Flavie Waters, MSc, MPsych, PhD

Throughout history, auditory hallucinations (“voices”) have been construed as evidence of communication with divine powers, although 20th century medical models have often viewed these experiences as “undesirable” and a sign of mental illness. Until recently, auditory hallucinations carried considerable weight in the diagnostic process as pointing to schizophrenia spectrum disorders. It is increasingly clear, however, that auditory hallucinations occur in a range of psychiatric and medical disorders as well as in individuals without mental illness.

Despite these recent advances, there are important gaps in our understanding of hallucinations outside of psychotic disorders. This article focuses specifically on adult populations. (For a discussion of hallucinations in children and adolescents see the article by Jardri and colleagues.

Auditory hallucinations refer to auditory percepts that a person experiences when awake that are not elicited by an external stimuli. They may be experienced as coming from anywhere in external space, “in the mind,” or on the surface of the body. The contents vary widely and may involve language or other sounds, such as music, footsteps, telephone ringing, buzzing, scratching, whistling, bangs, animal calls, water falling, or engines. Noise volume varies from hardly audible (eg, whispers) to very loud.

Auditory hallucinations have veridical perceptual qualities in the sense that individuals are often convinced of the objective reality of the experience. However, they are much more than auditory perceptions. The message carried by hallucinated voices often contains such personalized and emotionally charged contents that it often resonates with the idea of a “speaking character.”

Given the complex and multifaceted nature of hallucinations, it is helpful to segment their multiple phenomenological dimensions (

 In clinical settings, features such as frequency, emotional response, and functional interference are the most commonly used dimensions when evaluating response to treatment.

Auditory hallucinations occur more commonly in individuals with schizophrenia or schizophrenia spectrum disorders than in those with any other disorder: estimates range between 60% and 75%.

 Patients with schizophrenia who have auditory hallucinations commonly hear several different voices, and these are often recognized as belonging to someone who is familiar (eg, a neighbor, family member, or TV personality) or to entities such as God, the devil, or angels. In 55% of cases, the voices have negative and malicious content: they are derogatory, insulting, or commanding (to do something intolerable).

These negative voices cause considerable distress. However, in 40% of cases, the voices are pleasant and supportive-some individuals report feelings of loss when their treatment makes the voices disappear. The content of voices is usually highly personalized. The voices describe what the person is feeling or thinking, and speak about his or her fears or worries. The personalized content and subjective reality of the voices play a key role in the development of strong beliefs about the intent and power of voices, and an intense relationship may develop between the voice-hearers and their voices.

A significant proportion of persons with schizophrenia also experience nonverbal hallucinations (music and other sounds). Often, there is complete absence of verbal material, although a message or meaning is communicated without being heard (soundless voices). The clarity of hallucinated speech may be low or fuzzy, but the message is always clear.

The intensity and frequency of symptoms fluctuate during the illness, but the factor that determines whether hallucinations are central to the clinical picture is the degree of interference with activities and mental functions. In many cases, auditory hallucinations are intrusive and unwanted, and they cause much functional disruption in personal and vocational functioning. The person with schizophrenia and auditory hallucinations may or may not have insight.

Other key characteristics of auditory hallucinations in psychotic disorders are:

• Higher frequency of hallucinatory experiences

• Co-occurrence of other hallucinations and delusions

• The extent to which patients believe that others share this experience

 first-rank hallucinations (voices keeping up a running commentary on the person’s behavior or thoughts, or two or more voices conversing with each other) were thought to be of diagnostic significance for schizophrenia. While this subtype occurs prominently in schizophrenia, its specificity to schizophrenia has been questioned, and the special treatment of first-rank hallucinations in schizophrenia has since been eliminated from DSM-5.

Auditory hallucinations feature prominently in many psychiatric disorders other than schizophrenia. They occur in persons with bipolar disorder (10% to 25%), major depression (6%), PTSD (40% to 50%), and borderline personality disorder (25% to 50%). Compared with hallucinations in patients with schizophrenia, those in patients with other psychiatric disorders are often less severe. They are less frequent and intrusive and cause less functional interference.

Studies that compared the characteristic features of hallucinations of persons with schizophrenia with those of persons with other psychiatric disorders (on dimensions such as frequency, duration, location, content, form, negative content) report greater similarities than differences. However, the co-occurrence of auditory hallucinations with delusions and hallucinations in other modalities is more common in persons with schizophrenia.

In all psychiatric disorders, the presence of hallucinations is linked to a more severe psychopathological profile and to a less favorable prognosis. Baethge and colleagues

 reported that hospitalization for individuals with a range of psychiatric disorders and hallucinations (all modalities) averaged 17% longer than for those who did not have hallucinations. Individuals with psychotic depression also have a more severe course and an increased risk of relapse and hospitalization, compared with patients with nonpsychotic depression.

