Critical Cochlea/Vestibular Interactions

Abstract

There is a close interaction of the gravity detecting balance organs, the maculae of the saccule and utricle of the inner ear, with the hearing system of the inner ear. The need for this is that although they detect the sensations specific to their own function there is interference with this function due to overlap of wavelengths used by both systems resulting in extraordinary stimulation of the other system for both hearing and balance.

1. Introduction

The precise way that the cochlea and vestibular system interact is not clearly understood. This chapter addresses this deficiency attempting to relate the cochlear and vestibular inter dependency, in such a way that it will effectively lead to research more clearly outlining this association, and hopefully result in more effective therapy for patients with both cochlear and vestibular diseases.

2. Vestibular evoked myogenic potentials. What are they?

Cervical vestibular evoked myogenic potentials (Cvemps) are a response to repetitive sound into the ipsilateral ear resulting in reduction of tonic activity of the tensed ipsilateral sternomastoid muscle. Ocular vestibular evoked myogenic potentials (Ovemp) responses are a contralateral sound or vibration excitatory reflex response and move the eyes in the direction of the stimulus. Ovemps are done with the eyes raised and tonic stimulation of the superior ophthalmic muscles is measured [1].

Why do these responses occur, what are they for. At first I assumed that the ear nearer the sound which hears a sound louder speeds a rapid head turn in the direction of the sound. Perhaps these Cvemp and Ovemp sound responses are the beginning of a fast reflex eye movement and head turn in the direction of a sound and in combination are protective by turning the head as rapidly as possible to look at what may be a potential threat.

If that is correct then why is there an Ovemp response with direct vibratory stimulation of the skull. A head blow is a normal life occurrence. The reflex produces a physiological stimulus causing the individual to look toward where the blow has arisen. Vibratory Ovemps are a response to a repetitive tap on the skull. Clearly, this is not a physiological stimulus produced by an external source [2]. Vibratory OVEMP’s occur as a response to repetitive direct skull stimulation and are an externally measurable response to internally generated vibration from preplanned skull vibration, which occurs during chewing, speaking and other upper body internally generated vibrations. The externally recorded response is due to neural circuitry resulting in cochlea suppression of these internally generated sounds so that the threat of external potentially hazardous sound can be specifically differentiated from internal stimuli by the cochlea.

The stimulus used for sound Cvemp is a 95 dB, 500 Hz air conduction signal and for Ovemp induction in our laboratory is a 97 dB SPL,500 Hz air conduction signal [1].

These stimuli are considerably above any commonly occurring natural external sounds. Sounds louder than this do occur in nature, at waterfalls, for example, Niagara Falls also waves breaking at the seashore, with roaring animals, barking dogs and during thunder storms. In terms of an evolutionarily benefit, these sounds are so rare that it is unlikely that complex vestibular and cochlea responses of the sort described as causing vemp responses would have developed as a consequence of these rare occurrences. Also, Cvemps and Ovemps are done by having the patient take up an activity that is rarely done in normal life and requires an aphysiologically loud external sound stimulus. Persistent tonic sternomastoid contraction is not often undertaken. Head turn is usually a rapid response to a stimulus. Ovemp is done by having the eyes elevated 30 degrees. In life, this is done only briefly before the head is raised. The fact that unusual activities are needed to produce responses raises the question of what useful purpose they serve. Cvemps and Ovemps are extremely helpful to the clinician allowing detection of malfunction of the macula of the saccule and utricle respectively and in this they appear to be akin to the auditory brainstem responses [ABR] that are extremely helpful for the physician in perhaps suggesting the presence of an acoustic neuroma but do not as far as we know have a specific physiological function of their own.

Sound Ovemps at 500 Hertz the standard frequency used during this test are more difficult to record reliably than vibration Ovemps [2]. This is because the response to sound stimulation is only just above the level of electrical interference and careful often repeated testing has to be done with careful analysis to have confidence in the response recorded in each patient. It can, however, be done reliably after practice in all patients under 60 and in almost all over this age [2]. Each laboratory needs to establish its own technique and normal distribution curve using the equipment available to them just as in any other complex audiological test, for example, ABR so that abnormalities can be documented consistently and reliably. A normal distribution curve is essential for each laboratory when measuring amplitude as well as early and late latencies so that pathological abnormalities on the test are defined. As with all laboratory measurements in the neurotology field, results greater than 2 standard deviations from normal indicate pathology although there is a 1 in 20 chance that such a result is just an extreme or normal [1, 3].

