Verbal learning and forgetting in patients with temporal lobe epilepsy

Studies comparing non-surgical patients with left or right temporal lobe epilepsy (TLE) have shown irregular differences in verbal learning and memory. We assessed the performance of unoperated patients with epileptogenic temporal lobe lesions or cryptogenic TLE using a selective reminding procedure for the learning of a word list, and five delayed trials for the recall of learned words. On the selective reminding procedure, patients with left TLE were found to be more impaired than those with right TLE and controls, in agreement with the role of the left temporal lobe in verbal learning. The patients with right TLE were more impaired than the controls, possibly due to the semantic organization of the word list The rate of forgetting learned words was similar in the patient and control groups, suggesting that patients with left TLE can normally retain and/or retrieve stored items. These data support the hypothesis that distinct functional systems subserve learning and memory. Comparisons of the patient subgroups with epileptogenic lesions (hippocampal sclerosis or low-grade glioma) and those with cryptogenic TLE did not reveal any significant difference in learning or in memory, suggesting that epileptiform activity could affect verbal performance as a detectable temporal lesion.     

Drawing from memory in focal epilepsy: a cognitive and neural perspective

This study provides evidence of non-verbal cognitive functioning in temporal (TLE) and frontal lobe epilepsy (FLE) patients by exploring the mechanisms and neural correlates of drawing abilities. Sixty-six patients with left (n=32) or right TLE (n=34), 30 patients with left (n=18) or right FLE (n=12), and 30 healthy subjects were compared. The Drawing from Memory (DfM) test required participants to design 16 living or non-living items; the total score was the sum of all scores blindly provided by three judges who had to identify the drawings. The verbal and visual Pyramid and Palm Trees Test (PPTT), Raven Colored Progressive Matrices (Raven CPM), Cube Analysis, Token Test, Word Fluency, Card Classification, and Rey Complex Figure Test Copy trial (Rey CFC) assessed different verbal and non-verbal functions. Non-parametric statistics indicated that, with respect to controls, both TLE groups and the left FLE patients had significantly lower DfM scores. In the TLE group, hierarchical regression analyses revealed that the DfM score was predicted by the Raven CPM and PPTT scores, while, in the FLE group, it was predicted by the Rey CFC. Thus, drawing abilities may be impaired by TLE or FLE owing to different mechanisms that involve semantic or executive abilities. Implying cooperation between temporal and frontal areas that support these functions, DfM may be a sensitive index of integrity of cortical areas or neural pathways damaged by focal epilepsy.     

Verbal semantic memory in temporal lobe epilepsy

OBJECTIVES: Temporal lobe epilepsy (TLE) may determine memory difficulties not explained by episodic memory impairment. The present study was aimed to verify the presence of specific semantic memory dysfunctions in TLE and to explore their relations to epilepsy variables. SUBJECTS AND METHODS: Forty-seven patients with lateralized temporal (n = 26) or extra-temporal lobe epilepsy (n = 21) and 23 healthy subjects were compared. Picture Naming and Pointing to a Picture were used to explore expressive and receptive vocabulary and the Semantic Questionnaire evaluated semantic judgment of verbally presented items. The Selective Reminding Procedure for word list learning and Story Recall were used to assess episodic memory. Spontaneous speech and the Token Test controlled for language disturbances, and Raven's Coloured Progressive Matrices were used to evaluate abstract reasoning ability. RESULTS: Multivariate analysis of variance of test scores showed significant impairment of semantic memory in patients with left TLE compared to healthy controls, whereas episodic memory was impaired in left temporal and extra-temporal epilepsy (as measured by word learning) and all epilepsy groups (as measured by Story Recall). In the TLE groups, naming abilities were more compromised than single-word comprehension and semantic judgment - which were not significantly affected. No deficits in language abilities or in abstract reasoning were found in any patient group. Factor analysis of memory tests scores in the patients produced two factors, one semantic and the other episodic. Regression analysis revealed that the semantic factor was related to abstract reasoning, left hemisphere lateralization of seizures, and age of seizure onset; while the episodic factor was related to age. CONCLUSIONS: Left TLE may determine significant verbal semantic memory compromise, maybe due to impaired access to the semantic-lexical storage. In non-aphasic epilepsy patients, comparison of performance on semantic and episodic memory tests may be useful for assessing the nature of memory failures, and may complement clinical and neurophysiological means for defining the epileptic center.     

