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Psychiatry 73(1) Spring 2010

Hallucinations El-Mallakh and Walker

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Hallucinations, Psuedohallucinations, and Parahallucinations


Rif S. El-Mallakh and Kristin L. Walker

Background: There are several clinical phenomena that resemble hallucinations which are inadequately studied because the terminology defining them is inadequate. Methods: A review of the relevant literature, identified by searches of Ovid and PubMed databases. Results: A historical review reveals that the term pseudohallucination has been used to describe several separate and unrelated phenomena. Herein this term is redefined, and an additional term, parahallucinations, is introduced. Hallucinations are defined as sensory perceptions that have the compelling sense of reality of true perceptions but that occur without external stimulation of the relevant sensory organ and are experienced as following the sensory path, that is, can be localized in three-dimensional space outside the body. Pseudohallucinations are defined as hallucinatory phenomena that do not follow the sensory path and are experienced predominantly by psychiatrically ill subjects. Parahallucinations are defined as hallucinatory phenomena that occur due to an injury or abnormality to the peripheral nervous system. Insight into the reality of these experiences--the realization that they are not real--is not felt to be important in their phenomenology. Conclusion: Utilization of this classification system during clinical investigations will yield greater insight into the pathophysiology, course, treatment, and prognosis of psychiatric and neurologic disorders. Hallucinations are a fascinating clinical phenomenon and a frequent topic of discussion and research in psychiatric literature. Hallucinations are defined by the Diagnostic and Statistics Manual, fourth edition (DSM-IV) as a sensory perception that has the compelling sense of reality of a true perception but that occurs without external stimulation of the relevant sensory organ (American Psychiatric Association, 2000, p. 823). These distorted perceptual events can occur in any of the senses, producing auditory, visual, gustatory, olfactory, and somatic hallucinations. Hallucinations should not be confused with illusions, which are misperceptions or misinterpretations of real external stimuli or flashbacks, which can be defined as the recurrence of a memory, feeling, or perceptual experience from the past (p. 823) (Figure 1). True hallucinations must follow a sensory path, and typically occur as part of a brain dysfunction, including dementia, delirium, toxicity, and psychotic disorders such as schizophrenia and major mood disorders. However, there are other phenomena that can resemble or present in a

Rif S. El-Mallakh, MD, is with the Department of Psychiatry and Behavioral Sciences at the University of Louisville School of Medicine in Louisville, Kentucky. Kristin L. Walker is with the Department of Psychological and Brain Sciences at the University of Louisville. Address correspondence to Rif S. El-Mallakh, Department of Psychiatry and Behavioral Sciences, University of Louisville School of Medicine, MedCenter One, 501 East Broadway, Suite 340, Louisville, Kentucky, 40202; e-mail: rselma01@louisville.edu.

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similar fashion as traditional hallucinations whose clinical utility is of particular interest. The term pseudohallucination was introduced by Hagen in 1868 and was further discussed by both Kandinsky in 1885 and Bleuler in 1911 (cited in Bleuler, 1911) as a means of describing a different type of hallucination that did not follow a sensory path, yet was still a distortion of a persons perception. Blueler (1911) used the term pseudohallucinations to differentiate between auditory hallucinations that were perceived as coming from outside the body and inner voices which originated inside the head. This term has since been applied to multiple phenomena by both clinicians and researchers in the fields of psychiatry and more recently neurology. Pseudohallucinations have been defined and described in varying ways in the literature, and the inconsistency has caused a great deal of confusion for professionals. The terminology as it is currently being used is inadequate to describe the phenomenology of several different types of hallucinatory phenomena. The purpose of this article is to review the literature on pseudo-hallucinations, discuss the challenges both psychiatrists and neurologists face by using insufficient terminology, and propose a new model to remedy those challenges.
Methods

Relevant literature was identified by utilizing the search words pseudohallucinations, and pseudo-hallucinations. Older literature was identified through cited references in electronically indexed articles.
Results

