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Visual hallucinations of autobiographic memory and asomatognosia: a case of epilepsy due to brain cysticercosis a
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Juan Manuel Orjuela-Rojas , Jesús Ramírez-Bermúdez , Iris E. Martínez-Juárez , Nora d
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Estela Kerik , Iván Diaz Meneses & Fernanda Juárez Pérez-Gay
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Neuropsychiatry Unit, National Institute of Neurology and Neurosurgery, Mexico City, Mexico b
Medical School, National University of Mexico, Mexico City, Mexico
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Epilepsy Clinic, National Institute of Neurology and Neurosurgery, Mexico City, Mexico
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Molecular Imaging PET/CT Unit, National Institute of Neurology and Neurosurgery, Mexico City, Mexico e
Institut des Sciences Cognitives, Université du Québec à Montréal, Montréal, Canada
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Integrated Program in Neuroscience, McGill University, Montréal, Canada Published online: 10 Oct 2014.
To cite this article: Juan Manuel Orjuela-Rojas, Jesús Ramírez-Bermúdez, Iris E. Martínez-Juárez, Nora Estela Kerik, Iván Diaz Meneses & Fernanda Juárez Pérez-Gay (2014): Visual hallucinations of autobiographic memory and asomatognosia: a case of epilepsy due to brain cysticercosis, Neurocase: The Neural Basis of Cognition, DOI: 10.1080/13554794.2014.962548 To link to this article: http://dx.doi.org/10.1080/13554794.2014.962548
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Neurocase, 2014 http://dx.doi.org/10.1080/13554794.2014.962548
Visual hallucinations of autobiographic memory and asomatognosia: a case of epilepsy due to brain cysticercosis Juan Manuel Orjuela-Rojasa*, Jesús Ramírez-Bermúdeza,b, Iris E. Martínez-Juárezc, Nora Estela Kerikd, Iván Diaz Menesesd and Fernanda Juárez Pérez-Gaye,f Neuropsychiatry Unit, National Institute of Neurology and Neurosurgery, Mexico City, Mexico; bMedical School, National University of Mexico, Mexico City, Mexico; cEpilepsy Clinic, National Institute of Neurology and Neurosurgery, Mexico City, Mexico; dMolecular Imaging PET/CT Unit, National Institute of Neurology and Neurosurgery, Mexico City, Mexico; eInstitut des Sciences Cognitives, Université du Québec à Montréal, Montréal, Canada; fIntegrated Program in Neuroscience, McGill University, Montréal, Canada
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(Received 26 February 2014; accepted 3 September 2014) The current study describes the case of a woman with symptomatic epilepsy due to brain cysticercosis acquired during childhood. During her adolescence, she developed seizures characterized by metamorphopsia, hallucinations of autobiographic memory and, finally, asomatognosia. Magnetic brain imaging showed a calcified lesion in the right occipitotemporal cortex, and positron emission tomography imaging confirmed the presence of interictal hypometabolism in two regions: the right parietal cortex and the right lateral and posterior temporal cortex. We discuss the link between these brain areas and the symptoms described under the concepts of epileptogenic lesion, epileptogenic zone, functional deficit zone, and symptomatogenic zone. Keywords: metamorphopsia; asomatognosia; autobiographical hallucinations; epilepsy; neurocysticercosis
In 1938, Wilder Penfield described two main types of “mental phenomena” elicited by the electric stimulation of the cerebral cortex. He called “experiential phenomena” to the occurrence of mental experiences related to the personal background of the subject: autobiographic images or vivid memories in which perception, memory, and emotion are expressed in a unified manner (Elliott, Joyce, & Shorvon, 2009; Gloor, Olivier, Quesney, Andermann, & Horowitz, 1982). He also described other phenomena concerning the interpretation of the current situation of the subject, including illusions and emotional changes. He referred to these types of experiences as “interpretative phenomena.” Here, we present a clinical case of temporo-parietooccipital epilepsy that comprises both types of mental phenomena according to Penfield’s terminology: experiential and interpretative. In this case, they appear under the form of visual autobiographic hallucinations (classically named visual experiential hallucination), metamorphopsia, and asomatognosia. Lüders (Rosenow & Luders, 2001) described the epileptogenic zone as the “area of cortex that is indispensable for the generation of epileptic seizures”; the epileptogenic lesion as the radiographic lesion responsible for the generation of the seizures; the symptomatogenic zone as the one that reproduces the ictal symptomatology and the functional deficit zone as the area of the brain that shows abnormalities during the interictal period, which can be *Corresponding author. Email: [email protected] © 2014 Taylor & Francis
determined through the neurological or/and neuropsychological exams, electroencephalogram (EEG), singlephoton emission computed tomography (CT), positron emission tomography (PET), or other functional tests. Through the patient’s case work-up, magnetic resonance imaging (MRI) studies revealed the epileptogenic lesion, which in turn is related to the epileptogenic zone. The variety in the clinical symptomatology revealed multiple symptomatogenic zones, and the PET scan showed the epileptogenic and the functional deficit zones. Case report We present the case of a married 36-year-old woman with a bachelor’s degree in Psychology. Her clinical problem started when she was 5 years old, when she suddenly presented with fever, headache, leftward gaze deviation, vomiting, and generalized tonic–clonic seizures. At age 9, she reported seeing intermittent, colorful lights that appeared in the inferior and temporal quadrant of her left eye and lasted for a few seconds. During her adolescence, these visual phenomena were accompanied by illusions consisting of metamorphopsias. During these events, she experienced a distortion in the visual perception of the environment for a few seconds: “I see something like a bubble that appears in the left side of my eye, as if it was a kaleidoscope distorting the people, the lines, everything… It’s like putting a drop of water in a glass… Or like a
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Figure 1. Graphic representation of ictal metamorphopsia and visual hallucinations of autobiographic memory. The patient draw a schematic representation of the ictal visual phenomena (left side of the figure): first she described metamorphopsia, an effect located in the left inferior quadrant of the visual field, as if it was a bubble that distorted the image: “It’s like putting a drop of water in a glass… Or like a magnifying glass which moves upwards.” Sometimes she reported visual autobiographical hallucinations: a white and bright light that appears next to the area of metamorphopsia, where she could see personal memories quite clearly, for instance her deceased grandmother. In the right side of the figure, we present an image which resembles the experience described by the patient (courtesy of Grace Quintanilla, photographer).
