsevier Science B.V. All r ights reserved.