Historical Context Bleuler (1911) stated that patients with schizophrenia often experienced inner

voices and those voices were doing battle with their outside voices which were often critical and degrading. He also believed that transitions existed between voices and auditory thoughts, and he concluded that there were two separate groups: voices projected outside the body and inner voices (belonging in the category of pseudo-hallucinations). Jaspers (1963) stated that abnormal perceptions fall into three categories: illusions, hallucinations proper, and pseudohallucinations. He described pseudohallucinations as a class of phenomena that are often confused with hallucinations but looked at closely, these proved to be not really perceptions but a special kind of imagery (p. 65). He went on to say that these phenomena are seen by an inner eye and do not possess the reality of perception. He stated that there are two differences that distinguish hallucinations from pseudohallucinations. First, hallucinations are objective and based in a concrete reality while pseudo-hallucinations are subjective and figurative. Second, hallucinations occur in external space, and pseudohallucinations occur in internal space. The examples Jasper provided of such events are complex and confusing, and he often contradicted himself. For instance, he remarked that at any time a pseudohallucination can become a hallucination, yet he does not give any explanation as to how this event occurs (Jaspers 1963). In his An Outline of Psychiatry for Students and Practitioners, Fish (1964) used the term pseudohallucination in the glossary, but not in the main text, and defines it as hallucinations which lack the lively character of perceptions and can be distinguished from real perceptions (p. 247). Fish (1962) had previously stated in his book on schizophrenia that pseudohallucinations had no prognostic or diagnostic value in schizophrenia and remained a subject only of academic interest. Fish (1962) concluded that a key characteristic of a pseudohallucination is the presence of insight, and individuals who realized their hallucinations are not real were not experiencing true hallucinations,

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HALLUCINATORY PHENOMENA

PSYCHOTIC HALLUCINATIONS: TRUE HALLUCINATIONS

NON-PSYCHOTIC HALLUCINATIONS

ILLUSIONS

FLASHBACKS

PSEUDOHALLUCINATIONS

PARAHALLUCINATIONS

Figure 1. Classification of hallucinatory experiences (see Table 1 for definitions).

but rather pseudohallucinations. However, he went on to state that a patient can gain or lose insight, thus immediately reducing the value of this definition. Freedman and Caplan (1967) described similar phenomena but did not use the term pseudohallucinations. They stated that some hallucinations are experienced in the external world, while others are experienced within the body. In contrast with Fish, they argued that insight is not a fundamental characteristic of hallucinations, although the amount of insight present in a particular patient may have diagnostic and prognostic significance (p. 567). Hare (1973) reviewed the English language literature from 1957 to 1967. He concluded his review by emphasizing the lack of information on pseudohallucinations as well as the ambiguity and confusion surrounding this term in the literature. He initially suggested abandoning the term since authorities either differ or take no notice and since they adduce nothing to suggest clinical relevance, but he went on to say that a better idea is to systematically reappraise the term (p. 472). Hare (1973) stated that sensory experiences are either subjective or objective. He defined a subjective sensory experience as one in which there is an abnormal stimula-

tion of the sensory nerve endings. He went on to suggest that these experiences may occur from an organic disturbance in the nervous system or from a psychiatric disorder. Such subjective experiences have either a morbid or normal origin. Hare classified these experiences into four distinct groups. The first group, normal subjective experience with normal origin, includes such situations as when a person who has recently lost a loved one hears that relative call his or her name but then quickly realizes this did not actually occur. The second group, normal subjective experience with morbid origin, Hare believed, is not easily demonstrated and would likely be indicative of a psychiatric disorder. The third group, a subjective experience with a morbid origin but normal interpretation, would include such examples as the epileptic aura, tinnitus, and sensory experiences induced by drugs (such as LSD, mescaline, etc.). The final group, subjective sensory experiences with a morbid interpretation and morbid origin, would occur during a psychiatric disorder such as schizophrenia (Hare, 1973). Hare provided an example of a patient who hears voices and believes they are coming from other people, even when the patient states that those voices are coming from inside his or her own head.

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These experiences are not subject either to self-correction or to correction by friends or medical attendants (p. 474). The descriptions of these groups led Hare to his central question: Where do pseudohallucinations fit? He made a case that pseudohallucinations are best described as subjective sensory experiences that result from a psychiatric disorder and are interpreted in a normal way by the patient (Hare, 1973), thus fitting most neatly into the first group he described. Taylor (1981) stated that the term pseudohallucinations has received two incompatible definitions (p. 265). The term can refer to hallucinations that are recognized as such by the individual who experiences them. This definition is similar to Hares interpretation. The term can also refer to introspected images that possess vividness and spontaneity. Taylor (1981) argued that the term might be better sub-divided and described as perceived and imaged pseudohallucinations. He states that the German tradition supports the idea of pseudohallucinations as images and inner phenomena, and the English tradition supports the idea of perceived phenomena which appear to have objective characteristics (p. 270). Therefore, the definition of pseudohallucinations can vary depending on the tradition to which a person ascribes. Taylor believed the term is best differentiated by using imaged and perceived pseudohallucinations, although he clearly stated that authors need to pick one definition and maintain continuity in order to avoid confusion (Taylor, 1981). Sedman (1966b) has documented the commonality of non-psychotic hallucinations. He studied 72 patients (59 females, 13 males at the Manchester Royal Infirmary) with some hallucinatory phenomena (Sedman 1966a). He defined imagery as an experience appearing in inner subjective space and lacking concrete reality of perception (Sedman, 1966a, p. 10). (defined as pseudohallucinations in this paper). Pseudohallucinations were defined as hallucinations that were perceived through the senses but were recognized by the patient as not being