magnifying glass moving upwards” (Figure 1). This visual illusion continued to appear repeatedly during her life, even once a week. In some occasions, it was followed by generalized tonic–clonic seizures. She also experienced a different visual phenomenon related to seizures, between age 5 and age 17. This phenomenon occurred just after the previously described visual illusion: “Sometimes I saw a luminous dot, a white and bright light. Inside it I could see different things… Once I saw my deceased grandmother; sitting down, wearing a beige dress. It was a very clear image, as if I was watching the television. I was fond of her… She died when I was very young… After that I had a strong seizure. On another occasion, I saw the image of an aerialist: it was a young woman with a white suit, juggling on a trapeze, jumping from one place to another. I have also seen the school janitor screaming, wearing a white and blue striped polo shirt.” However, she stated she could not hear this janitor, but she thought he was screaming because of the mimic language. These visual experiential hallucinations lasted between one and five minutes and always appeared before a generalized seizure. At age 16, she manifested a different phenomenon related to the recognition of her own body: “I was going to take a glass, so I extended my left hand to reach it and I asked myself: what is it that is moving? And then I realized it was my hand!”. A minute later, she had a generalized seizure. This phenomenon was repeated at age 28, and since then she has experienced it briefly but repeatedly. “I feel strangeness in my left side. It’s not asleep, I perceive pain, I can move it, the only strange thing is the feeling that it’s not mine. At the beginning it was only the arm, then it spread to the leg and the half of my face. It’s as if I was not there, I need to touch my leg in order to know I have one. I know it’s mine because I see it,
but not because I feel it.” This phenomenon appears twice a month and lasts from seconds to minutes. Although the patient successfully finished her bachelor’s degree, she works as a housewife because of her frequent seizures. Besides the clinical facts related to epilepsy, her medical history is unremarkable. In her physical examination, her physical and neurological indications were normal. The mental status examination was also normal regarding cognitive functions and emotional state. However, she expressed several concerns related to the lack of recognition of the left side of her body. “My husband doesn’t believe me, but sometimes I feel that my left arm and leg are not mine; I have to lay down on my left side to make some pressure on them because I feel they are so strange.” Aside from these subjective abnormalities, no delusions or somatoparaphrenia were observed in any of the interviews with the patient, nor did the family complain about psychotic symptoms. The reality test was normal, and her main explanation for the above-mentioned symptoms agreed with the medical explanations. The laboratory tests were normal, including a complete blood count, hepatic and renal function tests, serum electrolyte tests, and hormonal measurements. The interictal EEG was normal. The neuro-ophthalmological assessment was also normal. The MRI showed in the T1, T2, fluid attenuation inversion recovery, and echo-gradient sequences an abnormal image described as rounded, hypointense, with well-defined limits, in the right occipitotemporal cortex, and without perilesional edema (Figure 2). This lesion was classified as a nodular calcification due to neurocysticercosis. In the computed axial tomography scan, the density of the lesion was similar to that of the bone. This supports the calcified nature of the lesion.
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Figure 2. Brain imaging findings in a 36-year-old female patient with visual hallucinations of autobiographic memory and asomatognosia as epileptic ictal phenomena. The interictal 18F-FDG PET shows hypometabolism in the right parietal cortex (A coronal, C axial3D) and in the right posterior temporal cortex (B coronal). Magnetic resonance imaging (MRI) revealed a well-defined, round hypointense lesion located in the right occipitotemporal cortex, as seen in the T1 sequence (E). Echo-gradient sequences confirm the hypointense aspect of this parasitic lesion, and a close-up reveals the scolex of the parasite, a pathognomonic feature of cysticercosis, which may be seen as a small isointense feature within the hypointense lesion (D). These studies reveal the localization of the epileptogenic lesion (D, E) and the epileptogenic zone (B) probably related to the metamorphopsia as well as the functional deficit zone (A, C) related to asomatognosia. The arrows indicate the areas of interest that should be compared. [To view this figure in color, please see the online version of this journal.]
