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402 Disorders of the Auditory System
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sence of corresponding external acoustic
stimuli (Evers & Ellger, 2004). For many
years, auditory hallucinations were considered the domain of the psychiatrist or
clinical psychologist. However, recently
there has been a growing interest among
professionals in the field of audiology
perhaps related to two factors: (1) auditory hallucinations are not only seen in
people with psychiatric problems but also
in those with auditory difficulties, and
the experience of auditory hallucina-
(2)
tions can be viewed as an auditory disturbance for which there is an anatomic and
physiologic correlate. Individuals who
suffer from auditory hallucinations without any comorbid psychiatric illness have
to be considered to have a form of auditory dysfunction. It also seems reasonable
that, even in patients with psychiatric illness, the auditory system is involved in
generating the hallucinations. Individuals with auditory hallucinations do perceive sound in some form; therefore, the
auditory perceptual mechanism must be
activated in some manner. This activation
is supported by functional imaging studies as will be discussed later. In this brief
review, auditory hallucinations related to
drugs and parkinsonism, although mentioned, will not be addressed in detail as
such coverage would be beyond the scope
of the present discussion of this particular
symptom.
Auditory hallucinations come in many
forms and can be perceived as whistles,
bangs, clapping, ticks, screams, voices,
intelligible or unintelligible speech, singing, and instrumental music, as well as
other permutations of sound (Bentall,
1990). The definition and many of the
examples of the perceived sounds in auditory hallucinations could, in part, be confused with tinnitus; although most would
agree that tinnitus, as it is commonly rec-
ognized, would seldom take the form of
voices, singing, speech, or music. In addition, there can be auditory hallucinations
that are perceived as multiple sounds
simultaneously or as different sounds that
are perceived at different times. In many
cases, however, the sounds heard are similar for each instance of an auditory hallucination (Musiek et al., 2007).
Symptoms
Like tinnitus and hyperacusis, an auditory hallucination is a symptom. It could
be associated with a peripheral or central
auditory problem and/or with a psychiatric disturbance. In some cases, hallucinations in other sensory modalities (primarily visual) can co-occur with auditory
hallucinations. The experience of auditory
hallucinations can be quite disturbing to
the individual. As a result, the individual
may become nervous, tense, irritated,
and/or worried (Tien, 1991). This psychological “baggage” makes the hallucinations much worse.
Incidence and Prevalence
Studies on the prevalence of auditory hallucinations show statistics that are higher
than one might expect. In a large sample
of adults ranging in age from young to
old, between 2% and 3% reported experiencing auditory hallucinations (Remschmidt, 2002). Tien (1991) reported the
incidence of auditory hallucinations also
to be in the 2% to 3% range and the prevalence to be between 10% to 15%, with little
influence of age until the 8th decade of
life. The most commonly reported auditory hallucination is “hearing” voices
(Sacks, 2012). In addition to the incidence
and prevalence data reported previously,
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Tien (1991) also reported that auditory
hallucinations were more common among
women than men and that visual hallucinations were the most frequently reported
hallucinogenic symptom, followed by
auditory, somatic, and olfactory hallucinations. It is notable that prevalence of
auditory hallucinations ranges from 60%
to 80% in the schizophrenic population
(Lim, Hoek, Dean, & Blom, 2016). A factor
potentially influencing the incidence and
prevalence of auditory hallucinations is
tinnitus. Tinnitus is sometimes difficult
to discern from auditory hallucinations,
especially in its more complex forms. It
therefore may be mistakenly identified
as an auditory hallucination rather than
as tinnitus.
Etiology and Pathology
As previously stated, auditory hallucinations frequently are associated with
psychiatric disorders, but they also can
be related to peripheral and/or central
involvement of the auditory system. In
regard to psychiatric disorders, as mentioned earlier, schizophrenia is the condition most commonly associated with
auditory hallucinations (Lim et al., 2016;
Shergill, Murray, & McGuire, 1998).