Multiple medical and neurological conditions can cause auditory hallucinations. Frequency is approximately 10% in autoimmune disorders involving the CNS (eg, systemic lupus erythematosus), neuroinfections (eg,viral encephalitis), and disorders arising from genetic mutations (eg, velocardiofacial syndrome and Prader-Willi syndrome). Auditory hallucinations may also be precipitated by neurological conditions, focal brain lesions, and cerebral tumors involving subcortical structures or the temporal lobe.

Auditory hallucinations also occur in persons with dementia (symptoms may present several years before the diagnosis), delirium, Parkinson disease, Huntington disease, and multiple sclerosis. The frequency of hallucinations increases with the progression of the disease and is associated with greater distress in the caregiver and higher mortality. Also, auditory hallucinations are very common; they occur in more than 50% of individuals who are abusing or withdrawing from substances such as alcohol, cocaine, and amphetamines.

People who experience auditory hallucinations do not necessarily suffer from a mental illness. Transient and infrequent episodes are common in the general population, without progression to a persistent mental illness. Hallucinatory-like experiences occur in 10% to 40% of persons without a psychiatric illness, as assessed using broad screening questions.

Factors such as intoxication and withdrawal from substances, and other physical states such as physical illness, stress, and grief contribute greatly to these experiences. Consequently, prevalence rates in the general population reduce to approximately 4% when research criteria exclude hallucinations arising in the context of drugs or medical problems.

 Hallucinations can also occur at sleep onset (hypnagogic hallucinations), and on awakening (hypnopompic hallucinations), particularly in persons with sleep disorders, although these phenomena are not well understood.

Healthy individuals can experience hallucinations under no special circumstances. Romme and colleagues

 conducted a survey of persons in the general population with auditory hallucinations. Approximately half of the sample who responded did not receive medical or psychiatric treatment, which suggests that hallucinations can occur in community individuals without the need for treatment.

Descriptive studies have since showed remarkable similarities to hallucinations reported by persons with schizophrenia (in acoustic quality, direction, linguistic details, etc), but with key differences: hallucinations in persons without mental illness are less frequent, less intrusive, of shorter duration, and more positive than in persons with schizophrenia. In addition, nonclinical persons tend to have greater control over their voices and report less interference. The absence of delusions also helps distinguish nonclinical hallucinatory experiences from those of schizophrenia.

Clinical assessment of auditory hallucinations

All assessments should begin with a detailed history. Consider the cultural background of the person with hallucinations because some cultures and communities encourage hearing voices and do not associate this with mental illness. In clinical settings, other neuropsychiatric symptoms (delusions, insight, language disorders) must also be assessed. Short scales with good reliability and validity for assessing general psychopathology include the Brief Psychiatric Rating Scale (BPRS).

 Comorbidities that have been linked to auditory hallucinations, such as drug and alcohol misuse, depression, anxiety, and medical and neurological disorders, must be assessed. Laboratory tests and brain scans can also offer further clues to the cause.

If communication and coherent thinking are not impaired, individuals are usually able to describe their hallucinatory experiences, although challenges include suspiciousness, guardedness, and malingering. A standard probe for auditory hallucinations reads, “Do you ever seem to hear noises or voices when there is nobody about, and no ordinary explanation seems possible?” A description of the experience in the patient’s own words is required for a positive rating.

Many scales (self-report and interviews) have been developed to assess hallucinations. In research settings, the most commonly used scale is the Psychotic Symptom Rating Scales (PSYRATS), and in clinical settings, the Hallucinations Change Scale (HCS).

 (See the upcoming book by Waters and Stephane

 for a comprehensive description and evaluation of 120 ratings scales on hallucinations and other symptoms.)

True auditory hallucinations must be differentiated from:

• Auditory distortions and illusions (misinterpretations of real existing stimuli)

• Vivid auditory imagery (under volitional control)

• Altered consciousness (sleep-related hallucinations, delirium, hypnosis)

• Delusion of reference (when individuals report that other people are talking about them)

Explanatory models of auditory hallucinations

The multifaceted nature of auditory hallucinations makes it very difficult to understand. Frameworks incorporating an interplay between biological and environment factors are best able to explain hallucinations. Of importance is the biographical context in which hallucinations emerged. Negative life events and trauma have been causally linked to the onset of hallucinations, and they are also key influences on the content of voices as well as on negative appraisals and disability. For example, stress has been implicated in provoking episodes of auditory hallucinations, as shown in high rates of hallucinations in bereavement, trauma, and sensory deprivations.

In individuals with a vulnerability for psychosis, a depressed mood significantly increases the risk of transition to a psychotic episode. Hallucinations, in turn, also increase levels of stress. Both the content and the experience of intrusive and personal voices can cause distress, and even suicide. Depression, anxiety, fear, and anger occur in 25% to 40% of persons with auditory hallucinations.

The exact processes underlying auditory hallucinations remain largely unknown. Neuroimaging techniques seek to examine the neural underpinnings of hallucinations with an examination of the brain regions and networks associated with these symptoms. Neuropsychological approaches, by contrast, target cognitive and psychological processes, providing an explanation regarding how unwanted internal events emerge and are accepted as being real and powerful.