Semantic memory in partial epilepsy: verbal and non-verbal deficits and neuroanatomical relationships

Semantic memory was evaluated in 124 epilepsy patients, including 84 with left (n=44) or right temporal lobe epilepsy (TLE) (n=40) and 40 with left (n=25) or right frontal lobe epilepsy (FLE) (n=15), in order to determine their verbal and visual deficits, and the neuroanatomical relationships between them. The controls were 35 healthy subjects. Semantic memory was assessed by means of Picture Naming, Picture Pointing, the verbal Pyramid and Palm Trees Test (PPTT), the visual PPTT, Object Decision Hard, and Drawing From Memory. Episodic memory was assessed by means of the Short Story, Rey's Complex Figure, the Verbal and Visual Selective Reminding Procedure and Brown-Peterson Procedure. Factor analysis of the epilepsy patients distinguished their semantic memory scores from other neuropsychological domains. The semantic memory factor was significantly related to the side of the epileptic region, with lower scores in the left hemisphere and left TLE patients. In comparison with the controls, the left TLE patients were significantly impaired on Picture Naming, Picture Pointing, and Object Decision Hard. Subsequent analyses showed that, in comparison with the controls and the right TLE patients, the left TLE patients with lateral temporal lobe lesions were impaired in Picture Naming whereas, in comparison with the controls, the left TLE patients with mesial temporal lobe lesions were impaired in Object Decision Hard. On the contrary, the episodic memory factor was not related to the side of the epileptic region, and a few material-specific tests revealed opposite impairments in the left and right hemisphere patients. These results show that left TLE may cause semantic memory deficits involving verbal and visual information. Unlike the material-specific pattern of episodic memory, this pattern of impairment is in line with the view of an amodal semantic store in which all of the information about a thing overlaps. The semantic memory impairment may reflect damage in the lateral and mesial temporal lobe regions that impair neocortical functions in storing and retrieving information or hippocampal functions in processing meaningful stimuli.     

Visual Learning on a Selective Reminding Procedure and Delayed Recall in Patients with Temporal Lobe Epilepsy

Summary: We administered a visual selective reminding procedure for the learning of designs to healthy controls and to left or right temporal lobe epilepsy (TLE) patients without demonstrable brain lesions. In comparison with the other groups, right TLE patients showed a deficit of learning characterized by an impairment in storing visual material and consistently retrieving it from long-term memory. Patients with left TLE performed similarly to controls. These data are consistent with the hypothesis of right hippocampal involvement in the learning of nonverbal material. Delayed retrieval of learned material was similar in all the subject groups tested at long time intervals, suggesting the impairment of learning in patients with right TLE does not necessarily imply a subsequent deficit in the retrieval of stored information. This finding may agree with the opinion that distinct functional systems subserve learning and memory.     

Raven's Coloured Progressive Matrices as a measure of cognitive functioning in Cerebral Palsy

Background Cognitive dysfunction is frequent in Cerebral Palsy (CP). CP motor impairment and associated speech deficits often hinder cognitive assessment, with the result being that not all CP studies consider cognitive dysfunction. Raven's Coloured Progressive Matrices is a simple, rapid test which can be used in persons with severe motor impairment and speech limitations. We studied whether this test can offer a reliable measure of cognitive functioning in CP. Method Visuoperceptual, language, memory and frontal lobe functions were evaluated in 30 participants with severe motor impaired CP and a variety of speech difficulties. The relationship between Raven's Coloured Progressive Matrices and a variety of tests was analysed. Results Raven's Coloured Progressive Matrices performance was associated with visuoperceptual, language, visual and verbal memory but not with frontal functions. Receptive vocabulary and visuospatial measures were the best predictors of Raven's Coloured Progressive Matrices raw scores. Conclusions Raven's Coloured Progressive Matrices is a fast, easy‐to‐administer test able to obtain a measure related with linguistic, visuoperceptual, and memory cognitive functioning in persons with CP despite their motor and speech disorders.     