The advantage of sound Ovemps as a stimulus compared to vibration Ovemps is that the side from which any abnormalities arises with sound Ovemps come from the stimulated side, whereas if there is an abnormality with vibration Ovemps, this can be due to abnormalities on either side although more commonly it is the contralateral side which is regarded as abnormal [4].

3. The stapedius reflex. What is it for?

In the human, the footplate of the stapes is directly above and about 3–4 mm lateral to the macula of the saccule [5]. It is visible as a white patch on removal of the stapes footplate. The utricle is close by and slightly above the saccule. Any external sound moving the footplate of the stapes causes a vibratory stimulation of the inner ear fluids. This stimulus reaches the saccule and vibrates the macula before it passes on to the cochlea to be heard.

Until 1964, it was assumed that the stapedius reflex muscle response was present to protect the individual from excessively loud external sounds. At that time, Blair Simmons [6] measured stapedius muscle reflex activity and demonstrated that it was occurring in response to speaking and swallowing. He showed that it began just before the event and ceased just after the event. Extrapolating this finding, it is probable that responses also occur due to biting and chewing food as well as swallowing and belching, blowing the nose, and sniffing, all of which potentially alter the pressure of the middle ear resulting in altered sound transfer to the inner ear and an effect on the cochlea. There is a stapedius reflex response to loud sound but necessarily there is a delay as the sound has to be heard through the cochlea and central processing is necessary for the facial nerve stapedius response. Prior to CT and MRI assessment of the internal auditory canal, the response of stapedius reflex decay in response to sound was one of the tests used to suggest the possible presence of an acoustic neuroma.

The stapedius reflex alters the way the stapes moves [7, 8]. This means that the stimulus received by the inner ear hearing and balance organs differs between when the sound occurs from an internal bodily induced sound stimulus and an external noise when there is no immediate activity of the stapedius muscle. There is a different pattern of vibration of the endolymph beneath the stapes footplate with internally and externally generated sound.

The stapedius reflex response is active immediately and precisely at the commencement of talking and swallowing. The stimulus to the maculae of the saccule and utricle is different when there is an external sound stimulus, and there is no immediate stapedius muscle activity compared to when it is activated due to internal stimulation. This difference allows central differentiation of whether there is an external sound or not. It is essential that both internal and external sound vibration of the perilymph avoids stimulation of the maculae of utricle and saccule resulting in dysfunction of balance activity. Should this occur it would result in instability of the individual potentially making it vulnerable to predation as its instability would reduce effective emergency safety measures such as running, hiding or fighting.

Simmons also speculated that further feedback systems to the inner ear related to hearing and balance would be discovered. The description of the olivocochlear bundle [9, 10] and vestibular efferent systems [11] fulfills his prediction.

A recent, detailed review of effects of loud sounds on the vestibular system was published [12]. It is clear from this, that in animal studies significant damage occurs. Not surprisingly pathological human information is limited. Despite this, it is definite that there is damage to the vestibular system from excessively loud sound, which is due to damage to the maculae of the saccule and utricle particularly the saccule.

A delay occurs between when sound arrives at the inner ear before it is processed in the cochlea, transferred centrally to the brainstem to result in altered stapedius muscle activity via the facial nerve. It offers some cochlea protection from unexpected loud sound. There is damage to the otoconia of the maculae not only impairing balance but also resulting in impaired control of reflex responses to sound. The cochlea is less protected than it would otherwise be by the baffle effect of the saccule and macula by otoconia being vibrated and possibly damaged with less afferent reflex responses induced by this stimulation. This will be discussed later. It is suggested that perhaps it is damage to the maculae of the saccule in particular but possibly also the utricle that results in subsequent damage to the cochlea in the 4 K range, which is the site of most noise induced hearing loss.

