By Professor Tony Wright
Most birds have eyes in the side of their head and so have almost 360° vision. This is why it is difficult to catch a chicken as they can always see you coming. In mammals the eyes move to the front of the head and so they have better, 3D vision with depth perception, but they cannot see danger coming from behind and so have hearing as an early warning system and as one of their first lines of defence. In the jungle, an unexpected, unusual sound such as the rustle of leaves or the hiss of moving grass coming from behind brings a possible warning. The two ears hear the sound at slightly different volumes and slightly different times if the sound is to one side or the other. These volume and time differences between the two ears along with the subtle differences introduced by the complex shape of the pinna enable the brain to calculate and localise the source of sound. This, in turn, allows the head to be turned in the correct direction and the eyes used to decide what was the cause of the commotion. During this time the brain stem is active preparing the animal for the worst. The heart rate increases; the pulse quickens; the breathing becomes deeper and quicker and the adrenaline starts to flow. The animal is physiologically “on edge” ready to flee or fight if the source of sound turns out to be an enemy – a snake looking for lunch, perhaps. The state of alertness continues until the animal determines that the sound was only wind rustling the leaves or running through the tall grass. The state of alertness then calms and the animal’s brain stem returns to “stand by”.
Skilled makers of horror movies use this effect to get their audiences on the edge of their seats by moving them into darkness and then introducing peculiar sounds from different directions that defy localisation or recognition or both and which cannot, of course, be identified by looking at them. The audience’s adrenaline starts to flow, the heart rate increases and they grip the arms of their seats even though they are only sitting in the cinema. It is a common sensation that creaky noises heard in a darkened house at night bring about the sensations of fear, anxiety and can even make the skin creep.
Tinnitus can be defined as the perception of sound by an individual in the absence of any external sounds. In my opinion tinnitus is not a disease but a symptom of some underlying disorder. It frequently relates to a hearing loss especially a sudden onset hearing loss as in “disco tinnitus” but can also be a result of many other factors and anything that perturbs the auditory pathways from impacted wax to tumours on the acoustic nerve or more central damage to the auditory pathways in the brain can result in tinnitus .
As described above, tinnitus can be particularly distressing because the onset of unexpected, unexplained internal sounds usually trigger a physiological “fight or flight” response as if there were dangerous sounds in the environment.
However, factors not clearly associated with the auditory pathways can also be linked to tinnitus. When specific factors outside the conventional auditory pathways generate tinnitus or enhance the perception of tinnitus this is called “somatic tinnitus”.
Tinnitus and temporomandibular joint disorders have long been associated (reference 1 and 2). It has, more recently been strongly suggested, on the basis of an analysis of many scientific papers, that “tinnitus patients with temporo mandibular joint complaints could constitute a subtype, meaning a subgroup of tinnitus patients responsive to specific treatments.” (Reference 2 and 4).
Tinnitus is also frequently associated with whiplash injury and other neck trauma in the absence of brain damage or hearing losses. (Reference 4 and 6.).
Folmer and Griest in their article (reference 6) state: “Tinnitus is a significant symptom that commonly occurs as a result of head or neck trauma. The fact that tinnitus resulting from head or neck injuries tends to be more severe (and is often accompanied by a greater number of co-symptoms) than tinnitus from other causes or origins should be taken into account by clinicians treating these patients.” This is possibly because head and neck trauma is usually always associated with “bad situations” and the negative psychology has a detrimental impact that does not occur with temporomandibular joint problems.
Mechanisms relating to Tinnitus.
The auditory pathways
The inner ear-the labyrinth-contains the sensory cells that undertake hearing (cochlear) and balance (vestibular). The auditory cells have hair-like, but rigid sensors projecting into the fluid that fills the labyrinth. In mammals the auditory cells form two groups-the inner and outer hair cells.
Below is a scanning electron micrograph of part of the cochlea from a gerbil. The three rows of outer hair cell (OHC) sensors can be seen and just above them is a single row of inner hair cell (IHC) sensors. This image was taken by my colleague Prof Andrew Forge at UCL Ear Institute. Here the structure that houses the hair cells – the organ of Corti – has been opened to show the bodies of the outermost row of outer hair cells.
This is the surface of the human organ of Corti in an image that I took and shows more clearly the outer and inner hair cells but also the more irregular pattern in the human.
Below is my image of the sensors – the hairs – of a single human outer hair cell. The appearance is no different from that seen in other mammals.
The inner hair cells are more “primitive” and connect with virtually all of the sensory fibres that form the auditory nerve that carries impulses to the brain. The outer hair cells are a more recent addition in evolution and act as internal amplifiers that boost and fine tune the auditory signal that reaches the inner hair cells. These IHCs , in turn, send signal via the 30,000 acoustic nerve fibres to the brain. There are about 12,000 outer hair cells and 3500 inner hair cells and each inner hair cell has about 10 acoustic nerve fibres connected to it, although there are less per hair cell at each end of the cochlea – that is the very high and very low frequency receptor zones. These connections are called synapses.