Interictal brain positron emission tomography with F-fluorodeoxyglucose (18F-FDG PET) was performed using a PET/CT scanner Biograph 16 (Siemens) with the standard clinical protocol. The 18F-FDG PET study showed mild hypometabolism in two regions: the right posterior temporal cortex and the right parietal cortex (Figure 2). The rest of the study was within normal limits. The International Neuropsychiatric Mini Interview did not reveal any mental disorders according to the DSM-V or to the International Classification of Disease, 10th version. A diagnosis of focal temporo-parieto-occipital (temporal “plus”) (Barba, Barbati, Minotti, Hoffmann, & Kahane, 2007) symptomatic epilepsy due to brain cysticercosis was made, and a treatment with valproic acid (500 mg b.i.d.) and levetiracetam (500 mg b.i.d.) was established successfully, reducing the frequency of the seizures. 18
Discussion The present case refers to a young woman who attended the Epilepsy Clinic at the National Institute of Neurology and Neurosurgery in Mexico City due to several ictal neuropsychiatric disturbances, including visual illusions in the form of metamorphopsia, visual experiential hallucinations, and asomatognosia. While EEG was normal, CT and MRI studies revealed the presence of a calcified lesion corresponding to neurocysticercosis (Lerner, Shiroishi,
Zee, Law, & Go, 2012), located in the right occipitotemporal cortex. Brain cysticercosis is the most common parasitic disorder affecting the central nervous system; it often provokes epilepsy and neuropsychiatric disturbances are not rare (Ramirez-Bermudez et al., 2005). The PET scan revealed two zones of hypometabolism that could not be identified by means of CT and MRI scans (except for the calcification): the right posterior temporal cortex and the right parietal cortex. This shows the complementarity of these brain imaging methods in the approach to epilepsy patients. 18F-FDG PET is a sensitive minimally invasive method for measuring brain metabolism. Interictal PET with 18F-FDG has demonstrated its suitability in the assessment of patients with epilepsy, by depicting areas of cortical hypometabolism related with epileptogenic and functional deficit zones (Goffin, Dedeurwaerdere, Van Laere, & Van Paesschen, 2008; Rosenow & Luders, 2001). It is best indicated when there are no anomalies in structural neuroimaging studies (Carne et al., 2004; Kumar & Chugani, 2013; Swartz et al., 2002). Even though the medical diagnosis was successful and the patient had a good outcome, the symptoms were quite disturbing for her, so she asked for a scientific explanation. We consider that the neurobiological correlates of asomatognosia, visual hallucinations, and visual illusions provided by means of brain imaging represent an opportunity to review the current hypothesis regarding the neuropsychiatric features of the case.
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Visual hallucinations of autobiographic memory The description of these events is consistent with seizures, taking into account that the duration of the experience, the stereotyped nature of the images, and the sudden onset strongly suggest an ictal phenomena, as does the secondary generalization observed in some events. Other neuropsychiatric disorders that may produce visual hallucinations were ruled out by means of repeated psychiatric interviews (including the MINI interview), standardized criteria (including DSM-V and ICD-10), and clinical consensus by two psychiatrists (JMOR and JRB). These categories include psychotic disorders of the schizophrenia spectrum, dementia with Lewy bodies, Parkinson’s disease, peduncular hallucinosis, Charles Bonnet syndrome, and delirium- and hallucinogen-induced disorders, among others. A formal assessment by the Neuro-ophthalmology Department was done in order to rule out visual acuity defects associated with Charles Bonnet syndrome. Simple visual hallucinations are common in occipital lobe epilepsy, with a prevalence described as being from 8% (Marques-Assis, Livramento, & Cury, 1971) to 72% (Salanova, Andermann, Oliver, Rasmussen, & Quesney, 1992). In our patient, the presence of elementary hallucinations in the left temporal quadrant of the left eye indicates that the lesion was located at the level of the right unimodal visual cortex. Structural MRI confirmed this localization; a calcified parasitic lesion was observed. Complex visual hallucinations are much more difficult to localize than elementary ones. An activation of the limbic system might be necessary for the production of complex visual hallucinations (Fish, Gloor, Quesney, & Oliver, 1993). By means of intracranial electrodes, Vignal, Maillard, McGonigal, and Chauvel (2007) designed a study of “dream-like” states. These authors concluded that the stimulation of the medial temporal regions provoked dream-like states and visual autobiographical hallucinations. Besides the variable contents of hallucinatory experience, the subjects most often experienced visions of people, as did our patient, who saw her grandmother, an aerialist and the school janitor. Even though our patient didn’t have temporal lobe epilepsy, autobiographic phenomena appeared. Intracerebral recordings in occipital epilepsy have shown how a fast propagation of the epileptic activity may involve temporal, parietal, and occipital regions (Bancaud, 1969; Takeda, Bancaud, Talairach, Bonis, & Bordas-Ferrer, 1970; Taylor, Scheffer, & Berkovic, 2003). In our case, a propagation of the abnormal epileptic activity toward the right medial temporal regions could account for the emergence of complex visual hallucinations of autobiographic memory. This case is also in accordance with previous studies about the neurobiology of autobiographic memory, which has shown that although left hemisphere activation is required to initiate search processes of autobiographical
