Material-specific deficits in "remembering" in patients with unilateral temporal lobe epilepsy and excisions

A growing body of research suggests that "remembering" and "knowing" may be dissociable aspects of recognition memory. Cognitive theorists have argued that the former reflects conceptual processing and is based on distinctive memory traces whereas the latter is associated with perceptual analysis and reflects fluency of processing. Here, we investigate whether this framework can account for memory deficits observed following right or left temporal lobe damage, as suggested by Blaxton and Theodore [Brain and Cognition 35 (1997) 5]. Recognition memory for faces and words was examined in patients with unilateral temporal lobe epilepsy or excisions (TLE) and controls using the "remember-know" recognition paradigm. Participants studied items under conditions designed to enhance either conceptual processing or focus their attention on superficial aspects of the items. For controls, there was an increase in "remember" responses following conceptually-based encoding for both words and faces. This enhancement was eliminated in patients with left TLE for words and those with right TLE showed a diminished effect for faces. This pattern indicates an impairment in the ability to benefit from conceptual encoding that is specific to material preferentially processed by the damaged hemisphere. Furthermore, this effect was only observed for "remember" responses, which are based on the participants' ability to recollect specific contextual aspects of the original study experience. These data can be interpreted in relation to current theories of hippocampal function, which emphasize the critical role played by the hippocampus in relational memory formation and retrieval. We offer this as a novel interpretation of the "remember-know" literature.     

Cognitive strategies in patients with unilateral temporal lobe excisions

The performance of patients with surgical excisions of either the left or right temporal lobe and a normal control group was compared on a hypothesis test. Subjects in both temporal lobectomy groups solved fewer problems than controls; and there was no difference in the performance of left and right lobectomy patients. However, analyses of cognitive patterns revealed specific strategies associated with subjects having undergone left temporal lobe excisions. These patients formulated fewer hypotheses than controls and tended to shift from a given hypothesis even when it was indicated to be correct. Conversely, right temporal lobectomy patients tended to retain a given hypothesis which was indicated to be incorrect. The same results were found with and without memory assistance, indicating that these cognitive strategies occur independent of overt memory deficits.     

The temporal unraveling of autobiographical memory narratives in patients with temporal lobe epilepsy or excisions

Medial temporal lobe epilepsy (TLE), a condition known to affect the integrity and function of medial temporal lobe structures such as the hippocampus, has been shown to disrupt memory for real‐life episodes. Here, patients with unilateral TLE, patients who received a unilateral temporal lobe resection to cure TLE, and healthy controls produced free narratives of autobiographical memories (AMs). To assess temporal resolution, narratives were segmented into bits of information, or details, which were classified according to how precisely they could be located within the time course of the AM. Categories included details corresponding to the entire AM, to parts or subevents within the AM, and to actions taking place within seconds to minutes. The number of details per category was tallied and compared between patients and controls. Temporal order was assessed by determining the correct (internally consistent) chronological order of the sequence of events within the narrative. Results indicate that while patients' memory for the parts or subevents of personal episodes was intact, as was their temporal order, their memory for the minute‐by‐minute unraveling of the episode was impaired. We believe this loss of temporally specific details may contribute to the reduced vividness of AM recollection in TLE patients. Our findings provide further evidence that patients with hippocampal damage retrieve skeletal AMs for which the gist of the memory is maintained, but the specific details are lost. © 2010 Wiley‐Liss, Inc.     

Remote memory in temporal lobe epilepsy

PURPOSE: The present study aims at characterizing remote memory in patients with temporal lobe epilepsy (TLE); it also considers the impact of its most important variables (lateralization of the lesion, duration of epilepsy, age at onset, and seizure frequency) on remote memory. METHODS: We examined the performance of 38 patients with unilateral TLE (19 right TLE and 19 left TLE) and 35 healthy subjects on six remote memory tasks. Memory for personal events was assessed by using the Autobiographical Memory Interview and the Modified Crovitz Test. Memory for public events was evaluated by means of photographs of famous faces and famous scenes, questions about famous events, and the Dead/Alive Test. RESULTS: Both right-TLE and left-TLE groups had impaired memory for autobiographic episodes and public events relative to normal subjects. In contrast, personal semantic memory was preserved. In addition, an effect of laterality was recorded, with right-TLE patients obtaining significantly better scores than left-TLE patients on every test. Duration of epilepsy, age at onset, and seizure frequency did not influence performance on remote memory measures. CONCLUSIONS: The comprehensive neuropsychological study of 38 TLE patients showed that this neurologic condition affects remote memory systems differently. We discuss the different factors that could account for this pattern of performance on the bases of both functional brain organization and memory theories.     

