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Anatomic correlates of psychological events related to temporolimbic epilepsy.

Introduction

Throughout history, ordinary people have been prompted to action by unusual phenomena. Others, after experiencing similar events, have accomplished unthinkable feats of courage and brilliance which have altered the course of mankind. Saul of Tarsus, a staunch Roman citizen, made a passionate conversion to Christianity after a cataclysmic event of light and voices Jeanne d'Arc, the pious daughter of a cattle herder and ploughman, was commanded by voices to lead the French rebellion against the invading Church of England. Fyodor M. Dostoevsky, a prolific Russian novelist, experienced such overwhelming feelings of ecstasy, that he was moved to incorporate the phenomenon into the personality of his characters.

What part did these unusual psychological events play in these demonstrations of fervor and commitment? Modern science, albeit retrospectively, with its technologies of electroencephalography (EEG) magnetic resonance imaging (MRI) and positron emission tomography (PET) has speculated that for these individuals, a seizure disorder may have played an instrumental role in their perception of and interaction with reality and the extrapersonal environment. All three of these individuals had recurrent experiences that were characterized by subjective phenomena. Contemporaries of these individuals, indeed the persons themselves, speculated on the foundation of their sanity and the forces shaping their lives.[16,28,48]

Today many of these experiences are thought to be partial seizures with psychologic symptomology. However, the association of mental illness and seizures continues to be an enduring myth. A comparative study by Silberman found that the transient sensory, cognitive and affective behaviors which constitute the basis of the DSM III-R diagnosis code for affective disorders occur more frequently in the individual with complex partial seizures.[45] This finding alone should make any nurse practitioner suspect of psychological behaviors in the general medical population as well as the neuroscience patient.

This paper will attempt to present the various affective behaviors which can be associated with temporal lobe epilepsy. Basic to this discussion will be a brief review of the pertinent anatomy and current theories of physiologic relationships.

Subjective Reporting of Affective Disturbances

Disturbances in motor behavior are commonly recognized as seizure activity. Less frequently identified however, are those ictal alterations which are sensory, autonomic, experiential and emotional. Joan of Arc heard voices. Dostoevsky and St. Paul experienced the heights of ecstasy as well as convulsive attacks. Your patient may experience unexplainable feelings of doom. These ictal phenomenon are all very subjective and cannot be observed by anyone else. It is the subjectivity of these symptoms which can result in lack of recognition by the nurse, or underreporting of the ictal event by the individual.

A sensory event may present as an isolated symptom or in association with an emotional component. Because this ictus has an internal, rather than an external origin, it is referred to as a hallucination. Sensory events, or hallucinations, may be unformed/simple or formed/complex. Studies indicate that unformed events usually arise from the primary sensory regions,[10,19] while formed hallucinations originate in the associative and limbic regions as well as the medial temporal area.[19,51] As with other behaviors associated with epilepsy, the epileptic hallucinations tend to be stereotypic, involving the same voices, sounds or sights. This may differentiate them from psychotic hallucinations, which tend to vary with each event, different voices, sights, or messages. Because of the association between hallucinations and mental illness, the patient may not report altered psychological behaviors associated with seizure activity even if specifically queried. Even when questioned, the patient may not divulge the subjective experience due to feelings of vulnerability and mistrust.

Specific Sensory Alterations

Gloor and King found that visual hallucinations are the most common phenomena, occurring in approximately 20% of individuals with temporal lobe seizures.[19,26] Visual hallucinations can produce distortion of size (micropsia/macropsia) as well as alteration of shape and color. Motion, illumination and distance can also be affected. Complex visual hallucinations usually indicate a posterior temporal onset[51] with the right hemisphere commonly involved.[36] Simple visual hallucinations, ie, flashing lights, may result from occipital seizures.

Case Study

A 27 year-old man had recurring seizures for one year. On one occasion, he saw a girl who was employed at the factory where he worked. Another time while walking, he saw the same or a similar girl walking. The street and buildings seemed to disappear. He continued to walk and when he reached where she should have been, there was no one there.[40]

Auditory ictal events have been produced by stimulation of the lateral superior temporal lobe, specifically in the transverse gyrus of Heschl.[11,40] Simple, unformed hallucinations are most common. These may present as buzzing, ringing or distortion of volume and pitch. Complex hallucinations such as voices are thought to arise from the temporal lobe outside the primary auditory Cortex.[37,40]

Case Study

KN was a 23 year-old man with a diagnosis of a Grade 4 astrocytic brain tumor. For the five months prior to his diagnosis, he had been experiencing complex partial seizures which would occasionally become generalized. During the surgical work-up, it was discovered the he had been experiencing buzzing noises, and sounds like muffled, unintelligible conversation for three years prior to the onset of the more overt seizures. He had not shared this information with anyone because they "would've thought (he) was crazy."