Response inhibition and set shifting in patients with frontal lobe epilepsy or temporal lobe epilepsy

Patients with frontal lobe epilepsy (FLE), patients with temporal lobe epilepsy (TLE), and matched controls were administered a test of response inhibition and set shifting (switching) (Color Word Interference Test, CWIT). Patients with FLE were impaired relative to the controls across all conditions of the CWIT, with the FLE patients showing disproportionate impairment in the Inhibition and Inhibition/Switching conditions. In contrast, the TLE patients did not differ from controls. Further analysis of the patient groups revealed that patients with left FLE were impaired relative to those with right FLE, left TLE, and right TLE in the Inhibition condition. In the Inhibition/Switching condition, patients with left FLE and left TLE were impaired relative to their right-sided counterparts. Finally, performance by the TLE group in the Inhibition/Switching condition was correlated with seizure frequency. These data suggest that patients with FLE, but not TLE, show impaired inhibition and set shifting relative to controls. In addition, side of the seizure focus and seizure frequency may contribute to executive dysfunction in patients with epilepsy.     

Neuropsychological Outcome in Children after Frontal Lobe Epilepsy Surgery

We investigated the neuropsychological performance of children with frontal lobe epilepsy (FLE, n = 12) before and 1 year after surgery. Children with temporal lobe epilepsy (TLE, n = 12) were included as control group. Preoperatively, children with FLE had a significantly higher IQ than children with TLE, but were significantly more often impaired in manual motor coordination. Postoperatively, both groups improved in attention, short-term and long-term memory, and manual coordination, although the latter was not significant. Neuropsychological outcome in FLE patients was not better in seizure-free patients than in patients with continuing seizures. To avoid deterioration in language functions of patients in whom surgery involved left area 44, correspondence of results in cortical stimulation and intracarotid amytal test may be essential. All in all, our data indicate a favorable cognitive outcome in children 1 year after frontal lobe surgery.     

Double dissociation between temporal and spatial pattern processing in patients with frontal and parietal damage

One hundred and twenty nine patients affected by a cerebral lesion confined to a single lobe, underwent a battery of tests including the "Temporal Rule Induction" (TRI) and the Raven's "Coloured Progressive Matrices" (CPM). Frontal patients scored lower than any other group on TRI and parietal patients on CPM. This contrasting pattern of performance provides strong empirical support to the hypothesis that the frontal lobe is specifically involved in tasks that require a control on temporally ordered information whereas the parietal lobe is concerned with cognitive activities that imply visuo-spatial analysis.     

Memory in paediatric temporal lobe epilepsy: effects of lesion type and side

This study investigated the role of underlying pathology on memory function of children with temporal lobe epilepsy (TLE). Memory was assessed in 44 children with TLE resulting from hippocampal sclerosis (HS) or dysembryoplastic neuroepithelial tumours (DNT), and 22 control children. Delayed story and paired associate recall performance was significantly more impaired in children with HS compared to those with DNT, irrespective of the affected side. Semantic memory was impaired in both HS groups, and also in the left DNT group. These results suggest a role for type, and to a lesser extent, side of pathology in the memory profile of children with TLE.     

A componential analysis of proverb interpretation in patients with frontal lobe epilepsy and temporal lobe epilepsy: relationships with disease-related factors

