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Experiential phenomena of temporal lobe epilepsy. Facts and hypotheses.

Experiential phenomena that occur in temporal lobe seizures and can be reproduced by electrical stimulation of temporal lobe structures typically encompass perceptual, mnemonic and affective features, either in combination or in isolation, which commonly relate to the patient's individual past experience. These phenomena raise interesting questions concerning brain mechanisms involved in human psychophysiology. The anatomical substrates for the evocation of these phenomena are widely distributed within the temporal lobe and include temporal isocortex and limbic structures (amygdala, hippocampus and parahippocampal gyrus). Arguments are presented which indicate that experiential phenomena are positive expressions of temporal lobe and limbic function and do not result from its ictal paralysis. Recent concepts of parallel distributed processing (Rumelhart and McClelland, 1986) and the importance of parallel distributed cortical networks for higher cognitive functions (Goldman-Rakic, 1988a, b) provide a theoretical framework on which a hypothesis explaining experiential phenomena can be based. In conformity with these concepts the hypothesis assumes that temporal lobe epileptic discharge or electrical stimulation of temporal lobe structures can induce the elaboration of patterns of excitation and inhibition in widely distributed neuronal networks, some of which are capable of forming a specific matrix representing the substrate of a given experience. Neuronal networks engaged in parallel distributed processing (1) have the capacity to recreate the totality of a given experience when only a fragment of the network is activated, and (2) they tolerate a great deal of degradation by random inactivation of its components or by interference through random noise without serious loss of information content. These features are compatible with the assumption that localized epileptic neuronal discharge or electrical stimulation involving some temporal lobe structures could create a matrix representing features of individual experience of the kind activated in the course of temporal lobe seizures. Such an experience could, up to a certain limit, resist the degrading influence of mounting noise which inevitably must attend seizure discharge.

Brain↗

Image guided audit of surgery for temporal lobe epilepsy.

Studies on surgery for temporal lobe epilepsy are hampered by lack of information about the actual surgery that has taken place. A method is described for accurately measuring the volumes of resection by MRI after surgery. Ten cases of surgically treated temporal lobe epilepsy (nine non-tailored resections, one selective amygdalohippocampectomy) are presented to show the technique. Indices of extent of resection in both the mesiobasal and lateral temporal lobe compartments have been measured, compared, and evaluated. By comparison with identical preoperative volumetric MRI the hippocampal resections have been correlated with the demonstrated hippocampal volume loss, thought to be of relevance in the aetiology of temporal lobe epilepsy. Detailed postoperative audit in this manner is vital in providing a rational basis for follow up studies of outcome.

Adolescent↗

Multiple personality and related dissociative phenomena in patients with temporal lobe epilepsy.

Many patients with temporal lobe epilepsy also experience dissociative episodes. Three patients with multiple personality exhibited alterations in speech pattern, personality, handedness, and sense of personal identity and claimed amnesia for the dissociative episodes. Another 10 patients identified alternative personalities or demons as motivators of ego-alien behavior. Of clinic patients with temporal lobe epilepsy, 33% exhibited some dissociative phenomena, which had no apparent association with individual seizures but always followed the development of the seizure disorder. The authors propose that intensified, dystonic affects, characteristic of the interictal period in temporal lobe epilepsy, may predispose some individuals to dissociative reactions.

Adult↗

Inter-ictal and post-ictal psychoses in frontal lobe epilepsy: a retrospective comparison with psychoses in temporal lobe epilepsy.