If an external sound is loud, a stapedius muscle reflex response is generated, necessarily after a short time delay due to processing to determine if it is loud enough to generate the reflex and cochlea brainstem circuitry stimulates the reflex via the facial nerve. The stapedius reflex changes the vibratory pattern received by the maculae but as stated there is necessarily a delay between the stimulus and response. If there is a time delay and change in quality of the signal, this indicates that the sound is external rather than a stapedius muscle reflex response to internal sound, which is predicted by and coordinated by the cerebral cortices with the motor activities of swallowing, coughing, etc.

The ability to precisely time the stapedius muscle response resulting in an altered pattern of stimulus to the maculae and cochlea between an internal and external source allows the individual to ascertain if an external sound should be given specific attention and response, while the internal sounds can be recognized and ignored.

4. Threat

Vegetarian animals spend much of their awake hours biting eating and chewing (roughly 80% of the time) and need to be aware of potential predators while continuing to safely and effectively maintain their calorie intake. Because of internal suppression circuitry, the cochlea is able to differentiate these internal noises from potentially dangerous external sounds, while the herbivore is actively biting, chewing or vocalizing. A purpose of this chapter is to explain how this is done.

5. Otoconia. How do they work? What do they do?

The temporal bone consists of calcified collagenous tissue. When undertaking histological study of the inner ear neural structures, it is necessary that the calcium of the temporal bone is dissolved prior to microscopic histology otherwise the calcium blunts the knife preventing satisfactory structural analysis. Unfortunately, the essential histological decalcification preparation means that the calcium in the otoconial system of the maculae is dissolved so it cannot be examined directly at the same time as the vestibular hair cell membranes beneath them. This makes examination to look for structural signs of disease more conjectural. The macula of mammalian saccule and utricle has two types of calcium carbonate otoconia. There are small ones of 2–3 um in diameter and larger ones from 20 to 30 μm in diameter [11]. Due to their inertia, these are vibrated during any head movement including lifting and lowering the head when gravity also affects their motion. When external sound occurs, it also results in movement of the maculae due to the pressure waves caused by the movement of the stapes footplate due to the external sound. They are also moved during the production of internal bodily activity.

6. Internal bodily sounds. How loud are they?

The internal bodily sounds related to speaking consist of a fundamental sound from the larynx adjusted by pharyngeal, oral, lingual, and lip activities. Depending on the frequency of the stimulus and individual resonances of the soft tissues and skull, the amount of vibration of the sounds amplitude varies. These sounds are transferred to the temporal bone (inner ear) in two ways. They are transferred by direct tissue vibration (bone conduction) and also by air conduction particularly the lower frequencies that are heard more clearly through the external auditory canal because of their low frequency characteristics [13]. Sound stimulation of the ears is dependent on the frequency of the sound. Due to the long wavelength of low-frequency sounds, their amplitude is not reduced at corners and little energy is lost. With higher frequencies there is significant attenuation of the sound due to the head shadow effect and therefore, it is heard better in the ear closest to the stimulus [14].

The quality of internal sound changes over time as an animal grows, and it is higher pitched when the animal is younger and smaller and has a lower frequency as the individual grows so that the animal is constantly adjusting responses to maximize the effectiveness of the stimulus detection response of the stapedius reflex in order to suppress dysfunction of the balance system while maximizing detection of external sounds through the ear canal (Figure 1).

Figure 1.

The black arrows represent efferent pathways from the cerebrum to the stapedius muscle, macular of the utricle, U, macular of the saccular, S, and the cochlear, C. the jagged red lines represent bone—Conducted sound from the larynx during vocalization, and from the mouth during biting, and chewing to the cochlea, utricle, saccule and external auditory canal (EAC). The blue line represents vocalization from the larynx, pharynx and oral cavity via the EAC, through the ossicles to the saccule and utricle. The macula of the saccular, S, diagrammatically shows a cross section of the striola at the line of polarity reversal. The macular of the utricle, U, shows the line of polarity reversal at the junction of the large lateral otoliths with the micro-otoliths of the striola region [15, 16]. The macula of the saccule, S, shows the line of polarity reversal below the microliths of the central striola in the chinchilla (Lysakowski a, personal communication). Taken from Acta Otolaryngologica [13].