Depression, compulsive disorder, and a
host of other psychiatric symptoms have
also been linked with auditory hallucinations, but the coincidence is extremely
small. Long-standing moderate to severe
hearing loss could be the basis for some
auditory hallucinations, especially in the
elderly population (Berrios, 1990). This is
likely related to what can be a long duration of auditory deprivation secondary
to the hearing loss. There also have been
many reports linking focal brain lesions
(epilepsy, tumors, strokes) and degenera-
tive diseases to the occurrence of auditory
hallucinations (Evers & Ellger, 2004; see
Musiek et al., 2007). A summary of possible causes of auditory hallucinations can
be found in Table 8–2.
The pathophysiologic mechanisms
underlying auditory hallucinations are
unknown. However, the leading theory
seems to be one of reduced neural connectivity and the existence of random neural
discharges in the auditory regions of the
brain. In brief, the reduced neural connectivity is presumed to be related to a loss
of neural connections as a consequence
of deprivation, damage, aging, and other
mechanisms, which results in regions of
the brain functioning in isolation (i.e., not
appropriately connected to other brain
regions) and randomly creating perceived
sounds. The neural discharge theory proposes that (damaged) neural generators in
the auditory cortex similar to epileptic foci
give rise to the firing of neuron groups
that results in the auditory hallucination
(Alderson-Day et al., 2016; David, 1994;
Musiek et al., 2007).
Site of Lesion
It is logical and likely that auditory hallucinations are caused by compromise
of the auditory cortex and other related
brain regions. The classic human neurosurgical study performed by Wilder Penfield and his colleague (Penfield & Perot,
1963) demonstrated that auditory perceptions can be triggered by electrical stimulation of the auditory cortex. This finding
opened the door to the likelihood that the
auditory cortex could play an integral
part in the occurrence of auditory hallucinations. As was alluded to earlier, damage
to the central auditory nervous system has
been linked to auditory hallucinations in a
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Table 8 –2 . Examples of Medical, Psychotic/Psychological, and Transient Conditions
That Can Cause Auditory Hallucinations
Type Possible Causes
Medical Medical Disease or Surgical Complications
• Delirium, metabolic disorders, sepsis, heart failure, postoperative
and posttraumatic states, high fevers and infections, thyroid
disease
Medication- and/or Substance-Induced
•
Side effects
• Hallucinogens, hallucinosis
Ear Disease
• Hearing loss
Disease of the Nervous System
• Alzheimer’s disease, dementia, Parkinson’s disease, cerebral
vascular disease, tumor, abscess, contusion, subdural hematoma,
meningitis, encephalitis, migraine headaches, epilepsy
Psychiatric/
Physiological
Transient Sleep-Wake Disturbances
Source: Based on Chaudhury (2010), Prerost, Sefcik, & Smith (2014), and Traynor (2018).
temporal manner in many patients, with
these perceptions occurring at the time of
or shortly after the event (e.g., during or
following a stroke).
Perhaps the most compelling evidence for a central nervous system locus
for auditory hallucinations comes from
anatomic and functional imaging stud-
Substance-Related Disorder
• Alcohol intoxication/withdrawal
Psychotic Disorder
• Schizophrenia, affective disorders (severe depression, mania),
dementia, postpartum psychosis, borderline personality disorder
Posttraumatic Stress Disorder
Intense Emotional Stress
Hypnagogic, hypnopompic
•
Deprivation (sleep, food, or sensory)
Bereavement
Prolonged Isolation
ies (Highley, McDonald, Walker, Esiri, &
Crow, 1999; Shergill et al., 2004). Anatomic
studies point toward smaller auditory
cortices in individuals with schizophrenia
and auditory hallucinations. Functional
magnetic resonance imaging (fMRI) studies have shown increased cortical activity
in the left inferior frontal gyri and right
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middle temporal gyri that occurred prior
to and during the perception of an auditory hallucination. In addition, activation
of the left insula (structures that are highly
auditory in nature) occurred with the perception of the hallucination. There is also
evidence which demonstrates a correlation between the gray matter volume in
the left temporal lobe (left superior temporal and Heschl’s gyrus) and the severity
of auditory hallucinations (Modinos et al.,
2013). In addition, there have been reports
that argue that the brain activity related
to an auditory hallucination could be subcortical, but it is likely to involve complex
interactions between the brainstem and
cortex (see Musiek et al., 2007).
