Musiek, Frank; Ballingham, Tee Marie; Liu, Barry; Paulovicks, Jennifer; Swainson, Brooke; Tyler, Kevin; Vasil, Kristin; Weihing, Jeffrey
Auditory hallucinations (AHs) are often associated with psychiatric illness. However, there are individuals without psychiatric disorders who experience auditory hallucinations. In these cases, one should consider direct involvement of the auditory system.
Even in patients with psychiatric illness, it is reasonable to assume that the auditory system plays a fundamental role in AHs. Since these patients perceive sound in some form, the perceptual mechanism for sound must be activated, at least in part, in a similar fashion as when one hears external acoustic stimuli. Although sound waves are not associated with what a person with hallucinations hears, the person does perceive sound nonetheless. Sometimes certain external sounds will result in, or trigger, a hallucination. However, in these cases the hallucination is different from the external acoustic stimulus.
Functional imaging techniques such as positron emission tomography (PET) and functional magnetic resonance imaging (fMRI), along with sophisticated audiological techniques, have begun to show central auditory system activity related to AHs (discussed later in this article). As a result of this new research, as well as the intriguing nature of psychiatric and non-psychiatric AHs, more audiological clinicians and researchers have become interested in this disorder. Therefore, now more than ever, there are psychiatrists, auditory clinicians, and scientists trying to understand this perplexing phenomenon.
The purpose of this article is to review and synthesize clinical and research information on auditory hallucinations from an audiological perspective. In addition, we would like to develop the notion that perhaps audiology could and should play a role in the evaluation, treatment, and investigation of AHs.
WHAT ARE AUDITORY HALLUCINATIONS?
Bentall defines hallucinations as perceptions that lack an external stimulus, have the full impact of an actual perception, and are not under voluntary control.1 Hallucinations have been reported to occur for all five senses. Auditory hallucinations are auditory perceptions that are experienced in the absence of corresponding external acoustic stimuli.2,3 AHs can be whistles, bangs, clapping, screams, ticks, voices producing intelligible or unintelligible speech, and music (instrumental, singing, or both).
There are two definitions relating to AHs that could be confused. One is the difference between pseudohallucinations and true hallucinations. Pseudohallucinations have been referred to as sounds perceived inside the head that have no correlation to the outside world, while true hallucinations are considered to be actual perceptions that have an association with the external or objective environment.4 However, studies by Oulis et al.5 and Copolov et al.4 showed there was a mixture of pseudo- and true hallucinations in a large number of patients with AHs and concluded there was little value in differentiating true from pseudohallucinations. This is the position we are taking here on this issue.
The other term that could easily be confused with auditory hallucinations is tinnitus. Tinnitus can be an auditory perception without an external stimulus and, therefore, could be considered an auditory hallucination. Tinnitus is often a humming, tonal-type sound of any pitch and, in some cases, more than one pitch. However, tinnitus can also be a pulsing, clicking, or frying (noisy) type of sound. It may be subjective (i.e., only the person with the tinnitus can hear it) or objective (i.e., others can hear it). Auditory hallucinations can be easily differentiated from objective tinnitus in that AHs are heard only by the person who has them.
Auditory hallucinations can be distinguished from subjective tinnitus in that tinnitus is seldom heard as voices, speech, music, or songs. However, according to Bentall's definition of AHs, perceptions of tones, clicks, noise, etc. not related to external stimuli could be either hallucinations or subjective tinnitus.1 Therefore, the two terms may be better differentiated by considering etiology. Unlike AHs, subjective tinnitus is often a result of damage to the inner ear, while the assumed generators of AHs are in the central nervous system (CNS). However, since tinnitus can also result from damage to the CNS even etiological site does not allow us to differentiate tinnitus from AHs consistently.
PREVALENCE OF AHs
The prevalence of AHs is greater than one might expect. In a sample of 18,572 community residents above 18 years of age, between 2% and 3% said they had experienced AHs.6 Auditory hallucinations occurred more often in women than in men and prevalence increased with age.
A study focusing on the prevalence of AHs in the elderly reported that 32.8% of this age group had experienced hallucinations.7,8 A possible issue with these studies relates back to the tinnitus versus AHs dilemma. It would be important for prevalence studies to make sure a differentiation between tinnitus and AHs is made as clear as possible to the respondents. Since tinnitus is more common than AHs, an unclear differentiation could result in a higher reported incidence of AHs. It also should be understood that many of the people who report AHs experience them so rarely that they are not a problem for them.
TYPES OF AUDITORY HALLUCINATION
As mentioned earlier, there can be a wide variety of sound perceptions in AHs. From an organizational perspective, categories of “formed” and “un-formed” seem logical and worthwhile.9,10 Formed AHs are the more complex hallucinations such as verbal and musical AHs. The perceptions of clicks, tones, chords, whistles, and other noises that vary in loudness, pitch, and timbre are classified as unformed AHs. These are often irregular and similar to tinnitus-type sounds.
Let's focus first on two types of formed AHs—verbal and musical.8 Verbal AHs are commonly associated with schizophrenia. They can vary among many dimensions, including internal or external location, acoustic clarity, number and gender of voices, linguistic complexity, time course, and associations with other hallucinations.3,8 Verbal AHs are most often first noticed by subjects in their mid-teens or 20s.11 Psychiatric and non-psychiatric groups hear hallucinations with the same physical characteristics; however, the psychiatric patients hear voices with more negative connotations than do the non-psychiatric groups.3
Musical AHs are less common than verbal hallucinations. This may be because most patients with schizophrenia have verbal AHs. Musical AHs are usually repetitive musical patterns that can be purely instrumental or may include lyrics. Most of the time, the music is familiar to the individual. Various kinds of music have been reported, ranging from religious to popular. The most common reaction to musical AHs is to find them frightening, rather than soothing or pleasant.2 Musical hallucinations are more common among women than men, and the average age of onset is around 60 years.
Another type of AHs is functional.12,13 Functional AHs, which are typically formed, seem to be found only in schizophrenic patients and are hallucinations that occur simultaneously with environmental stimuli. Hunter and Woodruff profiled an individual who heard voices whenever he heard a motor vehicle engine.12 Television and radio are common triggers of functional AHs.
