While hyperacusis can be worse in one ear than the other, it impacts both ears more often than peripheral disorders such as hearing loss. This strongly suggests that the central auditory system plays a role in the development of hyperacusis. The central auditory system is the complex and adaptive network of neurological pathways from the cochlea to the higher levels of the brain. There are two key features of this system that those with hyperacusis should know,
- The brain is highly adaptive and will adjust loudness and processing according to average sound exposure, even at the lowest levels of the brainstem.
- Adaptivity can lead to hyperactivity when cells are damaged in the cochlea.
It is thought that hyperactivity without sound stimulation may be an expression of tinnitus and sound-induced hyperactivity may be an expression of hyperacusis.
“These observations…suggest tinnitus and hyperacusis, while triggered by cochlear damage, result from a maladaptation of the central auditory system to this peripheral disfunction, similar to phantom limb pain.”
-Central gain control in tinnitus and hyperacusis, Auerbach et. al.
As the auditory system is a complex processor rather than a simple amplifier, it is best to interpret this hyperactivity as hyperreactive processing rather than simply a louder signal. This distinction allows for the possibility of hyperacusis pain without loudness discomfort (for example, pain from low level noise generators) to be included in the neurological model.
The following sections will describe some aspects of the central auditory system that are suspected (but not yet proven) to contribute to hyperacusis. A more comprehensive description of such mechanisms can be found by reading Central gain control in tinnitus and hyperacusis by Auerbach, Rodrigues and Salvi. Hyperacusisresearch.org and Dr. Salvi also created an excellent video for hyperacusis sufferers covering these topics. Another good source on central auditory system mechanisms is Part 2 of the recent hyperacusis literature review by Tyler et. al.
There is overwhelming evidence that cochlear damage will trigger hyperactivity and gain increases throughout the auditory system. This gain increase is an imperfect attempt by the brain to enhance the fidelity of the auditory signal and is expected to be a catalyst for the development of both tinnitus and hyperacusis. The figure below demonstrates the paradoxical behavior of increased activity throughout the auditory system despite reduced output from the cochlea.
Figure from Central gain control in tinnitus and hyperacusis, Auerbach B, Rodrigues P and Salvi R
It is important to ask how such hyperactivity can develop in those without significant hearing loss as roughly 40% of hyperacusis patients show normal hearing levels. As described in Potential Mechanisms: Hidden Hearing Loss, loss of high threshold nerve fibers, loss of inner hair cells, and hearing loss at frequencies above 8 kHz may not show up on a standard hearing test. Each of these has been shown to have potential to initiate increased gain and hyperactivity throughout the auditory system.
In-Depth: Time Course, Frequency Selectivity
Hyperacusis develops suddenly in roughly 60% of hyperacusis patients. Setbacks (large drops in sound tolerance) can occur suddenly as well. A big question on the minds of many with hyperacusis is how this can be a central gain issue if tolerances drop so quickly. Examples generally given for gain plasticity are from earplug or noise generator studies that show gain change is gradual and takes weeks to accumulate just 7dB of change (Formby 2003). How can the slow and steady adjustments of the central auditory system be blamed for the sudden and deep drops in sound tolerance that are experienced by hyperacusis patients? And if central gain can drop sound tolerance suddenly, why does it take so long to build the tolerance back up?
While answers to these questions are still being sought, the assumption that the auditory system is sluggish is not completely true. Some portions of the auditory system adapt to signal changes within 160ms while others take only 10s of seconds to adapt (Dean 2008). Studies on hearing loss have found other features of the auditory system take months to adapt (Syka 2002). Thus the auditory system and auditory gain are capable of adapting both suddenly and gradually. The next question is, at what rate does it adapt to cochlear damage?
Several studies have measured the adaptation of the auditory system after cochlear damage in animals. It was found that different regions of the auditory system adapted to cochlear damage at different rates. Immediately after this shock to the system, more neurons in the highest levels of the auditory system (the auditory cortex) showed highly synchronized, epileptic-like activity. The auditory cortex also showed hyperactivity and significant gain enhancement within an hour after damage that slowly settled over a period of days. At lower levels (Inferior Colliculus and Cochlear Nucleus), hyperactive responses were found to take days to develop. This shows that a shock to the auditory system can result in an immediate reaction from the auditory cortex with lingering changes to many levels of the auditory system taking days.
Neurons in the auditory system are always active and firing even in silence. The frequency of this activity is called the spontaneous firing rate and can range from 0 to 100s of spikes per second. The brain tunes these rates through the gradual process called homeostatic plasticity. One suspected mechanism for hyperactivity (and hyperacusis) is an attempt through homeostatic plasticity to maintain a fixed average firing rate after it has been reduced due to cochlear damage. In this scenario, the average firing rate will be returned to its pre-injury level at the cost of increasing both minimum and maximum firing rates. An exaggerated example of this is shown in the figure below,
Figure from A Review of Hyperacusis and Future Directions: Part II., Tyler R, Pienkowski M, et. al.