The ability to interpret nonliteral, metaphoric language was explored in patients with frontal lobe epilepsy (FLE) and temporal lobe epilepsy (TLE), and matched control participants, to determine (1) if patients with FLE were impaired in their interpretations relative to those with TLE and controls, and (2) if disease-related variables (e.g., age of seizure onset) predicted performances in either patient group. A total of 22 patients with FLE, 20 patients with TLE, and 23 controls were administered a test of proverb interpretation to assess their ability to grasp the abstract meaning of nonliteral language. Participants were presented with a series of proverbs and asked to provide an oral interpretation of each. Responses to each proverb were scored according to their accuracy and level of abstractness. Patients with FLE, but not TLE, were impaired relative to controls in their overall interpretation of proverbs. However, a subgroup analysis revealed that only patients with left FLE showed impaired interpretation accuracy relative to the other groups, whereas patients with both left FLE and left TLE showed impaired abstraction. Patients with FLE were also impaired when they were asked to select the best interpretation of the proverb from response alternatives. In patients with FLE, only a left-sided seizure focus was associated with poorer performance. In patients with TLE, both an early age of onset and a left-sided seizure focus predicted poorer performance. Overall, FLE patients exhibit greater impairment than TLE patients in interpreting proverbs. However, the nature and disease-specific correlates of impaired performances in proverb interpretation differ between the groups.     

Impaired gist memory in patients with temporal lobe epilepsy and hippocampal sclerosis

Purpose: Temporal lobe epilepsy (TLE) is the most common focal epilepsy and frequently causes memory problems. It is often associated with hippocampal sclerosis (HS) and is useful in exploring memory functions. We aimed to examine the effect of restricted hippocampal lesions on gist memory function in patients with TLE. Methods: Forty‐five patients with TLE and HS (16 left, 15 right, and 14 bilateral lesions) and 22 control subjects were recruited. Patients with magnetic resonance imaging (MRI) or electroencephalography (EEG) evidence of extratemporal lesions were excluded. All participants performed a gist‐based recognition task following the Deese‐Roediger‐McDermott paradigm and were tested for verbal IQ and memory functions. We conducted hippocampal volumetry on MRI of all the participants. Results: Patients showed multidomain memory impairments. Gist memory was impaired in patients with bilateral HS and probably in patients with right HS. Hippocampal volumetry supported such findings that total volume of hippocampi and volume of right hippocampus correlated positively with gist memory function. Discussion: HS has a dose effect and a probable right dominance effect on gist memory; good item memory supports gist memory performance; and a disproportionate deficit was noted in tasks with high relational demand but not in tasks with simple association. We should develop memory skills for patients with TLE by enhancing performance of gist memory related to simple association task.     

Learning and Memory Impairment in Patients with Temporal Lobe Epilepsy: Relation to the Presence, Type, and Location of Brain Lesion

PURPOSE: To study the influence of epileptogenic lesions on learning and memory alterations in patients with temporal lobe epilepsy (TLE). METHODS: We studied 131 patients (55 with left and 39 with right lesional TLE; 22 with left and 15 with right cryptogenic TLE) and 36 healthy subjects. We compared these groups by using a battery of tests to assess verbal and visual learning, delayed recall, and recall after the imposition of interfering activity. RESULTS: Compared with the controls and patients with right TLE, the patients with left TLE were significantly impaired on all verbal tests. On visual tests, patients with right TLE were impaired compared with controls but not more so than patients with left TLE. Separate multivariate analyses of variance (MA-NOVAs) of patients' verbal and visual test scores, taking the TLE side and morphologic features of the temporal lobes (i.e., normal, hippocampal sclerosis, low-grade glioma, or cavernous angioma) as independent factors, did not show any significant effect of these features. Separate comparisons of verbal and visual test scores of patients with lesional TLE, taking the side and location (mesial or lateral) of the epileptogenic lesion as independent factors, did not show any significant effect of location. CONCLUSIONS: Our findings show that some learning and memory abilities are impaired in patients with TLE irrespective of the presence of overt damage. This supports the theory that focal epileptic discharges, rather than the lesions themselves, affect these functions. The pathologic characteristics and intratemporal location of an associated lesion do not seem to play an important role in determining learning and memory impairment when clinical and treatment-related factors are taken into account.     

Raven's coloured progressive matrices: normative values on 305 adult normal controls

The use of Raven's Coloured Progressive Matrices (PM 47) in experiments with brain-damaged patients is briefly reviewed. Because norms for adults are still not available, normative data were calculated on 305 normals; corrections for age and education and centile allocation of the scores are furnished.     