Experiential AHs are yet another type. These are hallucinations that are evoked by external electrical stimulation of the auditory cortex and can be formed or unformed.14,15 The subject of experiential AHs brings to mind Penfield's classic studies of the auditory cortex nearly half a century ago.15,16 Penfield, a renowned neurosurgeon, conducted research, mostly on epileptic patients, that involved electrical stimulation of the temporal lobe during surgery.
During electrical stimulation at various loci on the temporal lobe, the patients would report “hearing” sounds such as buzzing, humming, ringing, or hissing, as well as music or speech. They heard music on both sides of the brain, but more often in the right hemisphere than the left. Verbal information was also heard in both hemispheres, but more often on the left side. In general, stimulation of the cortex resulted in the patient localizing the sound in the contralateral ear. Patients would often hear voices and words, but could not understand what was being said. Some heard singing, humming, and, sometimes, identifiable songs.
Might the auditory experience of Penfield's patients be the same as the AHs we have been discussing? Perhaps, since electrical stimulation resulted in AHs, a physiological link can be made. That is, the electrical stimulation caused auditory neurons to fire without any input from the auditory periphery. It could be assumed that the discharging neurons are the same neurons that would fire if stimulated by impulses coming from the auditory periphery in a regular hearing situation. If so, then AHs have an identifiable auditory physiological basis. Such a basis may allow us to study AHs using a framework similar to that used for other auditory disorders.
POSSIBLE BASES OF AUDITORY HALLUCINATIONS
Let's now discuss some theoretical pathophysiological mechanisms that may be the basis for AHs, along with disorders that may be responsible for AHs. It should be emphasized that, although auditory hallucinations are commonly associated with psychiatric illnesses such as schizophrenia, they can also occur in numerous non-psychiatric disorders. Of these, peripheral or central auditory problems are probably the most common.
One mechanism that has been proposed to explain AHs is reduced neural connectivity.17 Reduced connectivity occurs when certain areas of the brain (neurons) lose key neural connections to other parts of the brain. This results in these areas of the brain functioning autonomously and leading to, for example, (internal) speech production and perception without self-monitoring. This could occur as a result of deprivation or of damage to certain areas of the brain.
The theory of reduced connectivity could be extended to include a second theory proposed by David.18 His theory, similar to Evarts's,19 posits that a generator within the auditory cortex (similar to an eleptiform focus) gives rise to AHs. In other words, there are strong pathological neuronal discharges from auditory areas of the brain. These could be related to a number of neurological or psychiatric disorders, including deprivation, stroke, tumors, and degenerative diseases.
Another proposed mechanism for AHs relates to the inability to distinguish between internally and externally generated sound and may be related to a cognitive control deficit in the frontal lobe.20 Related to this mechanism is reduced social conversation, which makes the brain more likely to produce hallucinatory conversations.21 For instance, hearing loss often causes elderly people to withdraw from conversations rather than seem not to understand what is being said. This results in restricted social interactions and may contribute to AHs.
The final possible mechanism is a combination of two theories. We propose that this combination is feasible and logical. There are several scenarios that could apply here. One is that AHs are a result of the misperception of internally self-generated speech (or music) for externally generated speech (or music). The key here is the failure to recognize that internal speech is not external. This could be a cognitive problem. This, combined with an abnormal generator in the auditory regions (secondary to reduced connectivity), may make the internal representation stronger. This condition could be enhanced by a heightened emotional state that prompts the brain to produce information (hallucinations) consonant with the emotional state. We suggest that a heightened emotional state promotes confusion between internal and external speech.
As mentioned earlier, psychiatric illnesses are associated with AHs. It is difficult to say if there is a cause and effect relationship since not all people with psychiatric disorders have AHs. The most common psychiatric disorder associated with AHs is schizophrenia. AHs occur in about 60% to 80% of those diagnosed with this psychiatric problem.22 It has been said that auditory-verbal hallucinations are a cardinal feature of schizophrenia.23 Other mental disorders, including depression, obsessive-compulsive disorder, and other neurotic symptoms, have also been linked with AHs, but to a much lesser degree than schizophrenia.
The mechanisms underlying AHs and schizophrenia could be reduced connectivity and/or a heightened emotional state. Hearing loss, especially in the elderly, is a non-psychiatric disorder that can be a trigger for AHs. The mechanism here is likely sensory deprivation. Gradual onset of AHs has been shown to be associated with increased hearing loss.24 Often it is elderly women with moderate to severe hearing loss who experience AHs.2
Otosclerosis has been noted in individuals with AHs. Interestingly, in several instances, surgery to correct the hearing loss associated with otosclerosis resulted in arresting the AHs.25
These studies are important for two reasons. First, they illustrate that auditory deprivation may play a key role in AHs. Secondly, since otosclerosis is essentially a conductive hearing loss, these findings demonstrate that both sensorineural and conductive losses can lead to AHs. This fact supports the hypothesized deprivation mechanism, since both types of hearing loss deprive the central nervous system of stimulation. Although investigators are still pursuing the question, it appears that considerable bilateral hearing loss must be present for deprivation to evolve.24
Hammeke, McQuillen, and Cohen reviewed two cases of auditory hallucinations that were closely linked to hearing loss.10 In neither patient was there evidence of psychiatric disturbance, epilepsy, or dementia. The AHs were characterized by irregular sounds with varied pitch and timbre that could have been attributed to tinnitus. However, the patients also heard singing and music of different types.
One patient described her hallucinations as loud, vivid music that became more frequent over time. She heard the AHs in both ears and said they consisted of repetitive singing by one person or by a choir with the non-vocal music played by one instrument or by an orchestra. She perceived the songs as hymns she learned as a child and as nonsense melodies.
The patient in the second case had experienced a buzzing tinnitus for many years before the AHs began. After an incident of exposure to extremely loud traffic noise, she began to hear noises in her head that sounded like a boiler factory. After a while, her hallucinations turned into the song Jingle bells, interspersed with an occasional prayer or a voice calling her nickname. This auditory hallucination sequence has been repeating ever since.