knowledge, the posterior regions of the right hemisphere may be of critical relevance to support the retrieval process involved in the re-experiencing of an autobiographic event (Conway, Pleydell-Pearce, Whitecross, & Sharpe, 2002; Svoboda, McKinnon, & Levine, 2006). Visual illusions This case also provides useful insight into the classic phenomena of visual illusions, which can be divided into simple and complex. Our patient’s illusion clearly corresponds to a metamorphopsia because the main visual attributes under distortion are the form and contour of the objects located in the left hemifield. In fact, Heo et al. (2004) described a similar case in a patient with intermittent periods of facial metamorphopsia in which she saw people with grotesque and distorted facial aspects; this experience lasted a few minutes and recurred between 15 and 30 times a day. The MRI study revealed an encephalomalacy zone in the right temporo-occipital junction due to an old hypertensive hemorrhage. Asomatognosia Asomatognosia refers to the absence of body recognition and is one of the most amazing neuropsychiatric symptoms (Feinberg, Venneri, Simone, Fan, & Northoff, 2010). The most common form of asomatognosia is the lack of recognition and loss of ownership sensation in the left side of the body. This phenomenon is also known as hemiasomatognosia. Most often, this is a transitory symptom; for instance, it may appear during an epileptic seizure (Jam, 1985; So & Schauble, 2004). Thomas, Giraud, Alchaar, and Chatel (1998) described the case of a 69-year-old woman with ictal asomatognosia associated to hemiparesis, in the context of a simple partial nonconvulsive status epilepticus of right parieto-temporal origin. The present case supports the evidence for ictal asomatognosia as a rare but reliable localizing epileptic phenomenon. Although the epileptogenic lesion was located in the occipitotemporal region, the right parietal hypometabolism detected by means of PET imaging should be in close relationship to asomatognosia. The neuroanatomical basis of this symptom has been explored in different studies, and it has usually been associated to right temporo-parietal regions and thalamo-parietal projections (Feinberg, Haber, & Leeds, 1990; Feinberg et al., 2010). Right prefrontal cortex damage may also give rise to a multisensory deficit of left limb awareness (Arzy, Overney, Landis, & Blanke, 2006). Along with other clinical phenomena related to limb ownership, including anosognosia for hemiplegia, somatoparaphrenia, anosodiaphoria, and personification, asomatognosia has also been linked to insular damage in the right hemisphere, suggesting a neocortical–paralimbic
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Neurocase network dedicated to the integration of multisensory perceptual information and its relationship with emotional networks (Baier & Karnath, 2008). Although the dominant role of the right hemisphere in this phenomenon is generally accepted, it has been reported that left parietal lesions can exceptionally provoke right hemiasomatognosia, as described by Nishibayashi et al. (2011) who reported a case of a 23-year-old patient with left parietal cortical dysplasia who presented with an ictal loss of sensation in the right extremities. Invasive EEG monitoring showed ictal discharges in the cortex posterior to the postcentral sulcus. Asomatognosia can also be associated with paroxysmal alien hand-like behaviors in the context of partial status epilepticus (Feinberg, Roane, & Cohen, 1998). This relationship is interesting because asomatognosia is conceptualized as a lack of ownership feelings regarding left-side extremities, whereas alien hand syndrome refers to a loss of agency feelings, which means the subjective experience of not being in charge of one’s movements. It is possible that these phenomena (agency and ownership) are functionally related. Both of them have a critical participation in the construction of self-experience, which may fail in psychiatric syndromes such as depersonalization (Sierra, Lopera, Lambert, Phillips, & David, 2002) and delusions of alien control, often documented in patients with a diagnosis of schizophrenia (Frith, 2005). Besides, asomatognosia may present along with anosognosia, a well-known disorder of self-consciousness (Meador, Loring, Feinberg, Lee, & Nichols, 2000). Taken together, these symptoms and their link to the right hemisphere have been proposed as valuable sources to investigate the lateralization of self-consciousness neurobiology, closely related to the neural coding of embodiment, and particularly to the neuropsychology of agency and ownership feelings. The present case also supports previous views concerned with the construction of bodily self-consciousness and the critical role of the temporoparietal junction, along with other brain structures including the dorso-medial parietal cortex, the prefrontal cortex, and the default network (Heydrich, Dieguez, Grunwald, Seeck, & Blanke, 2010; Ionta et al., 2011). It has been posed that bodily selfconsciousness depends on multisensory information organized by cortical areas dedicated to self-identification (body ownership), self-location, and the building of first-person perspective (Blanke, 2012). Asomatognosia can be conceptualized as a lateralized disorder of body ownership which poses a right hemisphere dominance for bodily self-consciousness, along with other lateralized disorders as alien-limb syndrome, somatoparaphrenia, and anosognosia for plegia (Baier & Karnath, 2008). Interestingly, our patient showed a limb-ownership disorder not affecting self-location or first-person perspective, suggesting that these mechanisms can be dissociated in brain pathology.
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Final remarks Epilepsy is now known as a network disease (Wendling, Chauvel, Biraben, & Bartolomei, 2010); however, in this case the concepts of cortical zones help us to understand how the epileptogenic lesion overlaps with the epileptogenic zone and its relationship with the symptomatogenic and functional deficit zones. Our hypothesis to explain the neuropsychiatric dimension of the case is the following: there is an epileptogenic lesion corresponding to the aforementioned calcification located in the right occipitotemporal cortex. This cortex receives inputs from different unimodal areas located in the occipital, temporal, and parietal areas (Mesulam, 1998). This area also showed interictal hypometabolism, a fact that suggests that the epileptic activity arises from it (la Fougère, Rominger, Förster, Geisler, & Bartenstein, 2009). This epileptogenic zone is associated with different symptomatogenic zones (Rosenow & Luders, 2001). This means that an abnormal epileptic activity propagates through several topographic routes that generate symptoms beyond the epileptic origin. The propagation of activity through the occipital lobe is related to elementary visual hallucinations, whereas the distribution through the occipitotemporal pathway could generate the experience of metamorphopsia. Probably, the visual experiential hallucination arises when the epileptiform discharge reaches the anterior and medial temporal regions (amygdala and hippocampus). Finally, the asomatognosia should be related to the extension through the parietal lobe, which corresponds to the functional deficit zone revealed by the interictal hypometabolism. The present case provides a functional anatomy understanding of the many neuropsychiatric faces of epilepsy and brain cysticercosis. Acknowledgments We acknowledge both the Pontificia Universidad Javeriana of Bogotá, Colombia, and the McGill University Writing Center for their academic support.
Disclosure statement No potential conflict of interest was reported by the authors.