Surprisingly when measured, internal bodily sounds such as chewing and biting are excessively loud above a level where noise hearing loss would be induced if they were external sounds [13].

Shouting when done as loudly as possible is also excessively loud [13]. In these circumstances why is it that opera singers who are called upon to sing very loudly and practice frequently do not have noise-induced hearing loss. Choir members who are in close proximity to other singers and close to the orchestra do incur noise-induced hearing loss [17]. The explanation for this finding is that the loud internally generated sound in this case from singing is suppressed by internal mechanisms to protect the cochlea.

An extreme example of loud sounds in nature is the male white bellbird, which has been recorded singing with a measured loudness of 125 dB(A); however, birds replace their cochlear hair cells seasonally [18].

Shute [19] proposed many years ago that the saccule could have a hearing function. He ascribed this to nerves traveling to the cochlea via the inferior vestibular nerve but bifurcating to travel through the nerve of Oort [20] to reach the basal cochlea as well as the saccular macula. When a sound reaches the saccular macula, it passes by the inferior vestibular nerve centrally but also directly to the cochlea via an antidromic reflex through the nerve of Oort.

Excessive noise exposure is recognized as causing measurable vestibular damage. Could cochlea damage be due to lack of protection from otoconial vibration suppression. Should this suggestion be correct, then efforts directed at protection of the vestibular system from excessive noise would be expected also to reduce cochlear damage. Rosen [21] showed that sounds of much lower amplitude than those that cause noise-induced hearing loss result in reduced hearing in older adults exposed to the noises of civilization throughout life such as traffic noise. Wear of the macula system may also occur due to noises of civilization and be why there is gradual deterioration of balance with aging as well as hearing.

Calcium-active drugs have been shown to be associated with improved Cvemps in vestibular migraine. The authors who wrote that article [22] ascribed these improved Cvemp responses to stabilization of brainstem activity by the medication, verapamil; however, it appears logical to this author that verapamil as a calcium-active agent could have acted on the macula otoconia stabilizing them resulting in an improved Cvemp response.

After a patient has head trauma with persistent vestibular complaints, vemps are usually abnormal [2], and a trial of verapamil with sequential repetitive vemps and a quality of life questionnaire would be a worthwhile research project to determine if this type of medication has a place in specifically treating what maybe a macula disorder.

Could treatment to repair malfunctioning otoconia such as calcium-active agents be investigated as a means of restoring otolithic function and perhaps preventing further cochlear damage in individuals who are starting to show signs of noise-induced hearing loss.

Assuming that cochlea injury from excess noise is due to failed otoconial vestibulo-cochlea protection then the symptom of tinnitus which is frequently associated with almost any hearing deficit may well also have induction in the otoconial system as could hyperacusis, which is also frequently associated with hearing loss of any cause including aging and after head trauma.

7. Superior semicircular canal dehiscence syndrome

The sound stimulus for Cvemps and Ovemps is focused and concentrated through the external ear canal. The stimulus for vibration Ovemps applied to the head is a substantially stronger energy stimulus commensurate with the bone conduction sound of speech and chewing. When there is a third window, as in a superior semicircular canals dehiscence syndrome (SSCDS) [23] there is loss of energy from the sound induced C and Ovemp ear canal stimulus which dissipates through the dehiscence. This results in a sub threshold, Cvemp response and an excessively large Ovemp response because of the altered fluid dynamics in the inner ear. There is an apparent reduction in threshold response for air conduction pure tones due to diversion of hydrostatic energy through the third window so less energy reaches the cochlea. The bone conduction stimulus during Ovemp testing is a much larger physical stimulus of the whole temporal bone and is not altered significantly with little energy dissipated if any by the third window. This results in a measured intracochlear conductive hearing deficit during standard pure tone audiometric testing. In the absence of any obvious tympanic membrane or middle ear disorder in the past, this was assumed to be due to otosclerosis despite an intact perhaps raised stapedius reflex threshold prior to the recognition of SSCDS. This concerns the author who wonders over the years how many times low-tone conductive hearing deficits due to SSCDS has been assumed to be due to otosclerosis and the patient has had surgery undertaken. There is a small risk of poor results with otosclerosis surgery and to undertake a procedure for this incorrect diagnosis means that a hearing improvement would not occur but all the risks associated with the surgery exist. Of even more concern is the patient who had revision surgery because of a poor initial operative result because it was due to SSCDS but it was assumed to be a failed “otosclerosis” procedure as complications from revision surgery are much more frequent and serious than with the initial procedure [24, 25].