In both these cases, the AHs began after several years of progressive hearing loss and eventually became constant. The hallucinations were more bothersome to the patients when they were either mentally inactive or in quiet surroundings. It seems likely that tinnitus was present.
In many cases of peripheral hearing loss, it is impossible to be certain that the central auditory nervous system (CANS) is not also compromised. Damage to the CANS could be linked to the AHs. As we have learned, auditory deprivation primarily affects the CANS, resulting in possible degeneration and reorganization.26 Hence, the mechanism may not be deprivation alone, but also reduced connectivity secondary to central auditory system dysfunction.
Focal brain lesions involving the central auditory system—especially the left hemisphere—have been associated with AHs.2 Lesions typically caused by epilepsy, tumors, strokes, and degenerative diseases have all been associated with AHs. For the most part, these seem to have a locus in the CANS pathway.2,23 This is revealing in that it supports the idea of auditory system involvement in cases of AHs.
The temporal course of brain lesions linked to AHs is also of importance. Berrios reports that often the onset of AHs is related to the onset of a CNS lesion such as a stroke.22 In a case encountered by the first author, the onset of a right temporal lobe stroke also marked the onset of musical hallucinations, which disappeared when the patient began to recover.
Braun relates that in neurogenic AHs the lesions are essentially in the auditory pathways.21 Therefore, we would argue against the “inner speech theory,” which contends that it is the auditory and not the speech regions that seem to be involved. Auditory hallucinations have been linked to temporal lobectomy. Specifically, a patient in his 60s began to hear word hallucinations about a week after a right temporal lobectomy.27
Individuals with epilepsy that involves the auditory areas of the brain can experience an auditory aura before the seizure. These auras can result in the perception of various sounds, music, and/or speech. The auras are very similar to descriptions of auditory hallucinations, and may be better classified as such. Penfield and Perot stated that auditory or visual hallucinations sometimes are experienced by patients with seizures.15 They noted that these hallucinations can be produced by electrical stimulation of the cortex during neurosurgery.
Alcohol and drug intoxication have been related to AHs.2 Among the more common drugs associated with auditory hallucinations are quinine, salicylates, phenytonin, benzodiazepine, triazolam, pentoxifylline, propanol, clomipramine, amphetamine, triazlam, and marijuana. Lysergic acid diethylamide (LSD) and mescaline were investigated in the 1960s. These were both hallucinatory drugs and were powerful cerebral synaptic inhibitors.28 Interestingly, similarities between drug-induced hallucinations and hallucinations related to psychoses have been noted.29
Extreme hunger, thirst, lack of sleep, and lack of oxygen have also been reported to cause AHs.30 Not surprisingly, tension, anxiety, and stress seem to make AHs more common and more intense.
AUDIOLOGICAL ASSESSMENT OF PATIENTS WITH AHs
Since auditory hallucinations appear to be linked to the auditory system in several ways, it is only fitting that evaluation of the auditory system be performed on patients with AHs. The focus of most of these studies of audiological status is the central auditory system, and rightly so. The central auditory system is the likely site of the types of interactions that may produce AHs. Therefore, behavioral and electrophysiologic tests of higher auditory function have been employed to learn about the central auditory system and AHs (see Figure 1).
One theory regarding underlying mechanisms of AHs that was mentioned earlier is reduced (neural) connectivity, which likely results from damage to the auditory system and its neural connectors to other areas of the brain. Central auditory tests are designed to detect dysfunction of the central auditory system and could be important in learning how auditory dysfunction may be linked to AHs.
One of the key issues surrounding AHs and central auditory assessment is that schizophrenic patients both with and without AHs may perform poorly on tests of higher auditory function. This is likely related to the fact that schizophrenia can result in degeneration of neural tissue in the temporal lobe.23 In studying central auditory function in these populations, it has become important not only to have a control group, but also to include subjects with schizophrenia both with and without AHs.
Investigations of AHs have used various central auditory tests. The most revealing data have come from dichotic listening tests. Loberg, Jorgenson, and Hugdahl tested a variety of dichotic listening conditions and showed differences between schizophrenic patients with and without AHs in one condition.31 This was a free recall condition that demonstrated better performance in the left ear for the AH patients.
Conn and Posey conducted a similar study, but one that used not schizophrenic patients, but college students who had verbal hallucinations based on Barrett's questionnaire.32 Again, there was a significant difference between the AHs and non-AHs groups. However, the difference was seen in the right-ear scores not the left, as in the Loberg et al. study.32 In a speech-in-noise study, schizophrenic subjects with AHs scored lower than both schizophrenic subjects without AHs and controls.33
Auditory evoked potential studies have shown some interesting results with AH patients. Lindstrom et al. found that ab-normal auditory brainstem responses were reported by nine of the eleven patients with schizophrenia and AHs, but by only one of the nine who had schizophrenia but not auditory hallucinations.34 Lindstrom and colleagues stated that the ABR abnormalities could not have been related to peripheral hearing loss or medications. They proposed some possible brainstem pathological findings in schizophrenic patients that could be a basis for AHs. For example, post mortem studies have shown glial knots and perivascular infiltration in persons with schizophrenia. This kind of pathology could result in abnormal ABRs. In a recent study, Nam found that three out of eight schizophrenic patients with AHs yielded abnormal ABRs (one with an absent Wave I and two with extended central conduction times).35
Both Lindstrom et al. and Nam implicate the auditory brainstem pathways as playing a role in AHs. This notion gains support from Cambier et al.,36 who reported five cases of brainstem lesions that apparently linked AHs to the lesions. Interestingly, in a much earlier publication, Scheibel and Scheibel argued that the reticular core of the brainstem could play a role in hallucinations.37 It pointed out that the reticular activating system in the brainstem projects and influences the cerebrum in a variety of ways, including possible hallucinatory experiences.