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Neurocase: The Neural Basis of Cognition Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/nncs20
Visual hallucinations of autobiographic memory and asomatognosia: a case of epilepsy due to brain cysticercosis a
ab
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Juan Manuel Orjuela-Rojas , Jesús Ramírez-Bermúdez , Iris E. Martínez-Juárez , Nora d
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Estela Kerik , Iván Diaz Meneses & Fernanda Juárez Pérez-Gay
ef
a
Neuropsychiatry Unit, National Institute of Neurology and Neurosurgery, Mexico City, Mexico b
Medical School, National University of Mexico, Mexico City, Mexico
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Epilepsy Clinic, National Institute of Neurology and Neurosurgery, Mexico City, Mexico
d
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Molecular Imaging PET/CT Unit, National Institute of Neurology and Neurosurgery, Mexico City, Mexico e
Institut des Sciences Cognitives, Université du Québec à Montréal, Montréal, Canada
f
Integrated Program in Neuroscience, McGill University, Montréal, Canada Published online: 10 Oct 2014.
To cite this article: Juan Manuel Orjuela-Rojas, Jesús Ramírez-Bermúdez, Iris E. Martínez-Juárez, Nora Estela Kerik, Iván Diaz Meneses & Fernanda Juárez Pérez-Gay (2014): Visual hallucinations of autobiographic memory and asomatognosia: a case of epilepsy due to brain cysticercosis, Neurocase: The Neural Basis of Cognition, DOI: 10.1080/13554794.2014.962548 To link to this article: http://dx.doi.org/10.1080/13554794.2014.962548
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Neurocase, 2014 http://dx.doi.org/10.1080/13554794.2014.962548
Visual hallucinations of autobiographic memory and asomatognosia: a case of epilepsy due to brain cysticercosis Juan Manuel Orjuela-Rojasa*, Jesús Ramírez-Bermúdeza,b, Iris E. Martínez-Juárezc, Nora Estela Kerikd, Iván Diaz Menesesd and Fernanda Juárez Pérez-Gaye,f Neuropsychiatry Unit, National Institute of Neurology and Neurosurgery, Mexico City, Mexico; bMedical School, National University of Mexico, Mexico City, Mexico; cEpilepsy Clinic, National Institute of Neurology and Neurosurgery, Mexico City, Mexico; dMolecular Imaging PET/CT Unit, National Institute of Neurology and Neurosurgery, Mexico City, Mexico; eInstitut des Sciences Cognitives, Université du Québec à Montréal, Montréal, Canada; fIntegrated Program in Neuroscience, McGill University, Montréal, Canada
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(Received 26 February 2014; accepted 3 September 2014) The current study describes the case of a woman with symptomatic epilepsy due to brain cysticercosis acquired during childhood. During her adolescence, she developed seizures characterized by metamorphopsia, hallucinations of autobiographic memory and, finally, asomatognosia. Magnetic brain imaging showed a calcified lesion in the right occipitotemporal cortex, and positron emission tomography imaging confirmed the presence of interictal hypometabolism in two regions: the right parietal cortex and the right lateral and posterior temporal cortex. We discuss the link between these brain areas and the symptoms described under the concepts of epileptogenic lesion, epileptogenic zone, functional deficit zone, and symptomatogenic zone. Keywords: metamorphopsia; asomatognosia; autobiographical hallucinations; epilepsy; neurocysticercosis
In 1938, Wilder Penfield described two main types of “mental phenomena” elicited by the electric stimulation of the cerebral cortex. He called “experiential phenomena” to the occurrence of mental experiences related to the personal background of the subject: autobiographic images or vivid memories in which perception, memory, and emotion are expressed in a unified manner (Elliott, Joyce, & Shorvon, 2009; Gloor, Olivier, Quesney, Andermann, & Horowitz, 1982). He also described other phenomena concerning the interpretation of the current situation of the subject, including illusions and emotional changes. He referred to these types of experiences as “interpretative phenomena.” Here, we present a clinical case of temporo-parietooccipital epilepsy that comprises both types of mental phenomena according to Penfield’s terminology: experiential and interpretative. In this case, they appear under the form of visual autobiographic hallucinations (classically named visual experiential hallucination), metamorphopsia, and asomatognosia. Lüders (Rosenow & Luders, 2001) described the epileptogenic zone as the “area of cortex that is indispensable for the generation of epileptic seizures”; the epileptogenic lesion as the radiographic lesion responsible for the generation of the seizures; the symptomatogenic zone as the one that reproduces the ictal symptomatology and the functional deficit zone as the area of the brain that shows abnormalities during the interictal period, which can be *Corresponding author. Email: [email protected] © 2014 Taylor & Francis
determined through the neurological or/and neuropsychological exams, electroencephalogram (EEG), singlephoton emission computed tomography (CT), positron emission tomography (PET), or other functional tests. Through the patient’s case work-up, magnetic resonance imaging (MRI) studies revealed the epileptogenic lesion, which in turn is related to the epileptogenic zone. The variety in the clinical symptomatology revealed multiple symptomatogenic zones, and the PET scan showed the epileptogenic and the functional deficit zones. Case report We present the case of a married 36-year-old woman with a bachelor’s degree in Psychology. Her clinical problem started when she was 5 years old, when she suddenly presented with fever, headache, leftward gaze deviation, vomiting, and generalized tonic–clonic seizures. At age 9, she reported seeing intermittent, colorful lights that appeared in the inferior and temporal quadrant of her left eye and lasted for a few seconds. During her adolescence, these visual phenomena were accompanied by illusions consisting of metamorphopsias. During these events, she experienced a distortion in the visual perception of the environment for a few seconds: “I see something like a bubble that appears in the left side of my eye, as if it was a kaleidoscope distorting the people, the lines, everything… It’s like putting a drop of water in a glass… Or like a
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Figure 1. Graphic representation of ictal metamorphopsia and visual hallucinations of autobiographic memory. The patient draw a schematic representation of the ictal visual phenomena (left side of the figure): first she described metamorphopsia, an effect located in the left inferior quadrant of the visual field, as if it was a bubble that distorted the image: “It’s like putting a drop of water in a glass… Or like a magnifying glass which moves upwards.” Sometimes she reported visual autobiographical hallucinations: a white and bright light that appears next to the area of metamorphopsia, where she could see personal memories quite clearly, for instance her deceased grandmother. In the right side of the figure, we present an image which resembles the experience described by the patient (courtesy of Grace Quintanilla, photographer).