Radiologically SSCDS is recognized not infrequently in children but it is not symptomatic. This has been put down to very thick dura mater overlying the dehiscence [26]. A more logical explanation is that if an individual has SSCDS at birth or as a small child they adjust, they do not become symptomatic because by being exposed to their own excessively vigorous but to them physiological inner ear fluid movements adjusting “tuning” [8] to the excessive hydrostatically different stimulation of sound and vibration is normal. As an adult after trauma, it is not possible to overcome the sudden substantial physiological dysfunction that occurs with the development of this syndrome and it results in people becoming dizzy with loud sounds and during eating.

There are other third windows disorders where dizziness can be induced by loud sound, and it can occur in tertiary otological syphilis and perilymph fistula. The effects of altered inner ear dynamics in these two disorders on the configuration of Cvemps and Ovemps are dependent on the location in the temporal bone of the third window. Henneberts sign with dizziness due to loud sounds in Ménière’s disease is associated with saccular proximity and even attachment to the stapes footplate [27].

8. Cochlea and vestibular efferents. What are they for?

The olivocochlear bundle (OCB) is a poorly understood efferent pathway. How it functions and what it does is still being established [9, 10, 28], which serves to protect the cochlea. It originates in the superior olivary complex in the brainstem and projects to both the ipsilateral and contralateral cochlea. The lateral olivocochlear system has uncrossed synapses ending on type 1 spiral ganglion cells projecting to the inner hair cells. The medial olivocochlear system innervates the outer hair cells and the majority of the fibers project to the contralateral cochlea. Once the efferent reflex is activated, the medial system hyperpolarizes the outer hair cells, which decreases the gain of the cochlea amplifier and sensitivity of the inner hair cells and also reduces the responses of the auditory nerve fibers. Pang [29] has shown that there is an ascending masking effect of about 40 dB due to contraction of the stapedius muscle; this affects the low frequencies to prevent high-frequency attenuation.

There is a system analogous to the olivocochlear bundle efferent system in the macula vestibular system, and it is the vestibular efferent system. During vocalization and chewing, there is otoconial movement due to the vibration of the skull from [13] chewing, biting and vocalizing. The vestibular efferent system suppresses the hair cell stimulation to these expected otoconial vibrations so that specific responses to head and body movement due to gravity change and acceleration/deceleration and head movement are reliably detected without adulteration by extraneous internal stimuli. There is pre-activation of this direct brainstem macula activity and cessation after completion of the task as occurs with the stapedius reflex in response to chewing, biting and talking so that people do not become dizzy.

Activities such as chewing and biting are instructed to occur through standard motor pathways to the appropriate brainstem nuclei and like the stapedius reflex are precisely timed and coordinated with inner ear vestibular and cochlea efferent activity. This maximizes inner ear suppression of inappropriate inadvertent responses in the cochlea and vestibular systems. There is an extremely complex structure of both afferent and efferent vestibular axons with the type 1 and type 2 vestibular hair cells in the maculae [11, 30]. The otoconia are stimulated by internal sounds, swallowing, speaking, etc., but also by movement and gravity, external stimuli which is their main function. One of the main purposes of the complex innervation of the maculae is to allow differentiation of these two stimulus systems, internal and external, so that confusion between the two is avoided and the individual is not destabilized by internal sounds while maintaining perfect balance during movement. Internal sounds cause the otoconia of the maculae to vibrate. When stimulation of the maculae by internal vibration occurs, the stimulus is generalized and similar throughout the maculae, whereas when there is body movement, the complex nature of the orientation of the vestibular hair cells [11, 30] means that certain areas are stimulated while others are not. This optimizes recognition that movement and gravity affect the individual and it is not the effect of internal sounds. Vibration, internal or external, results in movement of otoconia stimulating the vestibular hair cells. As the internal sound of speaking swallowing, etc., is commanded by the cerebral cortex, via the brainstem, a vestibular efferent stimulus is sent directly to the maculae to cancel the response to these stimuli due to otoconial vibration caused by internal sounds so that they are available for detection of movement without interference by internal sounds. The brainstem position of the nucleus for vestibular efferents varies depending on taxonomic rank but in all mammals studied it is in close proximity to the facial nucleus making timing for their interrelated activity with the vibratory effect of verbalization, etc. more precisely. It also explains why the distal vestibular efferent neurons synapse on the base of the distal cup of the afferent axon where it surrounds the type 1 vestibular hair cell or directly on the distal afferent axon proximal to the cup as by doing so they are located at a site to most precisely nullify the firing of the afferent neuron in response to internal sound stimulation of the hair cells by the vibrated otoconia. Although the peripheral endings differ in structure in type 2 vestibular hair cells, they also terminate on the basal hair cell and distal peripheral axon, which optimizes there role in suppressing hair cell firing due to internal vibration.