Tiihonen et al. examined results for late potentials in cases of AH.38 They found that the N1 latency increased during the hallucinations from when there were no hallucinations. In another study, N1 and P2 late potentials were recorded in controls and schizophrenics with AHs. These potentials were obtained in silence and with the subjects talking to themselves. The N1 was unaffected in the talking condition for the schizophrenic subjects, but was reduced for the control group. The P2 showed no group effects.39
These behavioral and electrophysiologic central auditory test procedures may provide insight into the nature of auditory hallucinations. The benefit would be considerable if more studies included non-schizophrenic auditory hallucination subjects and controls. However, regardless of how well the subjects are defined, there remains a paradox in that many non-schizophrenic subjects experience AHs related to some kind of neural damage or dysfunction. Central auditory tests are sensitive to this dysfunction, whether or not it is causing AHs. Hence, the question arises, is it the neural damage or the hallucinations that drive the abnormal test scores? That's somewhat like asking, which came first, the chicken or the egg?
Also of significance are emerging data that may indicate that abnormalities of the brainstem auditory pathways play a role in generating AHs. It might seem that the auditory areas of the brainstem are located far from perceptual centers that could give rise to hallucinations. On the other hand, perhaps the brainstem abnormality could have led to distortions of the acoustic pattern that precipitated an abnormal conversion in the perceptual centers in the cortex from sound to voices and music. The possibility that the brainstem may be responsible for AHs deserves more research and clinical attention.
FUNCTIONAL IMAGING AND AUDITORY HALLUCINATIONS
There is no question that functional imaging studies such as functional magnetic resonance imaging (fMRI) and positron emission tomography (PET) have recently made contributions to our understanding of AHs (Figure 2). Functional imaging studies have provided possible lesion sites and a time course for AHs. In addition, imaging studies have served to provide a possible anatomical and physiologic basis for this elusive entity.
The fMRI studies have shown in-creased cortical activity during AHs. This increased activity is localized in both middle and superior temporal gyri in both hemispheres, as well as in the left insula and left inferior frontal gyrus.23 This indicates that both auditory perceptual areas and speech-generation areas are activated during AHs. It is interesting to note that in many cases the inferior frontal gyrus and right middle temporal gyrus were activated 6 to 9 seconds before the AHs were perceived.23 There also was ongoing insular activity as well as fronto-orbital activity after the hallucinations abated. This type of activation pattern seems to be relatively common in cases of AH. This pattern, by virtue of its anatomy, strongly implicates the auditory areas of the cerebrum in the generation and perception of AHs.
Another recent article reported on the use of fMRI to view activity in the higher cortical white matter in people with and without AHs.40 In patients with AHs, there was more activity in the temporoparietal areas of the arcuate fasciculus and anterior corpus callosum than in those without hallucinations (Figure 2). Could it be that the central auditory system is activated in much the same way, regardless of whether or not the individual experiences AHs? Or, is there some external acoustic stimulus that is heard? Perhaps auditory hallucinations are the misidentifications of endogenous, or imaginary, representations with an external or exogenous sound.
This thought leads to a question about imagining sounds such as music. When people imagine sounds, does the auditory cortex behave the same as when those sounds are actually heard? If sounds that are imagined are confused with externally generated sounds, could that be a hallucination? From a physiological standpoint, imagination, hallucinations, and actual hearing may be similar.
Studies from Zattore and colleagues may help us understand this. They used PET to study cortical activation in three conditions.41 One condition was to listen to a song played through a sound system and make a pitch judgment of two targeted words in the song. The second condition was to imagine the song and do the same task in silence. The last condition was a control condition without sound or imagining sounds.
Increased cortical activity of a similar pattern was noted for both the actual sound stimulation and the imagination conditions compared with the control condition. The activation areas included the temporal lobes (primarily superior temporal gyrus), parietal lobes, and frontal lobes. These activation patterns were slightly, but not markedly, different from activation patterns in the AHs mentioned above. Perhaps, as alluded to earlier, the experience of hallucinations may simply be the inability to distinguish an internally generated imaginary sound from an external sound. At the cortical level there may be little physiological difference among hallucinations, imagining sound, and hearing an external acoustic stimulus. On the other hand, it may be that the differences are so subtle that, given slight alterations in perception, emotion, and mental disposition, confusion arises.
DENTAL FILLINGS AND AUDITORY HALLUCINATIONS
As the first author's clinical experience has shown, AHs can be mistaken for an external acoustic stimulus that is transduced by a dental filling. A middle-aged patient complained of what he thought were AHs. A review of the patient's history revealed that the “hallucinations” began after he had visited a dentist to have a rather large cavity filled. The patient complained about hearing voices that seemed distorted, but sounded like someone reading a commercial or news report.
When it was suggested that the sounds could be radio signals transduced by his new filling, the patient was sure that was the case. The patient was referred back to the dentist, who modified the filling and the “hallucinations” stopped. These sounds, of course, do not fit the definition of AHs, but certainly this scenario is one that is confusing to patients and even professionals in determining what true AHs are.
AUDITORY HALLUCINATIONS IN CHILDREN
Auditory hallucinations occur in children in a manner similar to adults. Approximately 1% of non-psychotic children over 14 years of age have reported experiencing hallucinations (all types combined).42 Edelsohn et al. reported that of 62 non-psychotic children with AHs, 6 had only visual hallucinations and 32 had only auditory hallucinations.43 In this study, 24 children experienced a combination of auditory and visual hallucinations. These children, though not diagnosed with a psychiatric disorder, did have a co-morbid disorder (e.g., ADHD, depression, and/or disruptive behavioral disorder).
Children with schizophrenia are more likely to have AHs than those who are not schizophrenic. There is a 0.1% to 1% incidence of schizophrenia by age 10, and it increases at puberty, with no difference between male and females.44 Highly reliable epidemiological data are not available due to varying definitions of hallucinations and unclear differentiation from other childhood psychoses.45 However, it has been reported that between 60% and 80% of persons with schizophrenia have hallucinations.22 While, this finding was based on adults, it does provide some approximation of the incidence of AHs in children.