Gustatory hallucinations have been found to originate from the parietal opercular region.[32,39] Distortion of taste is usually described as a bitter, sharp, sickly sweet blood, bile or metallic taste. Hausser-Hauw and Bancaud localized these hallucinations to the rolandic operculum. In their study, propagation of the seizure/auras to the suprasylvian area were accompanied by salivation, eye deviation and clonic facial contractions.[24]

Case Study

MJH is a 53 year-old woman with a history of paranoid depression and complex partial seizures. She had been in and out of institutions since the age of 17 years. One of her frequent hallucinations included that of caregivers "making drugs in the basement and giving them to her." She stated she knew when this was happening because "the pills tasted like metal shavings." Preoperative monitoring indicated an epileptogenic focus in the rolandic area which only infrequently spread to other regions. The paranoid ideation associated with the metallic tasting pills dramatically decreased following temporal lobe surgery.

Olfactory hallucinations occur infrequently as seizure activity. Generally originating from an anterior temporal lobe focus, the sensation is usually an unpleasant foul odor or one normally pleasant, which is so strong as to be excessive and overpowering. The incidence of olfactory auras is approximately 1% with common reporting of smells similar to burning rubber, sulfur or organic solvents.[9] Studies indicate that the uncus in the anteromesial temporal region and the basal frontal olfactory cortex can also be involved in this type of hallucination.[4,19]

Case Study

JM was a 54 year-old man admitted for monitoring of complex partial seizures. During one attack he was observed to squat down in the middle of the bed and sniff at the air with an unpleasant expression on his face. During the post-ictal review he related "smelling the stink of garbage" and felt he needed to "sit on the garbage can to make sure the lid was closed."

Vertiginous seizures result from stimulation of the superior temporal gyrus.[37] These seizures result in a feeling of displacement and movement, including rotary sensations. The most common rotation is around the vertical axis although rotation along the sagittal axis is also reported. Horizontal movements are reported as side to side and fore and aft sensations. Smith's study of 120 patients revealed the most common symptom to be a sense of spinning, which was commonly associated with epigastric sensations, sensory disturbances, dreamy states and loss of consciousness.[44] Specific questioning by the nurse is usually necessary to clarify the "dizziness" generally reported by the patient. Statements describing feelings of "falling into a bottomless pit," "going up of down in a fast elevator" or feelings of "the walls closing in" are all indications of epileptic vertigo.

Case Study

SM, a 21 year-old woman working as a school cook, was recently injured secondary to her new onset of seizure activity. For several months prior to the accident, SM had been noted to grab hold of something for support and hold her head as if she had a headache. Upon questioning she denied a headache or weakness, but was indeed experiencing brief episodes of what she related as a "fuzzy head" which would clear almost immediately. At the time of the accident, SM was noted to grab her head, twirl to the right and into a nearby stove with an active burner. She later reported the feeling as that similar to the spinning sensation of "log-rolling downhill like when I was a kid."

As partial seizures, the unformed hallucinations do not interfere greatly with the individual's quality of life. They may, however, prompt introspective comparison of "reality" to the external environment and often go unreported if the comparison is not validated. The complex hallucinations, however, particularly visual and auditory, may prompt a response which seems inappropriate to an observer unfamiliar with the seizure phenomenon. Observing an overt response to such a hallucination without thought of possible seizure activity does tend to suggest a diagnosis of mental illness, or substance abuse, particularly by the lay population.

Viscerosensory Phenomenology

Ictal phenomena which involve the autonomic system are primarily mediated by the insular cortex and the amygdala region with its connections to the hypothalamus,[27] as well as the opercular, mesial and orbito-frontal regions.[4] Sensations of nausea, butterflies in the stomach, gastrointestinal hypermotility or a rising sensation in the epigastric region are among the most common symptoms with significant localization to the right temporal lobe.[27] Other autonomic phenomenon are more discernible and include pupillary changes, irregular respiratory and cardiac patterns, facial flush or a rash, and piloerection. Chest and abdominal pain have also been recorded as seizure activity.[13,49]

KG is a 19 year-old young woman who has had seizures since age nine. Clinically KG's seizures are characterized by nausea, and a sensation of being "squeezed" all over. On occasion, they have been so intense she was observed to hold her abdomen and collapse to the floor. During these episodes, she remains aware of her environment but is unable to respond.