real perception (Sedman, 1966b), and that they are a special form of imagery that is subjective, occurs in internal space, and is often incomplete (Sedman, 1966b). True hallucinations were defined as experiences which followed a sensory path and were perceived by the subject as a real perceptions (Sedman, 1966b). Nearly one-fifth of the sample (15 patients, 21%) reported experiencing imagery, 25 (34.7%) patients reported experiencing pseudohallucinations, and 24 (33.3%) patients reported true hallucinations (Sedman, 1966b). Sedman (1967) also reported a significant relationship between premorbid personality and the likelihood of experiencing pseudohallucinations. He found that the patients who had an attention-seeking or insecure personality type were more likely to have experienced pseudohallucinations (2 = 4.6; p < 0.05) (Sedman, 1967). The other premorbid personality types did not have a relationship with the occurrence of pseudohallucinations (Sedman, 1967). Brasic (1998) wrote a detailed article on hallucinations, providing both definitions and descriptions of various phenomena and focusing his efforts on differential diagnosis. He stated that hallucinations are sensory perceptions without environmental stimuli (p. 851). He also wrote that the nature of the hallucination is critical for localization, differential diagnosis, and treatment planning (p. 851). In his article Brasic described that hallucinations in Parkinsons patients can be indicative of dementia and rapid deterioration (Brasic, 1998). Hallucinations occurring in individuals with Alzheimers disease are often predictive of behavioral problems and rapid cognitive decline. He also provided theories on the etiology of hallucinations, including stimulation and inhibition. Inhibition is the damage of normal inhibitory functions which can result in disinhibition, similar to what is seen in phantom limb and Charles Bonnet syndromes. Those individuals who experience hallucinations due to neurologic syndromes often realize their hallucinations are not real (Brasic, 1998).

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Critchley and Rossall (1978) also described hallucinations that occur in non-psychiatric states, such as sensory deprivation, reticulo-hypothalamic-cortical dissociation, focal hallucinations, and peripheral endorgan dysfunction. The authors stated that hallucinations with peripheral end-organ dysfunction are activated by factors such as the absence of normal stimuli for the periphery, distortion of information as a result of spontaneous irritability of the end organ, alterations in the state of alertness, and coexistent disturbances of cerebral function (pp. 264-265). Many neurological reports have subsequently appeared in which hallucinatory phenomena associated with peripheral nerve injury are described as pseudohallucinations [e.g., Kasten and Poggel, 2006]. Spitzer (1987) reviewed pseudohallucinations and concluded that its various uses have left the term ambiguous and with reduced utility. He proposed dropping the term. Van der Zwaard and Polak (2001) arrived at a similar conclusion after their review of the literature. They propose the term nonpsychotic hallucinations as an alternative. Thus, it appears that many generations of clinicians and researchers have recognized that there are variations in the hallucinatory experience that are important to note. However, while a multitude of variables were identified--experiences not following the sensory path, insight into the unreality of the hallucinatory experience, hallucinations related to neurologic injury, hallucinations in the setting of an otherwise clear sensorium, or a special kind of imagery--one term has been used to describe them all: pseudohallucinations.
Discussion

ing phenomena may be lost if terms defining them are not standardized. For example, patients with borderline personality disorder and dissociative identity disorder will frequently experience internal voices (that do not follow the sensory path) that typically begin early in life and whose content is related to the history of trauma (Kluft, 1987; van der Zwaard and Polak, 2001). Similarly, the presence of pseudohallucinations is more common in subjects with attention-seeking or insecure personality types (Sedman, 1967). Van der Zwaar and Polak point out that these perceptual disturbances are problematic since in our opinion, psychosis would be too strong a label, while imagery would not capture its severity (van der Zwaar and Polak, 2001, p. 47). While they propose the term transient hallucinations, they acknowledge that they are never absent for a prolonged time (p. 46). Proposed Terminology The problems with imprecise and inconsistent terminology are abundantly clear. Psychiatrists, psychologists, neurologists, and other clinicians use the terms hallucinations and pseudohallucinations (Brasic, 1998; Sedman, 1967), but, it is often the case that the same concept or problem is not being discussed. For instance, psychiatrists may refer to voices inside the head or the realization that hallucinations are pathologic phenomena as pseudohallucinations, while neurologists frequently refer to hallucinatory phenomena due to peripheral nerve injury, such as phantom limb syndrome, as pseudohallucinations (Blueler, 1911; Brasic, 1998). The goal of this article is to create a new set of definitions which will allow clinicians to discuss these phenomena in a consistent and coherent manner. We propose that hallucinations (true hallucinations) must follow a sensory path and, more specifically, occur in the context of the central nervous system (Table 1). In other words, these experiences do not dif-