Treatment of auditory hallucinations is usually focused on ameliorating the underlying cause. This strategy is applied when the etiology can be determined with some level of certainty. Of course, in many cases it is difficult to determine the underlying cause. In this section, we will first address management of AHs when an underlying cause can be determined and then move into treatments that have a more general application when the specific cause and effect are not obvious.
As mentioned, there are illicit hallucinatory drugs (non-medically prescribed) that can cause AHs. Discontinuing their use will often resolve this problem, though not always immediately or completely.
There are also prescribed medications that can result in AHs. These can present a dilemma, since the patient may require the medication to manage a medical problem. For example, some treatments for Parkinson's disease, such as dopamine agonists, anticholinergic drugs, and antimuscarinic agents, have been shown to lead to AHs.46 A case study has been reported in which extra doses of oxycodone were linked to AHs.47 In this case, a patient treated with oxycodone for pain management experienced AHs, but the symptoms were reduced and ultimately eliminated when the drug dosage was cut back and then stopped entirely.
Kuykendall and Rhodes reported a case of drug interaction that apparently resulted in AHs.48 Meclizine, an anti-dizziness drug, and metaxalone, a muscle relaxant, were combined to treat a patient who soon afterwards reported hallucinations. When the patient took low doses of the two drugs or high doses of one drug and low doses of the other, the AHs ceased. Moreover, other combinations of medications with meclizine or metaxalone did not result in AHs.
Antifungal medications such as voriconazole have also been linked to AHs.49 There is a paucity of data of drug interactions related to AHs and, as a result, there is no comprehensive list of drugs that may cause hallucinations. There is also concern that auditory hallucinations may represent an “idiosyncratic reaction,” as opposed to a true drug interaction. Perhaps some patients are more prone than others to drug-induced AHs.
Treating disease processes linked to AHs is another important way to improve the condition. Two cases of AHs associated with Lyme disease were treated with ceftriaxone, an antibiotic. When treatment began to ameliorate the Lyme disease, the hallucinations stopped.50
Two cases of migraine headaches were temporally linked to AHs. The AHs appeared and disappeared concurrently with the migraine episodes.51
Roberts et al. reported on a patient with musical AHs who was found to have intracranial aneurysms.52 After the an-eurysms were clipped, the AHs ceased. In the first author's clinical experiences, a woman in her 60s suffered a stroke in the right hemisphere that seemed to be linked to the onset of musical hallucinations. As she recovered from the stroke, the hallucinations stopped.
When the underlying cause of AHs can be determined and treated, it seems reasonable to expect that the chance of eliminating the hallucinations is good. However, often the underlying cause of AHs is unknown or untreatable. Therefore, considerable effort has been directed toward developing therapies for such cases. We have categorized these therapies into several areas: (1) behavioral/cognitive, (2) acoustic, (3) transcranial magnetic stimulation, and (4) pharmacological.
Shergill et al. published a useful review of treatments for AHs, and their article is the basis for some of our comments and discussion here.22
One treatment for AHs is a focusing approach. The patient is asked to focus on the hallucinations and then discuss his thoughts about the AHs and their characteristics. Though at the initial stages this therapy did seem to help, long-term it was found not to be of great value.53
Another therapy involved helping patients understand the nature of AHs. They were encouraged not to try to suppress them, which often makes them worse, but to cope as best they could. This therapy did not stop the AHs, but it made them less disruptive of the patient's everyday activities.54
Therapy trials that involved relaxation training, discussion of AHs, and attempting to discriminate between externally and internally generated sounds were undertaken. Five patients underwent this 3-month therapy and felt they gained some control over their AHs. They also felt there was some decrease in the occurrence of the hallucinations.55
Shergill et al. reviewed a number of other cognitive therapies.22 These included distraction techniques and mood monitoring,56 which challenged beliefs about AHs, and counseling.56 Language-based therapy (e.g., discourse planning, reading aloud, conversations) and didactic education classes about AHs have been attempted, but with little success.57,58
Behavioral/cognitive therapy techniques for AHs suffer from relatively small numbers of studies and small sample sizes. In addition, the overall success rate is mediocre, at best. Given that AHs involve the auditory system, it may well be that acoustic interventions have a better chance at helping these patients.
Using one earplug and distracting oneself with external sounds or self-vocalization has been reported to help patients with AHs.59-61 In one study of 20 patients with AHs, 14 reported that listening to an external acoustic stimulus was helpful, while 8 found the earplug useful.59 Collins et al., had mixed results when they used an earplug in one ear and had the subjects listen to music, the news, and discussions.60
It is difficult from an auditory standpoint to understand how an earplug in one ear influences the perception of AHs. It might allow the patient to hear his or her own voice better through the occlusion effect, but it is difficult to envision any other advantage in regard to AHs. Shergill et al. relates that acoustic stimuli serve primarily as a distraction, which prevents the patient from focusing on the hallucinations.22 Auditory distractions seem to work reasonably well.
We would submit that, in addition to distraction, there is another phenomenon known as “auditory masking” that plays a role in helping these patients. Auditory masking is defined as one sound (the masker) interfering with or even obliterating the perception of another sound. In the first author's experience, use of a white noise masker and appropriate masking protocols easily masked AHs, much to the patient's surprise. Wearable maskers have been used for many years to treat patients with tinnitus.62 Masking techniques may also hold much promise for helping patients with auditory hallucinations.
TREATMENT: TRANSCRANIAL MAGNETIC STIMULATION
Transcranial magnetic stimulation (TMS) is a non-invasive method of stimulating regions of the brain. A magnetic coil, applied to the scalp, passes a high current alternating electric pulse to underlying brain tissue. This current results in action potentials being discharged, causing an effect that may be excitatory or inhibitory.63
Given that the anatomy of AHs involves temporal areas of the cortex and that hyperactivity of the cortex may propagate AHs, Hoffman et al. predicted that TMS might inhibit cortical activity and reduce AHs.64 In that first study conducted in 1999, they employed slow-rate TMS with three schizophrenic patients with AHs. All three patients noted a decrease in the incidence of the hallucinations. Two of them reported almost complete elimination of AHs for 2 weeks following active TMS treatment.