Medical and Audiologic
Evaluation
The medical evaluation of hallucinations
requires a psychiatric and/or neurologic
consult. If the patient has no psychiatric
problems, the focus should be on neurology; however, if the patient is at risk for
a psychiatric condition, then the psychiatrist becomes the key professional. The
focus of both of these professionals is to
find the underlying cause. For example, if
a person suffered a temporal lobe stroke
and auditory hallucinations appeared in
the same time period, the objective following evaluation would be to treat the
stroke. Often, however, there is no clear
underlying cause, especially in psychiatric cases. A thorough medical and psychiatric history is essential. It is important that drug use be ruled in or out as a
cause of the auditory hallucination. Longstanding, severe hearing loss can also be
a factor that needs to be considered, especially in the elderly. Details of the medical
and psychiatric evaluation of patients pre-
senting with auditory hallucinations are
beyond the scope of this chapter. For more
information on these topics, see Griswald,
Del Regno, and Berger (2015).
There is a paucity of data on the
audiologic assessment of auditory hallucinations. Clearly, the direct evaluation
of auditory hallucinations is difficult.
Perhaps the most direct approach would
be to try to mask the auditory hallucinations. In one of the author’s (FM) experience, masking of an auditory hallucination can be accomplished, but much
depends on the specific type of auditory
hallucination that the patient is experiencing and how well the masker matches the
type of sound(s) composing the auditory
hallucination(s). Perhaps the most useful
audiologic evaluation of auditory hallucinations is not the evaluation of the hallucination itself but rather the audiologic
evaluation of the integrity of the central
auditory nervous system. This approach
assumes the auditory hallucinations are
related to dysfunction of the central auditory system.
There have been some studies of dichotic listening, speech-in-noise recognition performance, and auditory evoked
potential assessments that have demonstrated differential performance for individuals with schizophrenia and auditory
hallucinations when compared to groups
of subjects without auditory hallucinations. These studies have essentially taken
two approaches. One is that performance
of subjects with auditory hallucinations
has been compared to either normal controls (Løberg, Jørgensen, & Hugdahl,
2004) or to a group of normal controls and
a group of subjects with schizophrenia
without auditory hallucinations (McKay,
Headlam, & Copolov, 2000). The second
approach assessed subjects who have
intermittent auditory hallucinations while
406 Disorders of the Auditory System
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they are experiencing hallucinations and
when they are not (Tiihonen et al., 1992).
Those with schizophrenia and auditory
hallucinations, as a group, performed
more poorly than the other groups (see
Musiek et al., 2007, for a more detailed
review of these studies). This poor performance on central auditory tests is likely
related to the possible degenerative neural process that accompanies schizophrenia and auditory hallucinations. This link
is an important one and one that is consistent with the literature on central auditory evaluation. That is, the relationship
between reduced central auditory function
as measured by central tests (with proven
sensitivity) and reduced neural substrate
has been well established. Although more
work is needed, there clearly is emerging evidence showing a link between
reduced volumes of auditory cortex (and/
or related areas) and those with auditory
hallucinations and schizophrenia.
Models for the Generation
of Auditory Hallucinations
As has and will be mentioned again later,
auditory hallucinations can be triggered
by neurologic disorders — especially those
affecting the central auditory system. Also,
hearing loss, aging, and sound deprivation from communication seems to be
linked to auditory hallucinations. However, perhaps of greater interest are the
models for the underpinnings of auditory
hallucinations in those with schizophrenia. There are many models that have
been proposed but here only two of the
more popular ones will be discussed. One
model is the inner speech model (ISM),
sometimes termed the mis-attribution
model. The other is the theory of reduced
connectivity, also termed the abnormal
auditory cortex activation model. The
ISM model is based on the idea that the
patient with auditory hallucinations cannot distinguish from internally generated
perceptions and externally generated
ones (Waters et al., 2012). The connectivity model is one that focuses on abnormal
neural discharges from the auditory cortex and/or other central auditory areas
as the basis for the hallucinations. These
abnormal discharges in turn result in poor
connectivity among neurons and neuronal
pathways in the brain. This “misfiring”
of fibers and the lack of proper conduction of electrical impulses in the auditory
system may be perceived as words, music
sounds, or other auditory sounds by the
individual with schizophrenia. Although
this model was proposed to explain the
basis for the auditory hallucinations experienced by patients with schizophrenia, it
also fits the neurologic and hearing loss
etiologies (see Alderson-Day, McCarthyJones, & Fernyhough, 2015, for review).