Below is a diagram from the late, great Henrik Spoendlin who painstakingly evaluated and showed the distribution of nerve fibres in the cochlea. At least 95% of the acoustic nerve fibres arise from the inner hair cells.
Each normal acoustic nerve fibre when stimulated has what is called an “action potential” as the electrical signal passes along it. Whilst it is possible to measure individual action potentials in single fibres of the acoustic nerve in experimental animals, this is not possible in humans but the Whole Nerve Action Potentials can be recorded. This is the summed result of multiple, individual nerve action potentials when the ear is stimulated with a loud, broadband sound so that many of the inner hair cells are stimulated. These recording are variously called Whole Nerve Action Potentials, Compound Action Potentials or Brainstem Auditory Evoked Potentials (BAEPs).
The inner hair cells in the cochlea provide almost all the information travelling to the brain via the acoustic nerve. The acoustic nerve fibres travel to the cochlear nucleus in the brainstem and within this nucleus there is a complex branching pattern but fibres end up reaching the so-called fusiform cells. From here the majority of the information passes via the superior olive, the inferior colliculus and the medial geniculate body to the auditory cortex in the temporal lobe on the other side of the brain. This is where “hearing” is believed to occur.
When the cochlear nucleus receives signal that is unexpected or unexplained then output passes to the centres in the brainstem that change, inter alia, pulse rate, blood pressure, breathing and the production of stress hormones such as adrenaline. The individual becomes ready for “fight or flight”. Pleasant sounds such as a nice phrase in a piece of music can also have an effect and cause a tingling in the muscles and even make the hair stand on end. People do not just hear sounds but sounds affect the individual’s physiology.
Below is a very simplified diagram of some of the pathways involved. Increased spontaneous firing rates (SR), especially in the cochlear nucleus, in response to altered inputs, both auditory and non auditory, have been proposed as a correlate of tinnitus and have now been detected and measured. The non auditory inputs are shown below.
[There are some suggestions that there is no direct “pain input” [nocioceptive] into the cochlear nucleus although it is clinical experience that pain heightens the perception of tinnitus; so the pathway may relate to the Auditory Cortex or its connections with the cochlear nucleus rather than the nucleus itself.]
The cochlear nucleus “expects” to receive signal. The world may be quiet but the world is never silent and if there is reduced input then the cochlear nucleus responds by attempting to enhance the input signal. There are several mechanisms to achieve this and which are outside the scope of this discussion, but the effect is to increase neural activity (spontaneous rate – SR) which then becomes detected as noise in the system. This is tinnitus and is the phenomenon that occurs when people with normal hearing and no tinnitus are put into silent rooms-anechoic chambers-when after a few minutes they all develop tinnitus. The mechanism of this is that the lack of input causes the brain to respond by turning up the gain and thereby generating internal noise.
If there is damage to the inner hair cells say from prolonged noise in the discotheque then the input to the brainstem reduces and the brain responds by turning up the “gain” so that neural activity is now generated and detected.
However there are also external inputs to the cochlear nucleus and the temporo mandibular joint, for example, can produce significant input into the cochlear nucleus and generate the perception of tinnitus. This then stimulates the “fight or flight” responses.
On top of the “physiological” model shown in the diagram, humans have a” psychological” component of thoughts, feelings and emotions, overlaid on this and the impact of the adverse psychological effects often compounded by a poor sleep pattern makes the perception of the tinnitus worse. This can result in a downward spiral of tinnitus distress.
So the management of tinnitus can be complex. If there is a possible causal factor such as a hearing loss, temporo mandibular joint disorders, sinus disease and so on then this should be treated but the management of tinnitus is essentially psychological.
The interaction between the physiology and psychology is, in my opinion, a “software, programming fault” in humans. The natural fight and flight response that occurs with an unexpected unexplained sound unfortunately induces an anxiety in humans that when the stimulus sound is internal appears to make the perception of the sound worse which in turn increases the fight and flight responses. Breaking the “loop” can be difficult.
Amongst many other dedicated scientists, Susan Shore from the Kresge Hearing Research Institute at the University of Michigan has spent years in investigating the neurophysiology of the auditory pathways and their relationship to tinnitus. She has published extensively and is referenced below. More recently she has been investigating the effect of electrical stimulation of the neck muscles on reducing the perception of tinnitus with encouraging results although additional sound input appears to improve the tinnitus reduction. The picture is complex.
References.
1. Tinnitus and vertigo in patients with temporomandibular disorder
Arch Otolaryngol Head Neck Surg. 1992 Aug;118(8):817-21.
Abstract
The association of tinnitus and vertigo with temporomandibular disorder (TMD) has been debated for many years. The observation that patients with TMD have otologic symptoms is confounded because tinnitus and vertigo are common symptoms in the normal population. The present study was conducted to determine if tinnitus and vertigo are actually more prevalent in patients with TMD than in appropriate age-matched controls. One control group was recruited from patients seeking care for health maintenance and the other from patients seeking routine dental care. We surveyed 1032 patients: 338 had TMD and 694 served as two age-matched control groups. Tinnitus and vertigo symptoms were significantly more prevalent in the TMD group than in either of the control groups. The mechanism of the association of TMD and otologic symptoms is unknown.