Since then, several other studies have been conducted that used slow TMS for AHs. Schreiber et al. re-ported a case of AHs that was treated with slow (10-Hz) TMS over the dorsal aspect of the frontal cortex.65 The patient showed improvement as reflected by the Positive and Negative Symptoms Scale, as well as the Brief Psychiatric Rating Scale. In addition, neuroSPECT evaluations performed before, during, and after TMS treatment showed increased general profusion of the brain as well as specific increases in some regions.
Several papers have dealt with the efficacy of TMS in treating AHs. In general, the findings show success rates of approximately 50%.17,66 That is, about half the patients reported significant improvement based on the topography of voices rating scale after 10 days of TMS. Recent research by Lee et al. and McIntosh et al. also indicates improvement of AHs with TMS.67,68
Though the success of TMS to date is not overwhelming, some degree of improvement seems to be noted consistently across studies. This becomes more impressive when one considers that many of the patients in these TMS studies are not responsive to other kinds of interventions for AHs. It is difficult, however, to compare studies and determine precisely how much better some patients actually do.
Even though many of the studies use appropriate designs (e.g., double-blind, crossover, sham approaches), quantification of improvement over long periods of time is difficult to achieve. Variable degrees of involvement, problems in judgment, and contamination from medication and/or other therapies are difficult to control in these kinds of studies. Self-reporting allows insight into patients' complaints, but falls short along a number of psychometric lines. As mentioned earlier for other therapies, the TMS studies often have small numbers, making it difficult to draw conclusions (see Shergill et al.22). Therefore, although TMS seems promising, more work must be done.
It is interesting to speculate on the potential physiological similarities between TMS and acoustic stimulation with white noise (white noise masking). TMS is an electrical current that is believed to cause the firing of neurons in the brain region underlying the place of stimulation.
White noise has also been shown to result in considerable activity in the auditory cortex after being transduced into electrical impulses at the cochlea.69 The activity created by the white noise can be regulated by the intensity of the stimulus and the intensity of the TMS can be regulated by the amount of current. Therefore, it appears there are some similarities in these two forms of cortical stimulation.
There is also a similarity between residual inhibition noted in tinnitus patients and the inhibition of AHs related to TMS. Acoustic stimulation of the ear or ears at the frequency of the tinnitus often causes abatement of the tinnitus for a period of time (seconds to hours) after the stimulation is stopped. This abatement is called residual inhibition. Is this similar to what happens in TMS?
Although certain drugs can trigger AHs, other drugs can be used to treat the condition. Korczyn relates that, theoretically, AHs can be caused by a cholinergic-dopaminergic imbalance in the brain.46 He reported that euroleptic medications that are dopamine and cholinesterase antagonists were effective for treating auditory hallucinations.
Many of the medications used to treat schizophrenia and Parkinsonism are also frequently used for AHs. However, many drug treatments for Parkinson's disease can also cause AHs. Risperidone is one neuroleptic drug that is used for Parkinson-induced AHs. In a study of 39 patients with hallucinations, treatment with Risperidone resulted in complete or nearly complete resolution of hallucinations in 23 patients.70 Donepezil, a cholin-esterase inhibitor, was used in eight patients with Parkinsonism and hallucinations. All eight patients reported a decrease in hallucinations after a trial with this drug.71
What future role might audiologists assume in treating patients with auditory hallucinations? First, we believe audiologists can make a significant contribution to the understanding, diagnosis, and habilitation of AHs. Perhaps the most direct contribution may be to non-psychotic patients with AHs. Patients who have had strokes or other damage to the CANS and who experience AHs are a population to which audiological expertise may be especially relevant. Research and clinical developments in this population, however, would also be relevant for cases of AHs with psychiatric origins, since conditions are also likely to involve CANS dysfunction.
The comparison between psychiatric and non-psychiatric cases of AHs introduces our next future directive. There needs to be more research comparing auditory hallucinations that have a neurological cause with those with a psychiatric cause, such as schizophrenia.
Clearly, a condition such as a stroke in the auditory regions of the brain can produce hallucinations due to neuronal damage. We contend that in psychiatric disease there is also direct damage to auditory neurons—-though it is less obvious. Individuals with schizophrenia have been shown to have abnormal evoked potentials and MRIs secondary to neural degeneration.22,23 As Hoffman et al. relate, AHs can be a result of reduced neural connectivity (which is often related to neural damage).17
Is it that people with AHs have abnormal function of auditory neural substrate that, in turn, results in their being unable to discern internally from externally generated sounds? Or is it the mechanism responsible for identifying and discriminating external from internal perception that is the main contributor to the problem? Or are both pathological mechanisms required? We think to address this question requires audiological (as well as psychiatric) input. Central to this query are the following topics that need to be studied to determine the similarities and differences between these two populations:
* AHs in patients with psychiatric disorder
* AHs in patient without a psychiatric disorder
* Imagination of sound
* Auditory auras before/during seizures
These conditions should be studied with functional imaging, as well as with sophisticated audiological approaches using both psychophysical and electrophysiologic techniques.
Another area of future research is the use of masking and masking techniques. We think that the use of masking paradigms to determine if the AHs can be obliterated by masking could yield useful information. Additionally, it would be helpful to quantify effective levels of masking when treating AHs. As mentioned earlier, wearable tinnitus maskers have proven helpful to tinnitus sufferers. Research should be directed toward the possible use of maskers for patients suffering from AHs. Even if this technique is helpful to only a portion of the clinical population with the condition, it may still be a valuable contribution.
The purpose of this article was to review information on auditory hallucinations from an audiological perspective in an attempt to stir interest across disciplines. Bentall defines hallucinations as perceptions that lack an external stimulus, have the full impact of an actual perception, and are not under voluntary control.1 Auditory hallucinations have been commonly associated with psychiatric conditions, but this is not always the case. They can be linked to a variety of otological, neurological, and pharmacological disorders.
People with AHs perceive a wide range of sounds. Their sound perceptions can be divided into formed and unformed AHs. Formed AHs are more complex, internal acoustic perceptions, such as music and speech. Types of unformed AHs include tones, clicks, chords, etc., which vary in pitch and loudness. In many instances, it is difficult to differentiate unformed AHs from tinnitus.