magnifying glass moving upwards” (Figure 1). This visual illusion continued to appear repeatedly during her life, even once a week. In some occasions, it was followed by generalized tonic–clonic seizures. She also experienced a different visual phenomenon related to seizures, between age 5 and age 17. This phenomenon occurred just after the previously described visual illusion: “Sometimes I saw a luminous dot, a white and bright light. Inside it I could see different things… Once I saw my deceased grandmother; sitting down, wearing a beige dress. It was a very clear image, as if I was watching the television. I was fond of her… She died when I was very young… After that I had a strong seizure. On another occasion, I saw the image of an aerialist: it was a young woman with a white suit, juggling on a trapeze, jumping from one place to another. I have also seen the school janitor screaming, wearing a white and blue striped polo shirt.” However, she stated she could not hear this janitor, but she thought he was screaming because of the mimic language. These visual experiential hallucinations lasted between one and five minutes and always appeared before a generalized seizure. At age 16, she manifested a different phenomenon related to the recognition of her own body: “I was going to take a glass, so I extended my left hand to reach it and I asked myself: what is it that is moving? And then I realized it was my hand!”. A minute later, she had a generalized seizure. This phenomenon was repeated at age 28, and since then she has experienced it briefly but repeatedly. “I feel strangeness in my left side. It’s not asleep, I perceive pain, I can move it, the only strange thing is the feeling that it’s not mine. At the beginning it was only the arm, then it spread to the leg and the half of my face. It’s as if I was not there, I need to touch my leg in order to know I have one. I know it’s mine because I see it,
but not because I feel it.” This phenomenon appears twice a month and lasts from seconds to minutes. Although the patient successfully finished her bachelor’s degree, she works as a housewife because of her frequent seizures. Besides the clinical facts related to epilepsy, her medical history is unremarkable. In her physical examination, her physical and neurological indications were normal. The mental status examination was also normal regarding cognitive functions and emotional state. However, she expressed several concerns related to the lack of recognition of the left side of her body. “My husband doesn’t believe me, but sometimes I feel that my left arm and leg are not mine; I have to lay down on my left side to make some pressure on them because I feel they are so strange.” Aside from these subjective abnormalities, no delusions or somatoparaphrenia were observed in any of the interviews with the patient, nor did the family complain about psychotic symptoms. The reality test was normal, and her main explanation for the above-mentioned symptoms agreed with the medical explanations. The laboratory tests were normal, including a complete blood count, hepatic and renal function tests, serum electrolyte tests, and hormonal measurements. The interictal EEG was normal. The neuro-ophthalmological assessment was also normal. The MRI showed in the T1, T2, fluid attenuation inversion recovery, and echo-gradient sequences an abnormal image described as rounded, hypointense, with well-defined limits, in the right occipitotemporal cortex, and without perilesional edema (Figure 2). This lesion was classified as a nodular calcification due to neurocysticercosis. In the computed axial tomography scan, the density of the lesion was similar to that of the bone. This supports the calcified nature of the lesion.
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Figure 2. Brain imaging findings in a 36-year-old female patient with visual hallucinations of autobiographic memory and asomatognosia as epileptic ictal phenomena. The interictal 18F-FDG PET shows hypometabolism in the right parietal cortex (A coronal, C axial3D) and in the right posterior temporal cortex (B coronal). Magnetic resonance imaging (MRI) revealed a well-defined, round hypointense lesion located in the right occipitotemporal cortex, as seen in the T1 sequence (E). Echo-gradient sequences confirm the hypointense aspect of this parasitic lesion, and a close-up reveals the scolex of the parasite, a pathognomonic feature of cysticercosis, which may be seen as a small isointense feature within the hypointense lesion (D). These studies reveal the localization of the epileptogenic lesion (D, E) and the epileptogenic zone (B) probably related to the metamorphopsia as well as the functional deficit zone (A, C) related to asomatognosia. The arrows indicate the areas of interest that should be compared. [To view this figure in color, please see the online version of this journal.]