2. Impact of Temporomandibular Joint Complaints on Tinnitus-Related Distress
Niklas K. Edvall et al.
Frontiers in Neuroscience 2019, 13, Article 879.
3. Plasticity of somatosensory inputs to the cochlear nucleus – implications for tinnitus
S.E. Shore
Hear Res. 2011 November ; 281(1-2): 38–46.
Abstract
This chapter reviews evidence for functional connections of the somatosensory and auditory systems at the very lowest levels of the nervous system. Neural inputs from the dosal root and trigeminal ganglia, as well as their brain stem nuclei, cuneate, gracillis and trigeminal, terminate in the cochlear nuclei. Terminations are primarily in the shell regions surrounding the cochlear nuclei but some terminals are found in the magnocellular regions of cochlear nucleus. The effects of stimulating these inputs on multisensory integration are shown as short and long-term, both suppressive and enhancing. Evidence that these projections are glutamatergic and are altered after cochlear damage is provided in the light of probable influences on the modulation and generation of tinnitus.
4. Neural mechanisms underlying somatic tinnitus
Susan Shore,1 Jianxun Zhou, and Seth Koehler
Prog Brain Res. 2007; 166: 107–123
Abstract
Approximately two-thirds of individuals with tinnitus can modulate the loudness or pitch of their tinnitus by voluntary or external manipulations of the jaw, movements of the eyes, or pressure applied to head and neck regions, including the temporomandibular joint. In some cases, the necessary manipulations reported were forceful while in others less vigorous manipulations could produce the changes in perceived loudness and or pitch of the tinnitus In addition, there is an increased prevalence of somatoform disorders in individuals with tinnitus as well as reports of tinnitus occurring after dental pulpalgia that resolved after endodontic therapy. Tinnitus is also associated with upper craniocervical imbalances such as prolapsed intervertebral disks or instability of the craniocervical junction, which can be resolved following stabilization surgery. Similarly, tinnitus occurs more frequently in patients who have craniocervical mandibular disorders such as temporomandibular joint syndrome .
These factors have something in common: they all involve stimulation of the somatosensory system, usually associated with the jaw, temporomandibular joint, extra-ocular muscles, and the neck. While most reported changes in tinnitus involve somatosensory regions of the head and neck, changes in tinnitus can even occur with stimulation of the median nerve or upper limbs all leading to the term “somatic tinnitus.”
5. Diagnosis and management of somatosensory tinnitus: review article
Tanit Ganz Sanchez and Carina Bezerra Rocha
Clinics (Sao Paulo). 2011 Jun; 66(6): 1089–1094.
Abstract.
Diagnosis of somatosensory tinnitus
Somatosensory tinnitus is suspected clinically when anamnesis shows at least one of the following occurrences prior to the onset of tinnitus: (1) evident history of head or neck trauma, (2) tinnitus association with some manipulation of the teeth, jaw or cervical spine, (3) recurrent pain episodes in head, neck or shoulder girdle, (4) temporal coincidence of appearance or increase of both pain and tinnitus, (5) increase of tinnitus during inadequate postures during rest, walking, working or sleeping and (6) intense bruxism periods during the day or night.
This type of tinnitus often changes its loudness, pitch or localization during other stimulation coming from the head and neck. The most important characteristic of such tinnitus is that its origin seems to be related to problems of the head and neck, rather than to problems of the ear. Because of that, more than ever, these patients should be evaluated by an integrated team including an experienced dentist and a physiotherapist (or other professional) to evaluate possible bone or muscular disorders of the face, teeth and neck, in order to allow prompt diagnosis with a view to beginning adequate treatment as early as possible.
6. Chronic Tinnitus Resulting From Head or Neck Injuries.
Robert L. Folmer, PhD; Susan E. Griest, MPH.
Laryngoscope 113: May 2003. 821-827
Objectives: The main objectives were 1) to determine the percentage of cases of chronic tinnitus in a specialized clinic that resulted from head or neck injuries; 2) to describe the characteristics of this population; and 3) to compare patients with head or neck trauma with patients whose tinnitus onset was not associated with head or neck injuries.
Conclusions: Tinnitus is a significant symptom that commonly occurs as a result of head or neck trauma. The fact that tinnitus resulting from head or neck injuries tends to be more severe (and is often accompanied by a greater number of cosymptoms) than tinnitus resulting from other causes should be taken into account by clinicians treating these patients.
7. Tinnitus after head injury: evidence from otoacoustic emissions
Borka J Ceranic, Deepak K Prasher, Ewa Raglan, Linda M Luxon
J Neurol Neurosurg Psychiatry 1998;65:523–529
8. A Review of the Otological Aspects of Whiplash Injury
R.M.D. Tranter, J.R. Graham .
J Forensic Legal Med. 2009 Feb;16(2):53-5.
9. Tinnitus in Whiplash Injury.
C.-F. Claussen, L. Constantinescu.
International Tinnitus Journal Vol l, 105-114 (1995).