Lateralizing value of memory tests in drug-resistant temporal lobe epilepsy

Our aim was to test the lateralizing value of a neuropsychological battery including several memory tests on a large sample of consecutive patients with drug-resistant temporal lobe epilepsy (TLE) evaluated for epilepsy surgery. We studied 73 right-handed patients (56% males, mean age 35.3 +/- 11.2 years, 49% left TLE) aged 16 years or older with normal IQ who underwent a preoperative neuropsychological assessment including several memory tests and were seizure-free after at least 1 year of follow-up. Forty-seven had TLE due to hippocampal sclerosis, whilst 26 had TLE secondary to tumors or other lesions. Receiver Operating Characteristic (ROC) analysis and discriminant function analysis were used to evaluate the lateralization value of selected tests and of the battery as a whole, respectively. In patients with TLE secondary to tumors or other lesions, no test showed significant lateralizing value. In patients with TLE due to hippocampal sclerosis, the immediate (P < 0.01) and delayed (P < 0.001) Rey Auditory Verbal Learning Test (RAVLT) displayed substantial discriminatory ability. The battery as a whole correctly classified 82% of patients with respect to side of epileptogenesis. Our findings suggest that a non-invasive, relatively short and unexpensive neuropsychological battery based on memory tests may profitably complement other well-established diagnostic procedures such as video-EEG or magnetic resonance imaging (MRI), at least in patients with drug-resistant TLE due to hippocampal sclerosis.     

Theory of mind in frontal and temporal lobe epilepsy: cognitive and neural aspects

Purpose: Theory of mind (ToM) is an important prerequisite to social behavior. This study evaluated ToM in patients with temporal (TLE) or frontal lobe epilepsy (FLE) aiming to determine the cognitive aspects, severity, and pathophysiologic mechanisms of ToM impairment in focal epilepsy. Methods: One hundred thirty‐eight patients with TLE (n = 109) or FLE (n = 29) and 69 healthy subjects underwent the Faux Pas task (FPT), which evaluates the recognition and comprehension of others’ mental states, and neuropsychological tests for other cognitive functions. Key Findings: Factor analysis of all test scores yielded two ToM factors (Recognizing faux pas, FP; Excluding nonexistent FP) distinct from the Control, Language, Matching, and Praxis factors. With respect to healthy subjects, both TLE and FLE patients showed correct exclusion of nonexistent FPs but significantly lower recognition and comprehension of real FPs. FLE patients were also impaired with respect to TLE patients. In the whole patient group, schooling and group membership predicted ToM impairment. In FLE patients, the comprehension of mental states was predicted by disease duration, whereas TLE patients’ comprehension of affects and intentions was associated with early age of seizure onset and medial temporal lobe sclerosis (MTLS). Significance: Focal epilepsy impairs advanced ToM abilities. FLE may affect online performances owing to long‐lasting dysfunctions of the prefrontal areas. MTLS may provoke selective ToM deficits due to medial temporal damage, prefrontal dysfunctions, or early interference with cognitive development. Future studies are needed to determine the implications of ToM impairment on behavior and quality of life.     

Wisconsin card sorting test in children with temporal lobe epilepsy

To search for the origin of frontal lobe dysfunction identified by the Wisconsin card sorting test (WCST) in temporal lobe epilepsy (TLE) patients, we investigated the WCST performance among 19 children with TLE (with hippocampal atrophy (HA group N=12), without structural lesions (NSL group N=7)), 15 patients with frontal lobe epilepsy (FLE group), and age-matched normal controls (N group). The paired verbal association learning test (PVALT) and Benton visual retention test (BVRT) were also performed. HA group and FLE groups achieved significantly fewer categories and demonstrated more perseverative errors on the WCST than NSL and N groups. In addition, category achievement in WCST showed significant inverse correlation to age at the initial status convulsivus in the HA group (P<0.05). The achievement on PVALT and BVRT did not show any significant differences between HA and FLE groups (P>0.05). Thus, the frontal lobe dysfunction in the HA group is found to exist as early as 7 years old, when they seem to have only a short seizure history or to receive a little electrical interference from the temporal lobe focus to the frontal region. These facts would underscore the importance of prefrontal dysfunction persisting from the early insults and only becoming apparent after maturation of the prefrontal region in patients with mesial TLE.     