Interictal brain positron emission tomography with F-fluorodeoxyglucose (18F-FDG PET) was performed using a PET/CT scanner Biograph 16 (Siemens) with the standard clinical protocol. The 18F-FDG PET study showed mild hypometabolism in two regions: the right posterior temporal cortex and the right parietal cortex (Figure 2). The rest of the study was within normal limits. The International Neuropsychiatric Mini Interview did not reveal any mental disorders according to the DSM-V or to the International Classification of Disease, 10th version. A diagnosis of focal temporo-parieto-occipital (temporal “plus”) (Barba, Barbati, Minotti, Hoffmann, & Kahane, 2007) symptomatic epilepsy due to brain cysticercosis was made, and a treatment with valproic acid (500 mg b.i.d.) and levetiracetam (500 mg b.i.d.) was established successfully, reducing the frequency of the seizures. 18
Discussion The present case refers to a young woman who attended the Epilepsy Clinic at the National Institute of Neurology and Neurosurgery in Mexico City due to several ictal neuropsychiatric disturbances, including visual illusions in the form of metamorphopsia, visual experiential hallucinations, and asomatognosia. While EEG was normal, CT and MRI studies revealed the presence of a calcified lesion corresponding to neurocysticercosis (Lerner, Shiroishi,
Zee, Law, & Go, 2012), located in the right occipitotemporal cortex. Brain cysticercosis is the most common parasitic disorder affecting the central nervous system; it often provokes epilepsy and neuropsychiatric disturbances are not rare (Ramirez-Bermudez et al., 2005). The PET scan revealed two zones of hypometabolism that could not be identified by means of CT and MRI scans (except for the calcification): the right posterior temporal cortex and the right parietal cortex. This shows the complementarity of these brain imaging methods in the approach to epilepsy patients. 18F-FDG PET is a sensitive minimally invasive method for measuring brain metabolism. Interictal PET with 18F-FDG has demonstrated its suitability in the assessment of patients with epilepsy, by depicting areas of cortical hypometabolism related with epileptogenic and functional deficit zones (Goffin, Dedeurwaerdere, Van Laere, & Van Paesschen, 2008; Rosenow & Luders, 2001). It is best indicated when there are no anomalies in structural neuroimaging studies (Carne et al., 2004; Kumar & Chugani, 2013; Swartz et al., 2002). Even though the medical diagnosis was successful and the patient had a good outcome, the symptoms were quite disturbing for her, so she asked for a scientific explanation. We consider that the neurobiological correlates of asomatognosia, visual hallucinations, and visual illusions provided by means of brain imaging represent an opportunity to review the current hypothesis regarding the neuropsychiatric features of the case.
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Visual hallucinations of autobiographic memory The description of these events is consistent with seizures, taking into account that the duration of the experience, the stereotyped nature of the images, and the sudden onset strongly suggest an ictal phenomena, as does the secondary generalization observed in some events. Other neuropsychiatric disorders that may produce visual hallucinations were ruled out by means of repeated psychiatric interviews (including the MINI interview), standardized criteria (including DSM-V and ICD-10), and clinical consensus by two psychiatrists (JMOR and JRB). These categories include psychotic disorders of the schizophrenia spectrum, dementia with Lewy bodies, Parkinson’s disease, peduncular hallucinosis, Charles Bonnet syndrome, and delirium- and hallucinogen-induced disorders, among others. A formal assessment by the Neuro-ophthalmology Department was done in order to rule out visual acuity defects associated with Charles Bonnet syndrome. Simple visual hallucinations are common in occipital lobe epilepsy, with a prevalence described as being from 8% (Marques-Assis, Livramento, & Cury, 1971) to 72% (Salanova, Andermann, Oliver, Rasmussen, & Quesney, 1992). In our patient, the presence of elementary hallucinations in the left temporal quadrant of the left eye indicates that the lesion was located at the level of the right unimodal visual cortex. Structural MRI confirmed this localization; a calcified parasitic lesion was observed. Complex visual hallucinations are much more difficult to localize than elementary ones. An activation of the limbic system might be necessary for the production of complex visual hallucinations (Fish, Gloor, Quesney, & Oliver, 1993). By means of intracranial electrodes, Vignal, Maillard, McGonigal, and Chauvel (2007) designed a study of “dream-like” states. These authors concluded that the stimulation of the medial temporal regions provoked dream-like states and visual autobiographical hallucinations. Besides the variable contents of hallucinatory experience, the subjects most often experienced visions of people, as did our patient, who saw her grandmother, an aerialist and the school janitor. Even though our patient didn’t have temporal lobe epilepsy, autobiographic phenomena appeared. Intracerebral recordings in occipital epilepsy have shown how a fast propagation of the epileptic activity may involve temporal, parietal, and occipital regions (Bancaud, 1969; Takeda, Bancaud, Talairach, Bonis, & Bordas-Ferrer, 1970; Taylor, Scheffer, & Berkovic, 2003). In our case, a propagation of the abnormal epileptic activity toward the right medial temporal regions could account for the emergence of complex visual hallucinations of autobiographic memory. This case is also in accordance with previous studies about the neurobiology of autobiographic memory, which has shown that although left hemisphere activation is required to initiate search processes of autobiographical