From the cochlea to the auditory cortex, the central auditory system is spatially divided into frequency tuned regions from low to high frequencies. This arrangement of specific processing locations for specific frequencies is called tonotopic mapping.
As a result of tonotopic mapping, damage to the cochlea results in damage to specific frequency regions. However, as described in Audiometric Traits, loudness discomfort levels of hyperacusis patients are generally similar across frequency (as opposed to hearing sensitivity tests which often show notches or slopes). It is unlikely that the cochlea could be damaged uniformly across frequency from sound so the next question is, does the hyperactivity triggered by cochlear damage stay confined to the frequency regions where damage occurred?
The short answer is no. There have been several experiments that show cochlear damage to one frequency region can result in changes in neural activity in other frequency regions. This is thought to be a consequence of lateral inhibition. In the plot below, a single tone caused cochlear damage at 2 kHz (middle), resulting in changes in activity at both lower frequencies (left) and higher frequencies (right) in the auditory cortex and inferior colliculus (midbrain).
Figure from Central gain control in tinnitus and hyperacusis, Auerbach B, Rodrigues P and Salvi R
With these results in mind, it is then possible that damage and hearing loss at the more vulnerable cochlear regions (above 8 kHz) could reduce loudness tolerances at lower frequencies. It is unfortunate that hearing tests generally don’t test above 8 kHz. While this shows processing of frequencies outside of damaged regions can become hyperactive, these results alone do not show that LDLs will be similar across the full frequency range commonly measured (up to 8 kHz).
Another interesting interpretation which is supported by multiple studies is that each processing level of the auditory system responds differently. As a result, it is possible that sounds at low and mid frequencies can be sensed as equally loud in the auditory cortex while there could be significantly more activity in the midbrain at lower frequencies after damage. If pain and loudness are processed at different levels within the auditory system, it is possible that pain sensations could be triggered before loudness sensations develop.
The link between loudness and pain is currently unknown. As described in Pain Thresholds, pain from high intensity sound is normal and some suspect that those with hyperacusis have this pain triggered prematurely. The big questions are where is this pain signal generated, where is it processed, and how is it eventually sent to the pain centers of the brain?
The most simple, robust, and common way that pain signals are generated throughout the body is through sensing of cellular damage. As described in Inner Ear: Pain Receptors, traditional pain receptors have not been found in the cochlea however recent evidence suggests there is a type of nerve in the cochlea that is behaving like a pain receptor. These suspected pain receptors are routed from the cochlea to the granule cells of the cochlear nucleus (the auditory system’s first processing center). Wherever the pain signal is generated it would need to be processed. It is feasible that a hyperreactive pain processing center could reduce pain thresholds and create the sensation of localized pain in the ears. There may also be a scenario similar to phantom limb pain where the disconnection of pain receptors results in hyperactivity of pain processing centers (phantom limb patients sometimes report a burning sensation in the referred area just as hyperacusis patients sometimes do).
The recent hyperacusis literature review mentions the following about potential pain pathways:
“Pain information ascends to the brain through two main pathways and is interpreted by different brain structures. One path goes from the spinal cord to the thalamus and ends in the somatosensory cortex, and the other goes from the brain stem to the insular cortex through the amygdala (Basbaum, Bautista, Scherrer, & Julius, 2009). Glutamate, an excitatory amino acid, is the main neurotransmitter in the pain pathway (Julius & Basbaum, 2001; Pappagallo, 2005). Changes in pain intensity are processed in contralateral somatosensory and insular cortex (Rainville, 2002), but the anterior cingulate cortex is the main area thought to be responsible for the interpretation of the emotional significance of the noxious input (Rainville, Duncan, Price, Carrier, & Bushnell, 1997). The brain has a descending pathway that involves the peri-aqueductal gray and anterior cingulate. These pathways are thought to regulate the pain-related effects, such as analgesia and behavioral responses (Fields, 2000; Rainville, 2002).”
-A Review of Hyperacusis and Future Directions by Tyler, Pienkowski, et al.
General ear pain (pain not worsened by sound) can occur in both hyperacusis and tinnitus patients alike after an acoustic shock. This has been associated with the set of middle ear related symptoms called tonic tensor tympani syndrome (TTTS). It has been suggested this pain and possibly sound induced pain occurs when the brain initiates unusual, hyperactive control of the middle ear muscles (tensor tympani and stapedius). As described in Potential Mechanisms: Middle Ear, there are unanswered questions if this is to be used to explain pain hyperacusis.
Pain is complicated and involves processing and feedback throughout the central nervous system. Further research into the cause of sound-induced pain specifically rather than loudness perception alone would provide much insight on pain hyperacusis.
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