Associative episodic memory and recollective processes in childhood temporal lobe epilepsy

While the current literature on children suffering from temporal lobe epilepsy (CTLE) mostly focuses on material-related episodic memory deficits according to seizure-onset lateralization, the present study examined associative episodic memory according to the type of information to memorize (e.g., factual, spatial, and sequential) and further investigated subjective and objective recollection. Eleven children with left temporal lobe epilepsy (LTLE), 10 children with right temporal lobe epilepsy (RTLE), among whom 9 displayed hippocampal sclerosis (HS), and 42 healthy controls completed the WHAT–WHEN–WHERE protocol (Guillery-Girard et al., 2013). Group comparisons were first conducted according to the affected side and second according to the underlying pathology. Results showed associative memory impairments in patients irrespective of the affected side. Moreover, this study revealed that HS is particularly deleterious to associative and subjective recollection in CTLE. In addition, this study emphasizes the need for assessing episodic memory in childhood TLE beyond material specificity.     

Metabolic evidence for episodic memory plasticity in the nonepileptic temporal lobe of patients with mesial temporal epilepsy

Purpose: Metabolic changes have been described in the nonepileptic temporal lobe of patients with unilateral mesiotemporal lobe epilepsy (MTLE) associated with hippocampal sclerosis (HS). To better understand the functional correlate of this metabolic finding, we have sought to characterize brain regions in patients with MTLE that show correlation between unilateral episodic memory performances, as assessed by intracarotid amobarbital test (IAT), and interictal regional cerebral metabolism measured by [¹⁸F]‐fluorodeoxyglucose positron emission tomography (FDG‐PET). Methods: Resting FDG‐PET was performed interictally in 26 patients with unilateral MTLE caused by HS (16 female, mean age: 36 years; 16 left HS). Using statistical parametric mapping (SPM8), we performed a group comparison analysis comparing brain metabolism in the patients and in 54 adult controls (27 female, mean age: 32 years), with FDG‐PET data of right HS patients being flipped. IAT scores of nonepileptic hemisphere functions (amobarbital injection ipsilateral to HS) were used as covariates of interest in a correlation analysis with regional brain metabolism. Key Findings: The group comparison analysis revealed significant hypometabolic areas in a widespread temporofrontal network ipsilateral to HS. In addition, a significant increase in metabolism was found in mesial and lateral temporal regions contralateral to HS. Significant positive correlations were found between IAT scores of nonepileptic hemisphere functions and mesial temporal metabolism in this hemisphere. Significance: This study demonstrates the existence of significant increase in relative regional cerebral glucose metabolism in mesial and lateral temporal regions contralateral to the epileptic focus in patients with unilateral MTLE associated with HS. The positive correlation in these brain regions between IAT scores and metabolism supports the role of disease‐induced plasticity mechanisms contralateral to HS in the preservation of episodic memory processes.     

Associative reinstatement: A novel approach to assessing associative memory in patients with unilateral temporal lobe excisions

We investigated whether unilateral medial temporal lobe (MTL) damage disrupts associative reinstatement, which represents the gain in item memory when the studied associative information is reinstated at retrieval. We were interested to see whether associative reinstatement relies on the same relational binding operations that support other types of associative memory (associative identification and recollection) thought to be subserved by the MTL. In addition, we examined whether such damage affects the different types of associative memory to a greater extent than item memory and item familiarity, and whether a different pattern is seen in patients with language dominant relative to non-dominant temporal lobe resection when the studied material consists of verbal information. To do so, we used a word pair recognition paradigm composed of two tasks: (1) a pair recognition task that provides measures of associative reinstatement and item memory, and (2) an associative identification recognition task that provides a measure of associative identification memory. Estimates of item familiarity and recollection were derived from performance on both tasks using a variant of the process-dissociation procedure. Our results showed that associative reinstatement, like other types of associative memory measures, was impaired in patients with unilateral resection, irrespective of the side of damage. Item familiarity, however, was impaired solely following language dominant resection. The lack of a laterality effect in our relational measures was likely due to using an encoding task that promoted formation of both verbal and visual associations, whereas item-based familiarity could rely exclusively on verbal operations. We propose that associative reinstatement provides a sensitive measure of relational memory that is less dependent on strategic processing and therefore more appropriate for evaluating MTL function in patients.     