There have been few studies of the psychopathology of patients with frontal lobe epilepsy (FLE). The majority of studies of both inter-ictal and post-ictal psychoses have strongly suggested the influence of temporal lobe disturbance on psychoses. Patients with organic brain damage or schizophrenia, however, sometimes show frontal lobe dysfunction. The purpose of this study was to better understand the effect, if any, of frontal lobe disturbance and seizure on psychopathology. Patients were divided into four groups based on epilepsy type and preceding seizures; 8 with FLE/inter-ictal psychosis, 3 with FLE/post-ictal psychosis, 29 with temporal lobe epilepsy (TLE)/inter-ictal psychosis, and 8 with TLE/post-ictal psychosis. Psychopathologic symptoms were retrospectively reviewed based on case notes, using a modified brief psychiatric rating scale (BPRS). Psychomotor excitement, hostility, suspiciousness, and hallucinatory behaviour were prominent features in all four groups. Six orthogonal factors were derived by factor analysis from the original data based on the 18 BPRS items. FLE patients with inter-ictal psychosis showed marked hebephrenic characteristics (i.e. emotional withdrawal and blunted effect). Our findings suggest that patients with FLE can exhibit various psychiatric symptoms. However, their psychotic symptoms, hebephrenic symptoms in particular, may often be overlooked.

Adult↗

Processing of rapid auditory information in epileptic patients with left temporal lobe damage.

The role of the temporal lobes in processing time-related (temporal) information was tested in a task of anisochrony (or irregularity) discrimination assessing the temporal processing of sequential auditory information according to different presentation rates or tempos (between 80 and 1000 ms inter-onset intervals, IOI). Epileptic patients with either left (LHA, n=8) or right (RHA, n=10) hippocampal atrophy participated in this study as well as six normal control subjects (NC). For all the subjects, an effect of tempo was obtained, thresholds deteriorating for the 80 ms IOI as compared to longer IOI (the latter conforming to Weber's law). Furthermore, there was a specific impairment of rapid anisochrony discrimination (80 ms IOI) for patients with LHA as compared to patients with a RHA and NC, whereas no significant deficit was observed in these patients for longer IOI. These findings are in agreement with studies carried out in patients with left-hemisphere damage associated with massive language disorders and suggest the specialisation of left medial temporal lobe structures in processing rapid sequential auditory information. However, these results might also be explained by an auditory memory deficit in the presence of left temporal lobe dysfunction, as opposed to a specific impairment of fast sequential temporal processing.

Adolescent↗

Jobst et al's "Detection in life of confirmed Alzheimer's disease using a simple measurement of medial temporal lobe atrophy by computed tomography".

"The medial temporal lobe of the brain is important for normal cognitive function, notably for memory, and is the region with the most extensive pathological change in Alzheimer's disease (AD). We wanted to find out if atrophy of the medial temporal lobe could be detected in life in patients in whom a diagnosis of AD was subsequently established histopathologically. The minimum width of the medial temporal lobe, measured by temporal-lobe-oriented computed tomography (CT) about one year before death, in 44 patients with a histopathological diagnosis of AD (cases) was nearly half (0.56 of the median) that in 75 controls of the same age with no clinical evidence of dementia (95% confidence interval 0.51-0.61). There was little overlap between the distributions of measurements in cases and controls. A cut-off (< 0.79 MoM) selected to yield a 5% false-positive rate gave an expected detection rate of 92%. A cut-off selected to yield a false-positive rate of 1% (< 0.70 MoM) yielded a 79% detection rate. 20 of the 44 patients with histopathologically diagnosed AD had been scanned more than once before death, and the test (cut-off < 0.79 MoM) was positive in all 20 more than a year before and in 9/10 more than 2 years before death. In 10 subjects with dementia but with histopathology excluding AD, the mean minimum width of the medial temporal lobe was significantly greater than that in the cases with AD, but was not significantly different from that in controls.(ABSTRACT TRUNCATED AT 250 WORDS)

Aged↗

Affective verbal memory in patients with temporal lobe epilepsy.

Eighteen epileptic patients with unilateral temporal lobe epilepsy (9 left, 9 right) were evaluated with a verbal memory task involving recall of 2 stories, 1 with affective content and 1 that was neutral. A trend for better performance by the group with intact left hemispheres was found for a quantitative score of number of story units recalled. For a qualitative score of number of symbolic distortions, a main effect of affective load was found, such that more distortions were made for the story with affective than neutral content. This effect remained significant when the left temporal lobe epilepsy patients were analyzed separately and was not found for the right temporal lobe epilepsy patients alone. Additional analyses for the subset of 5 patients with left and 6 patients with right temporal lobectomies involving removal of the hippocampus and amygdala were in the same direction as the analyses for all 18 participants. These findings are consistent with other reports of material-specific memory deficits, such that verbal memory deficits are associated with left temporal lobe epilepsy. The differences between performance on the affective and neutral stories for the left and right temporal lobe epilepsy patients are discussed and related to the role of the amygdala in affective processing.

