MIDDLE EAR PRESSURE NEURAL FEEDBACK CONTROL

Michael Gaihede

Department of Otolaryngology, Head and Neck Surgery, Aarhus University Hospital, Aalborg, Denmark

Introduction

The normal function of the middle ear (ME) depends on a pressure close to ambient pressure; however, impaired regulation of the ME pressure often leads to underpressure in diseased ears. Thus, underpressure is found in relation to clinical conditions such as retraction pocket of the tympanic membrane (TM), atelectasis, and formation of cholesteatomas.1 Basically, this underpressure is explained by gas absorption from the ME-mastoid air to the mucosal blood which is insufficiently replenished due to a decreased air supply related to an impaired function of the Eustachian tube (ET).2

The overall regulation of the ME pressure is basically unknown. Whereas it may depend solely on local factors such as the gas exchange of the ME and the ET function, it has also been suggested that an overall neural feedback control exists similar to, for instance, respiratory control (Fig 1).3 According to this hypothesis, mechano-receptors in the TM, the ME and/or the mastoid convey afferent neural information on the pressure status of the ME by the tympanic nerve (NIX). This information is transmitted to areas related to the respiratory centers of the brain stem nucleus of the solitary tract. These centers are also close and connected to the nucleus ambiguus and NV motor nuclei which control the opening of the ET. Thus, these brain stem centers obtain afferent information on the ME pressure from the NIX and exert their efferent activity via NV motor neurons activating the mm. levator palati and the mm. veli palatini. Therefore, opening of the ET can be elicited resulting in an equilibration of any differences between ME and ambient pressure.

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Fig. 1. Description of the overall mechanisms involved in neural feedback control of ME pressure.

This hypothesis has initially been based on animal studies, and further documentation is still demanded. However, over time a series of both basic and clinical experiments have supported this idea. These studies contain both anatomical components as well as physiological evidence for an overall neural control of ME pressure.

Anatomical studies

The early evidence on neural feedback control of ME pressure came from histological studies in rabbits using horseradish peroxidase as a neural tracer. The tracer was applied in two places: 1) at the promontory of the ME around the tympanic plexus; and 2) at the ET muscles in the palate.3 The subsequent findings of these tracers were: 1) in the brain stem at the nucleus of the solitary tract in areas of respiratory control; and 2) in the brain stem at the nucleus ambiguus and the NV motor nucleus.3 Since the same brain stem areas are all connected and involved in respiratory control, it has been suggested that similar mechanisms function in ME pressure control.3 Later, the same findings have been reported also for primates.4

The receptors for monitoring the pressure have been suggested to be baro- or stretch-receptors, but also glomus chemo-receptors; however, the latter are inconsistently found in human temporal bones.5 Modified Vater-Pacinian corpuscles have been described in the pars tensa of the TM,6 and similar corpuscles have been reported in the mucosa of the ME itself as well as in the mastoid in temporal bones.7 The pars flaccida of the TM has been suggested as a logical site for pressure monitoring because of its higher elasticity,8 and the region is rich in both myelinated and un-myelinated nerve fibers; however, no specialized nerve endings have been found here.7

In summary, the exact mechano-receptors playing a role in monitoring the pressure status of the ME have not been identified yet. However, the tympanic nerve innervates the mucosa of the entire areas of the ME including the tympanic plexus, the mastoid, and the ET, so that it is likely to convey any afferent information to the brain stem centers.9

Physiological studies

Important physiological studies have further supported the idea of a central neural feedback control for ME pressure regulation. Thus, electrical stimulation of the tympanic plexus has been demonstrated to elicit EMG recorded activity of the ET muscles with latencies of nine to 28 ms in primates.10 The connections between the ME and the ET muscles have also been suggested after clinical experiments anesthetizing the TM by iontophoresis which resulted in a decreased ability of the ET to equilibrate deviating ME pressures.11 Similar findings have been reported, where the anesthetics were applied directly at the promontory in subjects with a TM perforation or injected into the ME through a puncture of the TM.12

Clinical experiments with anesthesia of the TM lead to increasing thresholds of pressure sensation, when experimental pressures were applied to the ear canal; especially patients with pathological TM’s showed increasing thresholds, so that it has been suggested that depletion of neural receptors in the TM may result in an impaired pressure regulation.13

Animal experiments with sectioning of the tympanic nerve have been followed by formation of retraction pockets in a series of rabbits; moreover, ME effusion was formed in more of these animals.14 It was suggested that inactivation of the tympanic nerve resulted in a decreased aeration of the ME as well an impaired clearance function of the ET.14

Clinical neuro-physiological studies of evoked potentials with 3D recordings and source analysis from up to 128 electrodes have demonstrated distinct activation patterns of the brain stem related to static pressure stimulation of the TM in normal subjects.15 These static activations of the brain stem were clearly different from similar evoked potentials related to acoustic pressure stimulation, so that separate neural pathways to the brain stem have been presented for static pressures.15 In addition, activation of cerebellar centers has been demonstrated suggesting a coordination of related muscular activities.15 Further, these experiments also included wavelet analysis, which reflects the frequency contents of neural activities; these frequency contents are specific for different neural systems. Static pressures mainly result in θ-band activity (0–4 Hz), whereas acoustic pressures result in α-band activity (7–10 Hz).16 In conclusion, there are separate activation patterns related to static and acoustic pressure stimulations of the TM.

Finally, fMRI studies have demonstrated cortical activation in normal subjects in response to static pressure stimulation of the TM. This activation includes the post-central gyrus of the Brodmann area 43 which is related to control of the pharyngeal muscles. It has been suggested that these results represent a connection between the ME and activation of the ET muscles.17

Conclusions

More anatomical and physiological studies have produced evidence supporting the idea of an overall neural feedback control of ME pressure in humans. Considering the many similarities between these findings and respiratory control, it seems reasonable to conclude that ME pressure in humans is subjected to such a regulatory mechanism. In addition to the efferent activation of the ET, the mastoid may also take part in pressure regulation by vasomotor control of the perfusion and the congestion of its mucosa (Fig. 1).18 Further research is needed to increase our basic knowledge, and especially studies which can link the efferent and afferent parts of such a feedback regulation.

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18.Gaihede M, Cros O, Padurariu S. The role of the mastoid in middle ear pressure regulation. In: Takahashi H (Ed.), Proceedings of the 9th International Conference on Cholesteatoma and Ear Surgery, pp. 15-18. Amsterdam: Kugler Publications 2013


Addres for correspondence: Michael Gaihede, MD, Department of Otolaryngology, Head & Neck Surgery, Aarhus University Hospital, DK-9000 Aalborg, Denmark. mlg@rn.dk

Cholesteatoma and Ear Surgery – An Update, pp. 21–23

Edited by Haruo Takahashi

2013 © Kugler Publications, Amsterdam, The Netherlands