Vestibular hair cells are metabolically very active not only while an individual moves but also due to the effect of internal vibrations while at rest. This high energy demand may explain the need for extra-large mitochondria [31] at the apex of the hair cells to maximize their energy supply from oxidative phosphorylation, because the stereocilia are in a state of almost constant motion except during some periods of sleep when rest and refurbishment occur.

The activities of vocalizing biting and chewing are cerebral cortical tasks undertaken as part of normal human activity while undertaking other more complex tasks requiring significantly more concentration and cerebral cortical activity (thought) but even these simple task can be interrupted immediately by a more urgent need such as an external threat, which indicates that even though simple, these motor tasks at all times are under direct cerebral cortical control and do not function at sub-cortical or thalamic reflex control level.

The function of the semicircular canal system of the inner ear is specifically to maintain the eye fixed on a target while the body and head move. The system can be disconnected urgently if a sudden external stimulus sound or a visual stimulus calls for a rapid head turn and in these circumstances the vestibulo-ocular reflex [VOR] is instantly switched off. There is a coordination with the macula system [32] but this chapter is not the place to discuss the details of how [VOR] function works as it is not specifically related to vibration effects of sounds inside the head and their effect on macula function.

9. Summary

Internal sounds cause the otoconia of the maculae to vibrate. When stimulation of the maculae by internal vibration occurs, the stimulus is generalized and similar throughout the maculae, whereas when there is body movement the complex nature of the orientation of the vestibular hair cells means that certain areas are stimulated, while others are not. This optimizes recognition that movement and gravity affect the individual and it is not the effect of internal sounds. Vibration, internal or external, results in stimulation of the vestibular hair cells. As the internal sound of speaking swallowing, etc., is commanded by the cerebral cortex, via the brainstem, a vestibular efferent stimulus is sent directly to the maculae to cancel the activation of vestibular afferent hair cells due to otoconial vibration caused by internal sounds so that they are available for detection of head and body movements without interference by internal sounds. This explains why the distal vestibular efferent neuron synapse on the base of the distal cup of the afferent axon where it surrounds the vestibular hair cell or directly on the distal afferent axon proximal to the cup as by doing so they can most effectively nullify the firing of the afferent neuron in response to internal sound stimulation of the hair cells as this activity is precisely timed to the known internal stimulus to which they also respond. This system is closely analogous to the activity of stapedius muscle reflex in being caused as a response to internal stimuli and perhaps it is more than fortuitous that the brainstem origin of the vestibular efferent system is close to the facial nucleus.

10. Conclusion

This chapter emphasizes the close interaction of the cochlea with the acceleration and gravity detecting macula otoconial vestibular systems of the inner ear. It highlights the complexity and interdependence of the systems. There is need for further studies in this complex field to more fully understand its complex nature, which will hopefully lead to greater understanding of how each system works and to more effective therapy for hearing loss, tinnitus, hyperacusis and imbalance.

Acknowledgments

The author wishes to thank Dr. Art Mallinson for his enthusiasm support and scientific input over the years, Ms. Judy Rousselle for secretarial assistance and Ms. Vicky Earle for diagram production.

Conflict of interest

The author has no conflicts of interest.