Adult↗

Neuronal firing patterns during the spread of an occipital lobe seizure to the temporal lobes in man.

Neuronal recordings from occipital cortex and hippocampus during a seizure originating in the occipital lobe of a patient with an occipito-temporal tumor demonstrated that the visual aura resulted from neuronal activation of medial peristriate and possibly other occipital lobe neurons while the psychomotor automatisms followed 10-20 sec later and were caused by recruitment of hippocampal neurons bilaterally. This confirmed that the complex seizure symptoms were caused by propagation from an occipital lobe focus. The psychomotor symptoms have not recurred for the 6 months since interruption of occipito-temporal connections; however, the spared medial occipital neurons still produce visual auras.

Astrocytoma↗

Febrile convulsions. Is seizure duration the most important predictor of temporal lobe epilepsy?

The association between febrile convulsions and temporal lobe epilepsy is recognized, but is controversial. We attempted to clarify this and to determine which attributes of febrile convulsions were associated with temporal lobe epilepsy. During a study of genetic linkage in febrile convulsions, families with at least four affected members were identified. Clinical features of febrile seizures and EEG findings were compared in those who did and did not develop later afebrile seizures. In six selected families, 59 family members had febrile convulsions. Temporal lobe epilepsy developed in eight of these, whereas only one of 213 family members with no febrile convulsions had temporal lobe epilepsy (P < 0.0001). The mean durations of febrile convulsions in those with and without progression to temporal lobe epilepsy were 100 and 9 min, respectively (P = 0.02). Five patients had temporal lobectomies, which revealed mesial temporal sclerosis in all cases. Four patients who developed other types of epilepsy had a mean duration of febrile convulsions of 90 min. The total number, the maximum number in any one day, and the age at onset of febrile convulsions did not differ significantly between groups. Only two patients had neurological deficits, both of whom subsequently had nonlocalizable partial epilepsy. In these families, selected to reduce genetic and phenotypic heterogeneity, a strong association was evident between febrile convulsions and temporal lobe epilepsy with mesial temporal sclerosis. A prolonged febrile convulsion was the most important determinant of this association.

Adult↗

Unilateral mesial temporal atrophy after a systemic insult as a possible etiology of refractory temporal lobe epilepsy. Case report.

Mesial temporal sclerosis is the main pathological substrate present in refractory temporal lobe epilepsy and its presence is often related to the occurrence of febrile seizures in infancy. There is an on-going discussion on the nature of mesial temporal sclerosis as it related to epilepsy: cause or consequence. A previously normal child developed hyperosmolar coma after abdominal surgery at the age of 6. Three months afterwards he developed simple and complex partial seizures with an increasing frequency and refractory to multiple mono- and polytherapic drug regimens. He was evaluated for surgery at the age of 13. Ictal and interictal recordings showed left temporal lobe abnormalities. Early CT scanning suggested left temporal atrophy. MRI showed mesial temporal sclerosis. Neuropsychological testing showed verbal memory deficits and he passed a left carotid artery amytal injection. He was submitted to a cortico-amygdalo-hippocampectomy and has been seizure-free since then. The clinical data obtained from this patient suggest that at least in this case mesial temporal sclerosis would be related to the cause of epilepsy and not resultant from repeated seizure activity.

Adolescent↗

Electroencephalographic recording from the temporal lobes: a comparison of ear, anterior temporal, and nasopharyngeal electrodes.