Medical and Audiologic
Treatment
Treating underlying medical disorders is
the first route to help those with auditory
hallucinations. These underlying causes
could encompass a number of disorders
or conditions, ranging from high fevers to
trauma. Medical intervention is key if the
underlying cause is found. Although one
of the most common provoking causes is
the illicit use of hallucinatory drugs, several prescribed medications can also trigger auditory hallucinations. Treatment
for auditory hallucinations in these cases
typically involves the cessation of the use
of the drug or medication, and in some
8. Tinnitus, Hyperacusis, and Auditory Hallucinations 407
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cases, the prescription of an alternative
medication. Such approaches can often
reduce and/or arrest the auditory hallucinations. There are also pharmacologic
agents that are used to treat auditory hallucinations. For example, dopamine cholinesterase inhibitors have been shown
to be useful in treating hallucinations in
some patients (Korczyn, 2001). However,
in many cases, the cause of the auditory
hallucination cannot be determined, and
in other cases, the origins of the hallucination may be identified, but no medical treatment is available. In these cases,
other forms of therapy have been tried
with varying degrees of success.
Shergill et al. (1998) reviews a number of nonmedical therapies for auditory
hallucinations. Counseling and education of the patient appear to have positive results for some patients. In addition,
relaxation therapy, distraction techniques,
mood monitoring, and discussion classes
have all been tried but have not proven
to be highly successful. More studies on
the effectiveness of these therapies are
needed before these approaches are routinely recommended.
One treatment that seems to hold
some promise for controlling auditory
hallucinations is transcranial magnetic
stimulation (TMS) (Koops, van den Brink,
& Sommer, 2015). This procedure is a noninvasive technique used to stimulate various regions of the brain. A magnetic coil
applied to the scalp generates a current
that passes through the scalp and stimulates brain tissue (Haraldsson, Ferrarelli,
Kalin, & Tononi, 2004). This technique
has approximately a 50% success rate.
However, many investigators feel its full
potential in the treatment of hallucinations has not been realized (Haraldsson
et al., 2004).
Interestingly, acoustic treatments have
been tried with patients with auditory hallucinations with mixed results (Collins,
Cull, & Sireling, 1989; Nelson, Thrasher,
& Barnes, 1991). The use of sounds of various types to distract the patient’s attention
from the hallucination has been employed
as an intervention strategy. In some cases,
this intervention has worked to a moderate degree but, in other patients, this
approach was not effective. Masking is
also a consideration that could potentially
help some patients. In individuals with
long-standing hearing loss, deprivation is
potentially a key factor and the fitting of
amplification could be a major help.
summaRy
Tinnitus, hyperacusis, and auditory hallucinations are all auditory disorders/
symptoms that affect many people and
are of concern to the hearing health professional. None of these disorders/symptoms has a cure at this time, but they all
can be managed to some extent. Theories abound regarding their underlying
pathophysiologies. However, none of
these theories account for the many differences that often exist between patient
reports and their persistent difficulties.
Nonetheless, progress is being made in
these areas, especially with the use of
functional imaging techniques. As a result
of the progress that has been made, it has
become increasingly clear that the brain
is more involved in these symptoms and
their underlying disorders than has been
previously appreciated. This understanding, coupled with further research, could
lead to advances in both the diagnosis
and management of these three auditory
408 Disorders of the Auditory System
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disorders/symptoms. The importance
of careful and insightful audiologic,
otologic, and neurologic evaluations of
patients with tinnitus, hyperacusis, and/
or auditory hallucinations cannot be overstated. This triad of hearing disorders/
symptoms highlights the importance of
the ear–brain relationship and the need to
have several professionals involved in the
assessment and management of patients
with these disorders/symptoms.
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