The role of sleep in forgetting in temporal lobe epilepsy: a pilot study

The purpose of this study was to examine how sleep impacts memory function in temporal lobe epilepsy (TLE). Patients with TLE (n=7) and control subjects (n=9) underwent training and overnight testing on (1) a motor sequence task known to undergo sleep-dependent enhancement in healthy subjects, and (2) the selective reminding test, a verbal memory task on which patients with TLE have shown impaired performance 24 hours after training. Sleep data were collected by polysomnography. Results indicate that patients with TLE display greater forgetting on the selective reminding test compared with controls over 12 hours of daytime wakefulness, but not over a similar period including a night of sleep. Slow wave sleep is correlated with overnight performance change on the selective reminding test. Patients with TLE show no deficit in sleep-dependent motor sequence task improvement. The findings provide potential insight into the pattern and pathophysiology of forgetting in TLE.     

Intracarotid amobarbital procedure and prediction of postoperative memory in patients with left temporal lobe epilepsy and hippocampal sclerosis

PURPOSE: Although temporal lobe epilepsy (TLE) patients with dominant hemisphere hippocampal sclerosis generally have good cognitive outcome after anterior temporal lobectomy (ATL), a minority of patients experience at least mild post-ATL decline on one or more standardized measures of episodic and semantic memory. The goal of this investigation was to determine whether memory outcome in this group could be predicted from preoperative intracarotid amobarbital procedure (IAP) recognition memory scores. METHODS: Data from 22 left TLE patients were studied retrospectively. All were left hemisphere language dominant and had IAP scores for each hemisphere, a significant degree of pathology-confirmed left hippocampal sclerosis (HS+), and no positive MRI findings other than atrophy. Cognitive outcome status was represented by the number of pre- to post-ATL declines across three tests, as defined by 90th percentile Reliable Change Index (RCI) criteria. RESULTS: Only 14% of the sample exhibited decline on more than one memory test. Low right IAP (left hemisphere injection) scores and relatively high preoperative cognitive ability and age at surgery predicted a greater risk of post-ATL memory decline. CONCLUSIONS: A minority of left TLE HS+ patients experience at least a mild degree of RCI-defined decline in episodic or semantic memory after ATL. The right hemisphere IAP memory score, which reflects the functional reserve of the contralateral hemisphere, can help predict the risk of postoperative memory decline for TLE patients in whom HS+ is likely based on the presence of hippocampal atrophy on MRI or early age of seizure onset.     

List-learning and verbal memory profiles in childhood epilepsy syndromes

Findings of material-specific influences on memory performance in pediatric epilepsy are inconsistent and merit further investigation. This study compared 90 children (aged 6 years to 16 years) with childhood absence epilepsy (CAE), frontal lobe epilepsy (FLE), and temporal lobe epilepsy (TLE) to determine whether they displayed distinct list-learning and verbal memory profiles on the California Verbal Learning Test — Children's Version (CVLT-C). Group comparison identified greater risk of memory impairment in children with TLE and FLE syndromes but not for those with CAE. While children with TLE performed worst overall on Short Delay Free Recall, groups with TLE and FLE performed similarly on Long Delay Free Recall. Contrast indices were then employed to explore these differences. Children with TLE demonstrated a significantly greater retroactive interference (RI) effect compared with groups with FLE and CAE. Conversely, children with FLE demonstrated a significantly worse learning efficiency index (LEI), which compares verbal memory following repetition with initial recall of the same list, than both children with TLE and CAE. These findings indicated shallow encoding related to attentional control for children with FLE and retrieval deficits in children with TLE. Finally, our combined sample showed significantly higher rates of extreme contrast indices (i.e., 1.5 SD difference) compared with the CVLT-C standardization sample. These results underscore the high prevalence of memory dysfunction in pediatric epilepsy and offer support for distinct patterns of verbal memory performance based on childhood epilepsy syndrome.