Ictal erotic sensations may or may not be accompanied by genital sensations or signs of sexual arousal. Remillard et al conducted a study which localized the epileptogenic region to the general area of the temporal lobe. His work demonstrated this particular seizure was reported by a preponderance of women.[43]

Case Study

A 32 year-old married, childless physician developed a strange sensation rising from the stomach to the throat at 28 years of age, sometimes accompanied by a feeling of deja vu. These were followed by a pleasant sensation of anal and vaginal constriction approaching sexual orgasm. She automatically adducted her legs and then became "hot and bothered;" her face flushed. These attacks, which lasted for a few minutes, left her in a condition of complete sexual satisfaction so that her "sexual needs were fulfilled for several days." At other times, she was sexually active and had frequent intercourse. Most of her seizures occurred during the premenstrual period.[43]

Altered Cognitive States

Hughling Jackson in 1898 reported seizures arising from the temporal lobe which produced a "dreamy state" consisting of a vivid sense of having previously lived through the same situation.[25] It is now known that these experiential phenomena have a cognitive as well as a subjective component to the event. A feeling of familiarity for a visual event/scene is referred to as deja vu. A sense of an event already experienced is known as deja vecu. These feelings of having previously experienced the event/vision often leads to a sense of clairvoyance. Jamais vu is a feeling of unfamiliarity for visual sensations or events that are cognitively acknowledged as familiar (de, spouse is unfamiliar during a seizure). Jackson postulated that the `experienced' phenomenon and the cognitive reconciliation of the experience occurs within a mental state that was a `doubling' of the consciousness: a depressed personal subjective consciousness plus a simultaneous objective consciousness of the external environment. His study indicated an origin of discharge within the medial aspect of the temporal lobe. By electrical stimulation of the lateral temporal cortex, Penfield was able to evoke these experiential hallucinations.[38,39,40] Efron alternately suggested that the language dominant hemisphere is responsible for time analysis, and deja vu and jamais vu represent a time warp within the time labeling mechanism.[15] Gloor emphasized the temporal neocortex connections with the limbic structures as a means of linking perception (visual/auditory material) with the memory for this experience.[19,20] Bancaud supports the network theory postulating that declarative memory of the temporal neocortex encodes the event and the hippocampus forms a temporary memory trace.[5,22,23] With invasive monitoring, Weinand et al indicated a 75% localization of this phenomenon to the mesiotemporal lobe of the hemisphere non-dominant for language.[50]

Case Study

MT is a 34 year-old woman with convulsive seizures admitted for possible surgical management of her epilepsy. Prior to the intracarotid sodium amytal test, she expressed a concern regarding her "special powers" after surgery. MT stated she was able to "know about things before they happened." Thoughts would just "pop into her head" and they would happen. Some of the events made her feel frightened because she could not stop something from happening even though she "knew" about them beforehand. Examples of the more benign instances include the names of attendees at a party, and the personal data of her veterinarian.

Emotional Alterations

Naturally occurring emotions involve four related responses:[49]

* the subjective experience

* the visceral component

* the cognitive result

* the total organ response

Based on EEG recording, Ahern and Schwartz have suggested two processes for emotional mediation. These researchers found:[1]

* a mediation of emotion perception regardless of the affective color by the posterior right parietal zone

* a differential hemispheric lateralization/specialization for emotional expression by the frontal zones

The electrophysiologic work by Ahern also indicates greater involvement of the left hemisphere in expression of positive emotion and more involvement of the right hemisphere in the expression of negative emotions.[1,2] Studies by Gloor and Cendes implicate the role of the amygdala in the dysfunctional states of emotion and memory.[6,21]

As ictal phenomena, emotions are commonly negative in content and occur suddenly and without any obvious antecedent. Emotional behaviors which are observed and reported as seizures include embarrassment,[12] sudden crying, (dacrystic seizures)[19,29,30] and explosive laughter (gelastic seizures).[51] These behaviors occur without the associated emotional feelings such as sadness or happiness. However, fear is the most common emotion experienced as a seizure.[49] Fear will vary in its duration and intensity as in normal experience. Williams delineates this fear as a difference between fear of the immediate event and the seizure event which is experienced toward an unknown event at a longer period of time. He explains ictal fear as a thought secondary to the emotion, rather than the normal emotion of fear which is a response to an evoked thought. As with other body sensations, the emotion of fear, as an ictal event, occurs out of context and results in an affective experience without previous cognition. Because of this lack of cognitive origin, the fear emotion, which occurs during a state of clouded consciousness, resembles the fear of the unknown or supernatural and is often reported as a feeling of impending doom.