One common formulation suggests that the voices represent the involvement of language brain processes, and particularly inner speech processes referring to silent speech that people engage in. Neuroimaging studies show that hallucinations with a verbal content engage brain regions associated with language comprehension and production, such as the primary auditory cortex and Broca area.

 However, persons with hallucinations report nonverbal sounds as well as speech, and language processes are not always activated in imaging studies.

A dominant hypothesis in explanatory models of hallucination is that of a dysfunction in cognitive control.

 In view of the intrusive nature of hallucinations and difficulties with cognitive inhibition, self-monitoring, working memory brain circuitry, set-shifting, and ruminations, an explanation based on cognitive control dysfunctions is able to account for most salient features in both psychiatric and nonpsychiatric populations. That is, a diminution of inhibition and executive control processes in persons with hallucinations produces cortical release of auditory signals and (often emotionally charged) mental events that are unintentional and unwanted. As a result, hallucinations allow perceptions and thoughts to come to the foreground of mental experiences.

Spontaneous activity in the early sensory cortices of the brain at rest may also form the basis for the original signal. In most circumstances, early neuronal computation systems in the brain interpret this low-level power activation as random and nonrelevant, and do not allow it to progress for further processing. In persons with hallucinations, however, there appears to be a lower threshold for accepting these signals as real, so that cortical activity is allowed to be processed like any other real and meaningful events when it is in fact random. This may explain why some individuals report auditory events in the absence of any perceptual input.

A brain system that is excessively “tuned-in” to internal experiences may also be attentively listening to spontaneous sensory activity that is usually ignored by other people.

Hallucinations do not need medical treatment if the experience is not intrusive and if it does not interfere with personal or vocational functioning. When treatment is required, antipsychotic medication is usually the first choice in organic and psychiatric conditions. Because of adverse effects, clinicians should make sure to monitor the physical health of patients regularly. Few studies have compared the efficacy of different neuroleptic treatments, but it is understood that hallucinations often persist despite intensive and prolonged pharmacological treatment.

In recent years, neurostimulation methods have attracted increasing interest. Repetitive transcranial magnetic stimulation (rTMS) over the left temporoparietal areas has been proposed as a useful treatment method. Studies show that when rTMS is used as an adjunct to antipsychotic medication, the frequency and severity of auditory hallucinations can be reduced, although the duration of positive rTMS effects may be less than 1 month.

Newer neurostimulation applications include transcranial direct current stimulation (tDCS), which has the advantage of offering simultaneous inhibitory and excitatory action at different sites, thereby allowing greater coverage of distinct brain systems. Although tDCS shows promise for use in treatment-resistant hallucinations, more studies are needed.

Psychotherapies are widely recommended in practice guidelines, often as a complementary approach to neuroleptics and especially for treatment-resistant hallucinations. Much of this work derives from the seminal work by Romme and Escher,

 who demonstrated that the cognitive restructuring of auditory hallucinations had strong therapeutic effects. This led the way for a new generation of psychotherapies, of which cognitive-behavioral therapy for psychosis (CBTp) is the most common. The focus of CBTp is on assisting the person with hallucinations to reframe beliefs about voice identity, power, and intent of the voices. By changing the person’s relationship with voices, CBTp aims to reduce distress and the power of the hallucinations. Another approach-hallucination-focused integrative treatment-includes CBTp with additional motivation components, rehabilitation, and crisis management.

Finally, cognitive deficits underlying hallucinations have become targets of treatment with cognitive remediation strategies. Recent trials show increasing convergence between theory and practice by focusing on deficits found to be linked to auditory hallucinations. With this approach, patients practice techniques to recognize the source of the voices.

The concept of auditory hallucinations has changed markedly in the past 100 years, from early medical models that viewed hallucinations as a sign of mental illness to the contemporary view that acknowledges their existence in a continuum stretching from the general population to a range of medical and psychiatric conditions. Although there are many gaps in our understanding of hallucinations, the work of the International Consortium on Hallucination Research (hallucinationconsortium.org) is making good progress by stimulating international collaboration and encouraging multisite studies. Given the complexity of hallucinations, only such a concerted effort and large pooled sample sizes have the potential to give rise to truly novel advances in clinical developments. Hallucinations represent a fascinating phenomenon for further study and an important target for clinical interventions for individuals with intrusive and unwanted hallucinations.

Dr Waters is Associate Professor in the School of Psychiatry and Clinical Neurosciences, The University of Western Australia, Perth; Clinical Research Centre, Graylands Hospital, Western Australia. She reports no conflicts of interest concerning the subject matter of this article.

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Articles

This article focuses on auditory hallucinations, which occur in a range of psychiatric and medical disorders as well as in individuals without mental illness.

Author | Flavie Waters, MSc, MPsych, PhD

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Auditory Hallucinations in Adult Populations