Pseudoword and real word memory in unilateral temporal lobe epilepsy

Recognition memory for pronounceable pseudowords (PWs), real words, and degraded photographs of unfamiliar faces, was examined in 45 patients with unilateral temporal lobe epilepsy (TLE), before and after Anterior Temporal Lobectomy, to test predictions from two accounts of hemispheric differences in memory functioning: (1) The 'material-specific' account predicts that left TLE (LTLE) patients would be impaired in memory for both familiar (real words) and unfamiliar (PWs) verbal stimuli, while memory for novel complex visual stimuli (unfamiliar faces) would be impaired in right TLE (RTLE) patients. (2) The 'familiarity' account predicts that memory for familiar stimuli (such as words) will be impaired in LTLE patients, while memory for both linguistic and nonlinguistic unfamiliar stimuli should be disrupted in RTLE patients. Results were consistent with the 'material-specific' hypothesis suggesting that both familiar and unfamiliar linguistic stimuli are processed for memory in the left medial temporal lobe (MTL), whereas unfamiliar nonverbal stimuli are processed for memory in the right MTL.     

Nonspatial conditional learning impaired in patients with unilateral frontal but not unilateral temporal lobe excisions

The present study examined the effect of unilateral frontal- or temporal-lobe excisions on the acquisition of a conditional task requiring that the subjects respond to each one of six different coloured stimuli by selecting, from a set of six abstract designs, the correct design for each stimulus. Patients with excisions from the left or right frontal cortex were impaired in learning this task, whereas patients with left or right temporal-lobe excisions, with or without radical involvement of the hippocampal region, were not impaired. These findings demonstrate that the major role played by the frontal cortex in the acquisition of conditional responses is a general one and not restricted to situations involving different movements.     

Visual learning deficits in nonresected patients with right temporal lobe epilepsy.

A visual learning test Diagnostikum für Zerebralsch?den (DCS) was revised and applied to three matched patient groups defined by interictal and ictal EEG findings: 24 patients with left temporal lobe epilepsy (LTE), 19 patients with right temporal lobe epilepsy (RTE) and 34 patients with a bitemporal epileptic involvement (BTE). Fifty seven healthy subjects served as controls. Performance on a measure of sustained attention and visual construction was also assessed. Results were as follows: (1) In contrast to controls and LTE patients, patients with right temporal epileptic involvement (RTE/BTE) showed a significantly reduced immediate recall as well as a reduced learning capacity and mean learning performance. (2) Patients made significantly more errors than controls, with RTE patients exhibiting the most visuo-spatial errors. (3) RTE/BTE patients additionally showed impaired performances on visuo-construction, but when visual construction scores were used as covariate, they did not diminish the strong group effects upon learning. (4) Attentional deficits were independent from memory deficits and rather reflected the bitemporal extention of epilepsy. As a conclusion, the data suggest an impairment of visual-spatial consolidation processes in patients with right temporal lobe epilepsy.     

The localization and lateralization of memory deficits in children with temporal lobe epilepsy

PURPOSE: It is often reported that children with temporal lobe epilepsy (TLE) experience nonlateralized memory impairments. However, many of these studies have been exploratory and not based on memory theory. Further, differences between mesial and lateral subgroups have not been adequately examined. This study aimed to discern more specific patterns of memory impairment in children with TLE. METHODS: Forty-three children (5-16 years) with lesional TLE participated. Subjects were categorized in terms of lesion laterality (left, n = 21; right, n = 22) and intratemporal location (mesial, n = 31; lateral, n = 12). Verbal and nonverbal memory tasks were administered that reflected associative, allocentric and recognition paradigms. RESULTS: Facial recognition was poorer in right TLE (p = 0.03). There were no differences between left and right groups on any other memory task, even when comparisons were restricted to cases with mesial involvement. Irrespective of laterality, clear differences were observed between mesial and lateral lesion subgroups (arbitrary associative learning, p = 0.01; complex figure recall, p = 0.03). The lateral lesion subgroup displayed intact memory function relative to normative standards. CONCLUSIONS: Memory is more frequently impaired in children with mesial as opposed to lateral TLE. Tasks with an associative component discriminated between these subgroups, supporting an associative model of hippocampal function. With the exception of facial recognition, memory deficits were not lateralized. Therefore, the nature of memory impairment experienced by children with TLE cannot be extrapolated from adult models.     