Case Study

A 7 year-old boy experienced very frequent

attacks of pure fear. When in bed (in the

hospital) he would be seen to suddenly show

fear in his expression, and would rapidly

burrow under the bed-clothes, to emerge in a

few seconds, flushed and sweating, saying he

had had terrible fear. If this boy were on the

ward, he would impulsively rush to the nearest

nurse or adult clasp them around the legs and

bury his face in them to emerge in a few

moments, flushed and with the same

explanation.[49]

Macrae, Penfield and Jasper documented with cortical stimulation that the emotion of fear is represented in the anterior, upper and inferior aspects of the temporal cortex.[31,37] Because of this association, ictal fear is often accompanied by its appropriate autonomic and visceral activity such as a hollow feeling, palpitations and sensations rising to the throat.[49] Williams concludes emotional seizures may occur as an isolated phenomenon of the ictus, or may be accompanied by hallucinations of the special senses and any number of sensory or motor disturbances.

Case Study

A 45 year-old woman had had brief stereotypical attacks for sixteen years without cause. She suddenly feels "terribly frightened and horrible all over." This fear is intense and unnatural and with it she always has the thought "Now I'll know what I am frightened about," but never does. She says she goes stone cold, sweats profusely, has visceral activity- "my inside feels like a washing machine," and her body feels light. She is seen to go very pale. There is no loss of consciousness and the whole attack, which begins and ends abruptly, is over in a few seconds.[49]

Ecstatic seizures, although rare, are thought to have been experienced by all the historical figures which have been mentioned in this article. Dostoevsky writes of the ecstatic aura: "I do not know whether this bliss lasts seconds, hours, or minutes", "...yet, take my word, I would not exchange it for all the joys which life can give." (p.661).[48] Cirignotta, Todesco and Lugaresi in a case study were able to provide an EEG recording of this rare seizure characterized by "20- to 30 seconds of intense elation and pervading bliss accompanied by a feeling that the secrets of the universe were to be revealed." (p.710).[7]

Studies have reported that as much as 70-80% of seizure activity presents with temporal lobe phenomena and localization.[26] Review of these statistics begs the following questions be answered before a possible explanation of the data can be tentatively offered: What are the characteristics of the temporal lobes which contribute to these disproportionate statistics? Why are not other areas of the cortex such as the frontal or occipital regions, more frequently found to be the epileptogenic focus? Can these data be completely explained by the association of the temporal regions and head trauma? By the repeated presence of mesial sclerosis? Is this propensity for seizures related to it the cytoarchitecture of the area? Or does the low seizure threshold of temporal lobe structures as well as their connections with sensory, motor and limbic systems, help explain the ubiquitous contribution of this region to seizure activity? Does an understanding of these temporal lobe connections also elucidate the variety of affective and cognitive disturbances associated with seizures?[41] A brief review of the anatomy of the temporolimbic structures will be presented to provide a reference for the development and localization of the epileptogenic activity and help answer some of these questions.

Anatomy of the Temporal Lobe

The temporal lobe consists of the neocortical lateral region, the inferomesial portion limbic portion and a complex system of projections to adjoining regions of the cortex. The lateral surface of the temporal lobe is divided into four regions which help define its borders: the superior temporal gyrus, the middle temporal gyrus, the inferior temporal gyrus and the transverse temporal gyrus. Primary sensory and association areas are part of the lateral temporal lobe. Interpretive areas are found at the supramarginal and angular gyri near the junction of the temporal and parietal lobes.

The limbic system is physically contiguous with the temporal lobes. Structures of the limbic system include all cortical and subcortical structures that form the border of the lateral ventricles: the hippocampal formation, the dentate gyrus, the pyriform cortex of the anterior hippocampal gyrus and the cingulate gyrus. These structures are interconnected by the isthmus of the cingulate gyrus (Fig 1). Ammon's horn, a part of the hippocampus, has been found to be the most epileptogenic part of the brain.[14]

The amygdala is found in the rostral portion of the mesial temporal lobe. Projections from this system create an internal circuitry for the modulation of its many efferent and afferent functions. Afferent fibers carry impulses from diverse sensory cortical areas, the thalamus and the brain-stem, to the pyriform lobe, the dentate gyrus and posterior hippocampus. The fornix, a band of white fibers, forms the main efferent system of the hippocampal formation. Approximately half the fibers descend toward the anterior commissure; the rest branch to the thalamus, the mamillary bodies, the midbrain tegmentum and the reticular formation.[14]

Functional Organization of the Cortex

Localized function of the cortex was first demonstrated by Pierre Paul Broca in 1861. Hughling Jackson and Carl Wernicke furthered this endeavor with their investigations of epilepsy and aphasia respectively. Karl Kleist, a student of Wernicke's, developed a functional map of the cerebral cortex (Fig 2) based on differentiation of neuronal structure (cytoarchitecture) and myelin characteristics (myeloarchitecture). In the past 50 years, work of this type has been expanded with the introduction of electronic microscopy, histochemistry and microelectrodes. These technological developments have allowed physiologists to map many functional areas of the cerebral cortex. Today, 50-100 separate cytoarchitectonic areas can be differentiated. Although this organization can be invoked to explain certain isolated functions, it does not adequately reflect the integrative processes that serve to link these relatively isolated functional zones.