A prospective study was performed to evaluate the usefulness of ear, anterior temporal, and nasopharyngeal electrodes for recognizing temporal lobe epileptic electroencephalographic (EEG) foci. One hundred and three EEGs were performed on patients suspected of having epilepsy who had a previous normal record. Nasopharyngeal electrodes were simultaneously compared with ear and anterior temporal electrodes to determine their relative abilities to detect pathological epileptiform transients from the temporal region. Epileptic discharges were detected in 22% of the recordings. Pathological discharges seen in nasopharyngeal electrode derivations invariably were seen in ear and anterior temporal electrode derivations using carefully designed montages, and EEG diagnosis was not altered by use of nasopharyngeal electrodes. We conclude that EEG recording with ear and anterior temporal electrodes is sufficient to detect pathological temporal epileptiform transients, and that the use of nasopharyngeal electrodes as a routine procedure offers no added benefit.

Adolescent↗

Gender differences in temporal lobe structures of patients with schizophrenia: a volumetric MRI study.

OBJECTIVE: The temporal lobe and associated structures have been previously implicated in the neuroanatomy of schizophrenia. This study was designed to assess the potential influence of gender on the morphology of temporal lobe structures, including the superior temporal gyrus and the amygdala/hippocampal complex, in patients with schizophrenia and to examine whether schizophrenic patients differ morphologically in these structures from comparison subjects. METHOD: Magnetic resonance imaging was used to measure the volume of temporal lobe structures, including the superior temporal gyrus, the amygdala/hippocampal complex, and the temporal lobe (excluding the volumes of the superior temporal gyrus and amygdala/hippocampal complex), and two comparison areas--the prefrontal cortex and caudate--in 36 male and 23 female patients with schizophrenia and 19 male and 18 female comparison subjects. RESULTS: There was a significant main effect of diagnosis in the superior temporal gyrus and the amygdala/hippocampal complex, with smaller volumes in patients than in comparison subjects. There was a significant gender-by-diagnosis-by-hemisphere interaction for temporal lobe volume. Temporal lobe volume on the left was significantly smaller in male patients than in male comparison subjects. Female patients and female comparison subjects demonstrated no significant difference in temporal lobe volume. There were no statistically significant gender interactions for the superior temporal gyrus, the amygdala/hippocampal complex, or the comparison regions. CONCLUSIONS: These findings suggest that there may be a unique interaction between gender and the pathophysiologic processes that lead to altered temporal lobe volume in patients with schizophrenia.

Adult↗

Potentially misleading extratemporal lobe lesions in patients with temporal lobe epilepsy.

From a series of 217 consecutive temporal resections for intractable epilepsy between 1993 and 2000, we identified all patients with large non-neoplastic extratemporal lesions. Only patients with known postsurgical outcomes with follow up for more than two years were included. Fifteen patients were identified. All patients had a history of medically refractory epilepsy with clinical and ictal evidence of mesial temporal seizure onset. Eleven patients had extratemporal lesions ipsilateral to the seizure focus, whereas four patients had the lesions contralateral to the seizure focus. Nine of the 15 patients had evidence of hippocampal atrophy on magnetic resonance imaging (MRI). Following temporal resection, nine of these patients (60%) became seizure free (Engel class 1A), two patients were free of disabling seizures only (Engel class 1B), and two patients had a few early seizures but then became seizure free for at least two years (Engel class 1C). Two patients had significant improvement (Engel class 2). Thus, the finding of large extratemporal lesions on MRI was potentially misleading. When clinical semiology and ictal EEG recordings provide evidence of temporal onset seizures, anterior temporal resection should be considered in patients with extratemporal lesions.

Adult↗

Short-term cognitive changes after unilateral temporal lobectomy or unilateral amygdalo-hippocampectomy for the relief of temporal lobe epilepsy.

Forty two patients who had unilateral temporal lobe surgery (either temporal lobectomy or amygdalo-hippocampectomy) were evaluated using a selection of cognitive tests before and soon after surgery, to examine whether the amygdalo-hippocampectomy produces less cognitive impairment than the standard en bloc resection. On specific indices of cognitive functioning an amygdalo-hippocampectomy rather than a temporal lobectomy, undertaken on the temporal lobe thought to mediate that particular function, produced less impairment, in terms of change in cognitive function resulting from the operation. An amygdalo-hippocampectomy carried out on the temporal lobe not thought to mediate such skills, however, resulted in less improvement or more deterioration in these functions than a temporal lobectomy, except in the case of delayed prose recall, where a right amygdalo-hippocampectomy led to more improvement than a right temporal lobectomy. Overall there were few scores which distinguished between the different surgical procedures for cognitive outcome.