It is difficult to reach definite conclusions regarding the basis of AHs. Theories include reduced neural connectivity (loss of neural connections within the brain), a pathophysiological generator in the auditory cortex (similar to an eleptiform focus), sensory deprivation, and a misperception of what are internally (imagination) and externally generated sounds. All of these theories could ultimately be related to a pathophysiologic condition. A heightened emotional state may also contribute to the experience of AHs.
It is reasonable to consider sophisticated audiological evaluations as a key element in helping define AHs because of the auditory nature of the hallucinations. Although audiological results are scattered, there do seem to be some indications that dichotic listening performance and auditory evoked potentials may be useful in learning about AHs.
Perhaps one of the biggest breakthroughs in learning about AHs has been functional imaging studies (e.g., MRI, PET). Clearly, certain auditory areas of the brain become activated when AHs begin or even shortly before they begin. Functional imaging studies have provided an anatomical basis for AHs and support the role of the central auditory system in AHs.
Perhaps the most popular treatment for AHs is transcranial magnetic stimulation (TMS). Data are emerging that indicate this technique may develop into a dependable procedure. Counseling techniques, distraction approaches, and acoustic masking procedures have all shown some usefulness as a treatment for AHs. Although certain drugs (especially in high doses) can cause auditory hallucinations, medications can also help in their treatment. Ultimately, the most successful technique for treating AHs will probably be to remove the underlying cause—if it can be discovered.
1. Bentall RP: The illusion of reality: A review and integration of psychological research on hallucinations. Psychol Bull
2. Evers S, Ellger T: The clinical spectrum of musical hallucinations. J Neurol Sci
3. Johns LC, Hemsley D, Kuipers E: A comparison of auditory hallucinations in a psychiatric and non-psychiatric group. Brit J Clin Psychol
4. Copolov D, Trauer T, Mackinnon A: On the non-significance of internal versus external auditory hallucinations. Schizophrenia Res
5. Oulis P, Mamounas J, Hatzimanolis J, Christodoulou GN: A clinical study of auditory hallucinations. Psychiatriki
6. Remschmidt H: Early onset schizophrenia as a progressive deteriorating developmental disorder. J Neural Transmission
7. Tien Y: Distributions of hallucinations in the population. Social Psychiatry Psychiatric Epidemiol
8. Cole MG, Dowson L, Dendukuri N, Belzile E: The prevalence and phenomenology of auditory hallucinations among elderly subjects attending an audiology clinic. Int J Geriatric Psychiatry
9. Ross E, Jossman PB, Bell B, et al.: Musical hallucinations in deafness. JAMA
10. Hammeke T, McQuillen M, Cohen B: Musical hallucinations associated with acquired deafness. J Neurol Neurosurg Psychiatry
11. Harada S, Okazaki Y: A new cognitive therapy for auditory hallucinations and delusions: Development of a guide for psychotic patients and their family members. In Mizuno M, Falloon IRH, Kashima H, Asai M, eds., Comprehensive Treatment of Schizophrenia
. Berlin: Springer Verlag, 2002: 367–372.
12. Hunter MD, Woodruff PWR: Characteristics of functional auditory hallucinations. AJ Psychiatry
13. Boyle M: Schizophrenia: A Scientific Delusion?
(2nd ed.). London: Routledge, 2002.
14. Stephane M, Thuras P, Nasrallah H, Georgopoulos AP: The internal structure of the phenomenology of auditory verbal hallucinations. Schizophrenia Res
15. Penfield W, Perot P: The brain's record of auditory and visual experience. Brain
16. Penfield W: The Excitable Cortex in Conscious Man
. Springfield, IL: Charles C. Thomas, 1958.
17. Hoffman RE, Hawkins KA, Gueorgieva R, et al.: Transcranial magnetic stimulation of left temporoparietal cortex and medication-resistant auditory hallucinations. Arch Gen Psychiatry
18. David AS: The neuropsychological origin of auditory hallucinations. In David AS, Cutting JC, eds., The Neuropsychology of Schizophrenia
. Hove, UK: Lawrence Erlbaum, 1994.
19. Evarts EV: A neurophysiologic theory of hallucinations. West, LJ, ed., Hallucinations
. New York: Grune & Stratton, 1962: 1–15.
20. McKay SE, Golden CJ, Scott M: Neuropsychological correlates of auditory and visual hallucinations. Int J Neurosci
21. Braun C: Brain modules of hallucination: An analysis of multiple patients with brain lesions. J Psychiatry Neurosci
22. Shergill SS, Murray RM, McGuire PK: Auditory hallucinations: A review of psychological treatments. Schizophrenia Res
23. Shergill SS, Brammer M, Amaro E, et al.: Temporal course of auditory hallucinations. Brit J Psychiatry
24. Berrios GE: Musical hallucinations: A historical and clinical study. Brit J Psychiatry
25. Marneros A, Beyenburg St., Berghaus A: Unilateral hallucinations and other psychotic symptoms due to otosclerosis. Psychopathol
26. Schwaber M, Garraghty P, Kaas J: Neuroplasticity of the adult primate auditory cortex following cochlear hearing loss. Am J Otol
27. Calhoun J, Calhoun D: Prolonged bleeding time in a patient treated with sertraline. Am J Psychiatry
28. Marrazzi AS: Pharmocodynamics of hallucinations. West LJ, ed., Hallucinations
. New York: Grune & Stratton, 1962: 36–50.
29. Malitz S, Wilkens B, Esecover H: A comparison of drug-induced hallucinations with those seen in spontaneously occurring psychoses. West LJ, ed., Hallucinations
. New York: Grune & Stratton, 1962: 50–63.
30. Shurley J: Hallucinations in sensory deprivation and sleep deprivation, West LJ, ed., Hallucinations
. New York: Grune & Stratton, 1962: 87–91.