The Importance of Good Working Definitions It is clear that there are several hallucinatory phenomena. Insights that may be gleaned from investigations into these differ-

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TABLE 1. Terms and Their Definitions.


Illusion Flashback Hallucination A misperception or misinterpretation of a real external stimulus A recurrence of a memory, feeling, or perceptual experience from the past that may have the compelling sense of reality A sensory perception that has the compelling sense of reality of a true perception but that occurs without external stimulation of the relevant sensory organ and is experienced as following the sensory path. The person may or may not have insight into the fact that he or she is having a hallucination. A hallucinatory phenomenon that does not follow a sensory path and is only experienced predominantly in psychiatric illness A hallucinatory phenomenon that occurs due to an injury or abnormality to the peripheral nervous system

Pseudohallucination* Parahallucination*

*These definitions are proposed by the articles authors.

fer in quality from true sensory experiences and can be localized by the subject in threedimensional space. Voices or noises can be localized as coming from outside the body (as close as the ears); visions can be pointed to as outside the eyes; and somatic experiences can be localized directly in the affected body part. The experience is perceived as if it has traveled through the peripheral receptors (ears, eyes, skin, etc.), into the brain (i.e., following the sensory path). In these subjects the peripheral nervous system is intact and functioning normally, so the abnormal experience has its origins in the central nervous system. Patients may or may not have insight into the pathologic nature of the experience. Parahallucinations refer to hallucinations that follow a sensory path (see definition above), but they occur in the context of the peripheral nervous system dysfunction, as can seen in phantom limb, Charles Bonnet syndrome, optic or acoustic nerve injuries, and many other neuropathies (which may include paraesthesias) (Table 1). This sensation is indistinguishable from a true sensory experience and would be indistinguishable from a true hallucination (e.g., El-Mallakh, Junaja, and Casey, 1998) but is localized to the affected dysfunctional peripheral sensory organ or nerve, or to central nervous system pathways related to the injured nerve fibers (Hunter, Katz, and Davis, 2008). Insight into the pathologic nature of these sensory experiences may or may not be present, but the lack of insight is not related to the pathologic

process that created the abnormal sensory experience. Treatment response may also be different, with anti-epileptics being more effective than antipsychotics (El-Mallakh et al., 1998). This new term, parahallucinations, is proposed because these individuals are indeed experiencing an unreal experience that follows the sensory path, but this experience is occurring due to a pathologic process that is outside the central nervous system. The term pseudohallucination is proposed to refer to hallucinatory phenomena that do not follow a sensory path (Table 1). In other words, the experience cannot be localized in three-dimensional space, and it is most frequently described as originating inside the head. This experience most closely resembles vivid memories, but unlike memories it is not initiated willingly by the patient, and unlike flashbacks does not actually reflect a true (or false) memory. Similar to true hallucinations, this experience originates in the central nervous system (i.e., in the absence of peripheral injury), and while experienced as very real, unlike hallucinations is not experienced as indistinguishable from actual sensory experiences. This use of the term follows the use proposed by Bleuler (1911), referring to inner voices, and the actual definition of the prefix pseudo. Also inherent in our definition of pseudohallucinations is the idea that these can only occur in psychiatric disorders and do not have to be self-recognized as not being real. We specifically omitted insight into the reality of the

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HALLUCINATORY EXPERIENCE

THE EXPERIENCE OCCURS IN THE SETTING OF AN ENVIRONMENTAL STIMULUS WHICH IS MISINTERPRETED

YES

ILLUSION

NO THE CONTENT OF THE EXPERIENCE HAS OCCURRED PREVIOUSLY OR STRONGLY RESEMBLES A PREVIOUS OCCURRENCE YES

FLASHBACK OR RE-EXPERIENCE

NO THE EXPERIENCE FOLLOWS AN INTACT SENSORY PATH YES TRUE HALLUCINATION

NO PATIENT HAS NERVE INJURY ASSOCIATED WITH HALLUCINATORY EXPERIENCE YES PARAHALLUCINATION

NO EXPERIENCE DOES NOT FOLLOW SENSORY PATH AND IS NOT ASSOCIATED WITH NERVE INJURY YES

PSEUDOHALLUCINATION

Figure 2. Flow chart of determination of hallucinatory phenomena.