Adult↗

The effect of right temporal lobe lesions on matching of smells.

Thirty patients with bitemporal lobe epilepsy, 14 patients with right temporal lobe epilepsy, 14 patients with left temporal lobe epilepsy, 14 patients who had right temporal lobectomy, 10 patients who had left temporal lobectomy and 12 patients who had lobectomy involving frontal or fronto-parietal regions were tested for their ability to match smells. A simple matching technique was used. It was found that patients with right temporal lobe lesions had difficulty in matching smells. There was no significant difference between the right temporal lobe epilepsy group and the right temporal lobectomy group. The implications of these findings are discussed.

Discrimination Learning↗

High-resolution fMRI investigation of the medial temporal lobe.

The medial temporal lobe (MTL) is critical for declarative memory formation. Several theories of MTL function propose functional distinctions between the different structures of the MTL, namely the hippocampus and the surrounding cortical areas. Furthermore, computational models and electrophysiological studies in animals suggest distinctions between the subregions of the hippocampus itself. Standard fMRI resolution is not sufficiently fine to resolve activity on the scale of hippocampal subregions. Several approaches to scanning the MTL at high resolutions have been made, however there are limitations to these approaches, namely difficulty in conducting group-level analyses. We demonstrate here techniques for scanning the MTL at high resolution and analyzing the high-resolution fMRI data at the group level. To address the issue of cross-participant alignment, we employ the ROI-LDDMM alignment technique, which is demonstrated to result in smaller alignment errors when compared with several other common normalization techniques. Finally, we demonstrate that the pattern of activation obtained in the high-resolution functional data is similar to that obtained at lower resolution, although the spatial extent is smaller and the percent signal change is greater. This difference in the pattern of activation may be due to less partial volume sampling in the high-resolution data, resulting in more accentuated regions of activation.

Adult↗

Age-related changes in brain: I. Magnetic resonance imaging measures of temporal lobe volumes in normal subjects.

The volume of temporal lobe structures was examined in twenty-seven older (mean age of 69.2 +/- 8.3 years) and ten younger subjects (mean age of 26.1 +/- 4.1 years) using quantitative magnetic resonance imaging (MRI) methods. Multiple regression analysis, using gender, overall atrophy, and head size as covariates, showed unique contributions of age to variance in both medial and lateral temporal lobe volumes. Temporal lobe subregions that showed the strongest unique age-related reductions were the hippocampus, fusiform gyrus, and parahippocampus. These results suggest age-related reductions in temporal lobe subvolumes.

Adult↗

Seizure outcome after temporal lobectomy in temporal lobe cortical dysplasia.

PURPOSE: To identify the temporal lobe cortical dysplasia (CD) histopathology classification subtype and determine the seizure outcome of patients who underwent temporal lobectomy with coincident CD. METHODS: We reviewed the data of 28 patients with temporal lobe epilepsy who underwent surgery with pathologically verified CD at our institution from 1990 to 2000. The seizure outcome was assessed at a minimum of 1 year after surgery according to Engel's classification. RESULTS: Of 28 patients who underwent surgery, nine (32.1%) had isolated CD, and 19 (67.9%) had CD and hippocampal sclerosis (CD&HS). Twenty-six (92.9%) patients had histopathology subtype Ia (architectural abnormalities). Twenty (71.4%) patients were seizure free (Engel class I). Favorable seizure outcome (Engel class I, II) was achieved in 26 (92.9%) patients. No difference in seizure outcome was noted between patients with CD and CD&HS. CONCLUSIONS: The most common histopathologic subtype in patients with temporal lobe CD is type Ia (architectural abnormalities). Temporal lobectomy in temporal lobe epilepsy patients with CD can achieve favorable seizure outcome.

Adolescent↗