knowledge, the posterior regions of the right hemisphere may be of critical relevance to support the retrieval process involved in the re-experiencing of an autobiographic event (Conway, Pleydell-Pearce, Whitecross, & Sharpe, 2002; Svoboda, McKinnon, & Levine, 2006). Visual illusions This case also provides useful insight into the classic phenomena of visual illusions, which can be divided into simple and complex. Our patient’s illusion clearly corresponds to a metamorphopsia because the main visual attributes under distortion are the form and contour of the objects located in the left hemifield. In fact, Heo et al. (2004) described a similar case in a patient with intermittent periods of facial metamorphopsia in which she saw people with grotesque and distorted facial aspects; this experience lasted a few minutes and recurred between 15 and 30 times a day. The MRI study revealed an encephalomalacy zone in the right temporo-occipital junction due to an old hypertensive hemorrhage. Asomatognosia Asomatognosia refers to the absence of body recognition and is one of the most amazing neuropsychiatric symptoms (Feinberg, Venneri, Simone, Fan, & Northoff, 2010). The most common form of asomatognosia is the lack of recognition and loss of ownership sensation in the left side of the body. This phenomenon is also known as hemiasomatognosia. Most often, this is a transitory symptom; for instance, it may appear during an epileptic seizure (Jam, 1985; So & Schauble, 2004). Thomas, Giraud, Alchaar, and Chatel (1998) described the case of a 69-year-old woman with ictal asomatognosia associated to hemiparesis, in the context of a simple partial nonconvulsive status epilepticus of right parieto-temporal origin. The present case supports the evidence for ictal asomatognosia as a rare but reliable localizing epileptic phenomenon. Although the epileptogenic lesion was located in the occipitotemporal region, the right parietal hypometabolism detected by means of PET imaging should be in close relationship to asomatognosia. The neuroanatomical basis of this symptom has been explored in different studies, and it has usually been associated to right temporo-parietal regions and thalamo-parietal projections (Feinberg, Haber, & Leeds, 1990; Feinberg et al., 2010). Right prefrontal cortex damage may also give rise to a multisensory deficit of left limb awareness (Arzy, Overney, Landis, & Blanke, 2006). Along with other clinical phenomena related to limb ownership, including anosognosia for hemiplegia, somatoparaphrenia, anosodiaphoria, and personification, asomatognosia has also been linked to insular damage in the right hemisphere, suggesting a neocortical–paralimbic
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Neurocase network dedicated to the integration of multisensory perceptual information and its relationship with emotional networks (Baier & Karnath, 2008). Although the dominant role of the right hemisphere in this phenomenon is generally accepted, it has been reported that left parietal lesions can exceptionally provoke right hemiasomatognosia, as described by Nishibayashi et al. (2011) who reported a case of a 23-year-old patient with left parietal cortical dysplasia who presented with an ictal loss of sensation in the right extremities. Invasive EEG monitoring showed ictal discharges in the cortex posterior to the postcentral sulcus. Asomatognosia can also be associated with paroxysmal alien hand-like behaviors in the context of partial status epilepticus (Feinberg, Roane, & Cohen, 1998). This relationship is interesting because asomatognosia is conceptualized as a lack of ownership feelings regarding left-side extremities, whereas alien hand syndrome refers to a loss of agency feelings, which means the subjective experience of not being in charge of one’s movements. It is possible that these phenomena (agency and ownership) are functionally related. Both of them have a critical participation in the construction of self-experience, which may fail in psychiatric syndromes such as depersonalization (Sierra, Lopera, Lambert, Phillips, & David, 2002) and delusions of alien control, often documented in patients with a diagnosis of schizophrenia (Frith, 2005). Besides, asomatognosia may present along with anosognosia, a well-known disorder of self-consciousness (Meador, Loring, Feinberg, Lee, & Nichols, 2000). Taken together, these symptoms and their link to the right hemisphere have been proposed as valuable sources to investigate the lateralization of self-consciousness neurobiology, closely related to the neural coding of embodiment, and particularly to the neuropsychology of agency and ownership feelings. The present case also supports previous views concerned with the construction of bodily self-consciousness and the critical role of the temporoparietal junction, along with other brain structures including the dorso-medial parietal cortex, the prefrontal cortex, and the default network (Heydrich, Dieguez, Grunwald, Seeck, & Blanke, 2010; Ionta et al., 2011). It has been posed that bodily selfconsciousness depends on multisensory information organized by cortical areas dedicated to self-identification (body ownership), self-location, and the building of first-person perspective (Blanke, 2012). Asomatognosia can be conceptualized as a lateralized disorder of body ownership which poses a right hemisphere dominance for bodily self-consciousness, along with other lateralized disorders as alien-limb syndrome, somatoparaphrenia, and anosognosia for plegia (Baier & Karnath, 2008). Interestingly, our patient showed a limb-ownership disorder not affecting self-location or first-person perspective, suggesting that these mechanisms can be dissociated in brain pathology.
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Final remarks Epilepsy is now known as a network disease (Wendling, Chauvel, Biraben, & Bartolomei, 2010); however, in this case the concepts of cortical zones help us to understand how the epileptogenic lesion overlaps with the epileptogenic zone and its relationship with the symptomatogenic and functional deficit zones. Our hypothesis to explain the neuropsychiatric dimension of the case is the following: there is an epileptogenic lesion corresponding to the aforementioned calcification located in the right occipitotemporal cortex. This cortex receives inputs from different unimodal areas located in the occipital, temporal, and parietal areas (Mesulam, 1998). This area also showed interictal hypometabolism, a fact that suggests that the epileptic activity arises from it (la Fougère, Rominger, Förster, Geisler, & Bartenstein, 2009). This epileptogenic zone is associated with different symptomatogenic zones (Rosenow & Luders, 2001). This means that an abnormal epileptic activity propagates through several topographic routes that generate symptoms beyond the epileptic origin. The propagation of activity through the occipital lobe is related to elementary visual hallucinations, whereas the distribution through the occipitotemporal pathway could generate the experience of metamorphopsia. Probably, the visual experiential hallucination arises when the epileptiform discharge reaches the anterior and medial temporal regions (amygdala and hippocampus). Finally, the asomatognosia should be related to the extension through the parietal lobe, which corresponds to the functional deficit zone revealed by the interictal hypometabolism. The present case provides a functional anatomy understanding of the many neuropsychiatric faces of epilepsy and brain cysticercosis. Acknowledgments We acknowledge both the Pontificia Universidad Javeriana of Bogotá, Colombia, and the McGill University Writing Center for their academic support.
Disclosure statement No potential conflict of interest was reported by the authors.
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