More recent investigations of cortical function have focused on patterns of cortical associations subserving such as functions as language and memory, which result from the interaction of more than one region. This approach, first proposed by Broca in 1878 has found recent embodiment in the model proposed by Mesulam who described five subtypes of cortex and their connections which help explain the interactivity of neural connections and their behavioral correlates.[35]

Early theories postulated that complex behavior was produced by serial processing of information along a hierarchy of dedicated centers. Current concepts however, indicate that complex functions such as cognition and behavior are better explained by a theory of interconnective networks rather than isolated, unique functions. These networks (not to be considered identical to specific white matter tracts) are presumed to serve not only local areas defined by cytoarchitectonic fields but also widely separated areas of interconnected local networks.

McClelland et al first presented the notion of parallel distributed processing, which suggests that brain-behavior is accomplished by simultaneous integration of many items of information and constraints.[33] This theory of parallel distributed processing or large-scale neurocognitive networks, was further developed by Mesulam to explain such functions as directed attention, language and memory. According to his work, the "absence of a one-to-one correspondence among anatomical sites, neural computations and complex behavior" is a core attribute of the neural network concept. (p.599).[34] Such linked systems support the associative and integrative functions of the cortex and can be applied to the complex behavioral components of seizure activity.[42]

Awareness and remembrance of the ictal behaviors which have been experienced are of diagnostic value of the seizure event. Reported to the clinician as cognitive data, memories are in part an integration of multisensory information reflecting past experiences. Although long-term memory traces are thought to be distributed throughout the cortex, structures in the temporal lobe (especially the hippocampus) appear to be critical to the establishment of new memories and perhaps, the retrieval of old ones. An appreciation for the possibility of such local and dispersed networks as it relates to the reporting of psychologic alterations due to seizure activity is an important aspect of this discussion.

Nursing Implications

Although medical diagnosis of such subtle seizure activity is now technologically feasible, the history and description of the seizure itself remains an integral component of diagnosis, classification, medical treatment and localization for surgical intervention. Many of the questions during a medical history interview are directed and closed rather than open-ended. Frequently, the history of the seizure activity must be provided by an individual other than the patient who may have lost recollection for part of the incident. An assessment is not complete unless the nurse specifically addresses the issue of psychological experiences. Any admission history or post-ictal assessment should query the patient regarding such events as altered sensation and emotions. Use of the Silberman-Post Psychosensory Rating Scale can provide guidelines for this assessment. Information gleaned from a sensitive review of psychologic symptoms will provide further localization data.[44] It will also validate for the patient the extent of the seizure activity into the psychological realm rather than just the observable physical behaviors allaying the fear of being "crazy."

A working knowledge of cerebral anatomy and basic physiology is necessary for a thorough seizure assessment and appropriate epilepsy education. The nurse must have the ability to distill these complex concepts to a level appropriate to the educational level and queries of the patient and family. An idea of gross function and connective pathways will help the patient understand the development of a seizure and the variety of symptoms that can be experienced as part of a stereotypic pattern. An appreciation of the anatomic correlates of the behavioral symptomology will also help guide the historical interview, assist with lesion localization and provide a basis for patient education.

Summary

A discharge in the neural network can reproduce any sensation, memory, thought, or emotion that the brain is capable of transmitting. Appreciating the potential for psychological phenomena as a component of seizure activity can guide the post-seizure assessment by the nurse. Validation of the subjective event provides support for the patient and contributes to the historical data necessary for seizure classification and localization.

[Figures 1-2 ILLUSTRATION OMITTED]

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Questions or comments about this article may be directed to: Julie N. Tackenberg, RN, MA, MAOM, CNRN, clinical nurse specialist, University Medical Center, PO Box 245183, Tucson, Arizona 85724-5183. She is case manager of the Arizona Comprehensive Epilepsy Program.

Geoffrey Ahern, MD, PhD, is director at the Behavioral Neurology Unit, University of Arizona Health Science Center
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Author:Tackenberg, Julie N.; Abern, Geoffrey
Publication:Journal of Neuroscience Nursing
Date:Apr 1, 1996
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