hallucinatory phenomena as a distinguishing factor in any of the definitions because this varies as a consequence of therapeutic intervention. Often, people with schizophrenia, borderline personality disorder, and other psychiatric disorders hear voices that do not come through their ears, that is, from inside their heads, and they believe that these voices are indeed very real and separate from themselves. However, by the proposed definitions, these phenomena do not follow a sensory path and, therefore, are not true hallucinations.

Figure 2 provides a flow chart for classifying the hallucinatory phenomena. Each step in the figure allows for the definitive classification of the hallucinatory phenomenon. Use of this flow chart reduces the likelihood of confusion or error. Potential Utility for New Definitions These definitions provide clinical utility for describing and discussing varying types of hallucinatory phenomena, and they also open the doors for researchers to begin find-

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ing the best treatment approaches for each of these types of hallucinations. For example, in an exploratory study of patients presenting to an emergency psychiatric service, the presence of pseudohallucinations was associated with significantly greater severity of suicidal ideation than for patients experiencing true hallucinations (Penagaluri, Walker, and ElMallakh, 2009). Additionally, this nomenclature may begin to explain the discrepancy between observations that hallucinations are associated with higher risk for suicide and suicidal behavior (Nordentoft et al., 2002; Papolos et al., 2005; Walsh et al., 1999), and a meta-analysis of 29 separate studies that finds that the presence of hallucinations actually decreased the risk for suicide by half (Hawton et al., 2006). Specifically, given the finding that severity of suicidal ideation is

more closely associated with pseudohallucinations (Penagaluri et al., 2009), it is likely that the observed greater risk of suicide and suicidal behavior (Nordentoft et al., 2002; Papolos, Hennen, Cockerham, 2005; Walsh et al., 1999) reflects pseudohallucinations rather than true hallucinations. Future work may be more revealing. Is there a psychopharmacologic treatment for pseudohallucinations? Is there a difference between command hallucinations and pseudohallucinations in terms of suicide or violence risk? Are there different cormobidities for subjects experiencing hallucinations or pseudohallucinations? Are there different biological markers for the two phenomena? These questions can begin to be answered with the use of clear and consistent terminology.

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Nordentoft, M., Jeppesen, P., Abel, M., Kassow, P., Peterson L., Thorup, A., Krarup, G., Hemmingsen, R., and Jorgensen, P. (2002). Opus Study: Suicidal behavior, suicidal ideation and hopelessness among patients with first-episode psychosis. One-year follow-up of a randomized controlled trial. British Journal of Psychiatry, 43(Suppl), s98-s106. Papolos, D., Hennen, J., and Cockerham, M.S. (2005). Factors associated with parent-reported suicide threats by children and adolescents with community-diagnosed bipolar disorder. Journal of Affective Disorders, 86, 267-275. Penagaluri, P., Walker, K.L., and El-Mallakh R.S. (2009). Hallucinations, pseudohallucinations, and severity of suicidal ideation among emergency psychiatry patients: A pilot study. Journal of Crisis Intervention and Suicide Prevention. Sedman, G. (1966a). A comparative study of pseudohallucinations, imagery, and true hallucinations. British Journal of Psychiatry, 112, 9-17.

Sedman, G. (1966b). Inner voices. Phenomenological and clinical aspects. British Journal of Psychiatry, 112, 485-490. Sedman, G. (1967). Experimental and phenomenological approaches to the problem of hallucinations in organic psychosyndromes. British Journal of Psychiatry, 113, 1115-1121. Spitzer, M. (1987), Pseudohallucinations. Fortschritte der Neurologie-Psychiatrie (Stuttgart), 55, 91-97. Taylor, F.K. (1981). On pseudo-hallucinations. Psychological Medicine, 11, 265-271. Van der Zwaard, R., and Polak, M.A. (2001). Pseudohallucinations: a pseudoconcept? A review of the validity of the concept, related to associate symptomatology. Comprehensive Psychiatry, 42, 42-50. Walsh, E., Harvey, K., White, I., Manley, C., Fraser, J., Stanbridge, S., and Murray, R.M. (1999). Prevalence and predictors of parasuicide in chronic psychosis, UK700 Group. Acta Psychiatrica Scandinavica, 100, 375-382.