31. Loberg E, Jorgenson H, Hugdahl K: Dichotic listening in schizophrenic patients: Effect of previous vs. ongoing auditory hallucinations. Psychiatry Res
32. Conn R, Posey T: Dichotic listening in college students who report auditory hallucinations. J Abnorm Psychol
33. Hoffman RE, Rapaport M, Mazure C, Quinlan D: Selective speech perception alterations in schizophrenic patients reporting hallucinated “voices.” Am J Psychiatry
34. Lindstrom L, Klockhoff I, Svedberg A, Bergstrom K: Abnormal auditory brainstem responses in hallucinating schizophrenic patients. Brit J Psychiatry
35. Nam E: Is it necessary to differentiate tinnitus from auditory hallucination in schizophrenic patients? J Laryngol Otol
36. Cambier J, Decroix JP, Mason CP: Hallucinose auditive dans les lesions du tronc cerebral. Rev Neurol
37. Scheibel ME, Scheibel AB: Hallucinations and brainstem reticular core. West LJ, ed., Hallucinations
. New York: Grune & Stratton, 1962: 15–36.
38. Tiihonen J, Hari R, Naukkarinen H, et al.: Modified activity of the human auditory cortex during auditory hallucinations. Am J Psychiatry
39. Ford, J, Mathalon D, Kalba S, et al.: Cortical responsiveness during talking and listening in schizophrenia: An event related brain potential. Biological Psychiatry
40. Hubl D, Koenig T, Strik W, et al.: Pathways that make voices: White matter changes in auditory hallucinations. Arch Gen Psychiatry
41. Zatorre RJ, Halpern AR, Perry DW, et al.: Hearing in the mind's ear: A PET investigation of musical imagery and perception. J Cogn Neurosci
42. Garralda ME: Hallucinations in psychiatrically disordered children: Preliminary communication. J Royal Soc Med
43. Edelsohn GA, Rabinovich H, Portnoy R: Hallucinations in Parkinson's disease: A follow-up study. Movement Disorders
44. Remschmidt H: Early-onset schizophrenia as a progressive-deteriorating developmental disorder: evidence from child psychiatry. J Neur Transmis
45. Thomsen PH: Schizophrenia with childhood and adolescent onset: A nationwide register-based study. Acta Psychiatr Scand
46. Korczyn A: Hallucinations in Parkinson's disease. Lancet
47. Moore TA: Musical hallucinations induced by Oxycodone. Am J Geriatric Psychiatry
48. Kuykendall J, Rhodes R: Auditory hallucinations elicited by combined meclizine and metaxalone use at bedtime. Ann Pharmacotherapy
49. Agrawal AK, Sherman LK: Voriconazole-induced musical hallucinations. Infection
50. Stricker RB, Winger EE: Musical hallucinations in patients with Lyme disease. Southern Med J
51. Rubin D, McAbee GN, Feldman-Winter LB: Auditory hallucinations associated with migraine. Headache
52. Roberts DL, Tatini U, Zimmerman RS, et al.: Musical hallucinations associated with seizures originating from an intracranial aneurysm. Mayo Clinic Proc
53. Slade PD, Benton RP: Sensory Deception: A Scientific Analysis of Hallucinations
. London: Croom Helm, 1988.
54. Wilkinson P, Schuller S: Late-onset auditory hallucinations treated with cognitive behaviour therapy. Int J Geriatric Psychiatry
55. Persaud R, Marks I: A pilot study of exposure control of chronic auditory hallucinations in schizophrenia. Brit J Psychiatry
56. Drury V, Birchwood M, Cochrane R, MacMillan F: Cognitive therapy and recovery from acute psychosis, a controlled trial, I: Impact on psychotic symptoms. Brit J Psychiatry
57. Hoffman RE, Satel SL: Language therapy for patients with persistent voices. Brit J Psychiatry
58. Buccheri R, Trygstad L, Kanas N, et al.: Auditory hallucinations in schizophrenia: Group experience in examining symptom management and behavioral strategies. J Psychosoc Nursing Mental Health Serv
59. Nelson HE, Thrasher S, Barnes TR: Practical ways of alleviating auditory hallucinations. Brit Med J
60. Collins MN, Cull CA, Sireling L: Pilot study of treatment of persistent auditory hallucinations by modified auditory input. Brit Med J
61. James DA: The experimental treatment of two cases of auditory hallucinations. Brit J Psychiatry
62. Schleuning A, Johnson R, Vernon J: Evaluation of a tinnitus masking program: A follow up study of 598 patients. Ear Hear
63. Haraldsson HM, Ferrarelli F, Kalin NH, Tononi G: Transcranial magnetic stimulation in the investigation and treatment of schizophrenia: A review. Schizophrenia Res
64. Hoffman RE, Boutros NN, Berman RM, et al.: Transcranial magnetic stimulation of left temporoparietal cortex in three patients reporting hallucinated “voices.” Biol Psychiatry
65. Schreiber S, Dannon PN, Goshen E, et al.: Right prefrontal rTMS treatment for refractory auditory command hallucinations—a neuroSPECT assisted case study. Psychiatry Res
66. Poulet E, Brunelin J, Bediou B, et al.: Slow transcranial magnetic stimulation can rapidly reduce resistant auditory hallucinations in schizophrenia. Biol Psychiatry
67. Lee SH, Kim W, Chung YC, et al.: A double blind study showing that two weeks of daily repetitive TMS over the left or right temporoparietal cortex reduces symptoms in patients with schizophrenia who are having treatment-refractory auditory hallucinations. Neurosci Let
68. McIntosh AM, Semple D, Tasker K, et al.: Transcranial magnetic stimulation for auditory hallucinations in schizophrenia. Psychiatry Res
69. Rauschecker J, Tian B, Hauser M: Processing of complex sounds in the Macaque nonprimary auditory cortex. Science
70. Leopold NA: Risperidone treatment of drug-related psychosis in patients with Parkinsonism. Movement Disorders
71. Fabbrini GBP, Aurilia C, Pauletti C, et al.: Donepezil in the treatment of hallucinations and delusions in Parkinson's disease. Neurolog Sci
© 2007 Lippincott Williams & Wilkins, Inc.