Visual memory deficits in temporal lobe epilepsy: toward a multifactorial approach.

Temporal lobe epilepsies (TLE) are associated with material-specific memory deficits depending on the side of seizure origin. However, while verbal memory deficits have been consistently reported in patients with left-sided TLE, the relationship between visual memory deficits and right-sided TLE is more complex. Here, we review factors that influence the pattern of lateralization and the nature of visual memory impairments in TLE and discuss the possible relationship between these deficits and perceptual impairments in TLE patients.     

Lateralized memory deficits on the Wada test correlate with the side of lobectomy only for patients with unilateral medial temporal lobe epilepsy

The aim of this study was to determine whether the predictive value of the intracarotid amobarbital test (IAT) for the side to be resected is applicable only to medial temporal lobe epilepsy and to investigate whether there are different patterns of memory performances on the IAT between patients with unilateral mesial temporal sclerosis (UMT group) and those without (non-UMT group). We studied 30 patients in the UMT group and 10 in the non-UMT group, who underwent pre-surgical evaluation for intractable temporal lobe epilepsy. Memory performances on the IAT was defined as the percentage of memory items presented during unilateral hemispheric anesthesia that was recognized after recovery. More than a 20% decline of the memory performance on the IAT compared with the memory performance on the pre-test was regarded as a memory deficit. Age at onset of epilepsy was significantly younger in the UMT than in the non-UMT group. Surgical outcome was significantly better in the UMT than in the non-UMT group. The lateralizing value of unilateral memory deficits on the IAT was statistically confirmed. There was a significant association between falsely lateralizing memory performances and the non-UMT group. Excluding the exceptional cases with right-sided language dominance in spite of right-sided lesions, the high incidence of the unilateral right-sided memory deficits in the non-UMT group was statistically significant. This study suggested that the excellent lateralizing value of the memory performances on the IAT is limited to patients with mesial temporal lobe epilepsy. IAT memory performances in patients without such lesions can be misleading, even if lateralized, because their memory status presumably reflects a natural lateralization of the memory organization which is independent of the epileptogenic focus.     

Adequacy of language function and verbal memory performance in unilateral temporal lobe epilepsy.

We examined adequacy of language functions, their influence on verbal learning and memory performance, and the relative effects of language function and laterality of seizure focus on the memory performance of 99 left-hemisphere dominant patients with invasively verified epilepsy of left (N = 47) or right (N = 52) temporal lobe origin. Patients with left temporal lobe epilepsy (TLE) scored significantly lower than the right TLE group on several aphasia battery subtests (Visual Naming, Sentence Repetition, Token Test, Reading Comprehension, Aural Comprehension). Adequacy of language function (nominal speech) was significantly related to verbal learning and memory performance for both left and right TLE groups. Finally, comparison of the predictive significance of laterality of TLE and adequacy of language function indicated that language functions (Visual Naming and Aural Comprehension), but not laterality of TLE, were significant predictors for verbal learning and memory performance. It is concluded that: 1) adequacy of basic language functions is particularly compromised in left TLE, 2) there is a significant relationship between adequacy of language function and several aspects of verbal learning and memory ability in both left and right temporal lobe groups, and 3) clinical assessment and theoretical models of memory need to consider these relationships.     

Memory for public events in patients with unilateral temporal lobe epilepsy

Memory for public events (PEs) was assessed as a marker of remote declarative memory in 36 patients with temporal lobe epilepsy (TLE) and compared with that of 19 patients with extra-TLE (ETLE), 17 patients with idiopathic generalized epilepsy (IGE), and 23 healthy volunteers. Verbal IQ, inventory-based evidence of depression, handedness, onset of illness, disease duration, and medication were obtained. Memory for PEs was reduced in all patient groups (TLE, P < 0.0001; ETLE, P = 0.009; IGE, P = 0.008). The TLE group showed reduced memory for PEs compared with the other patients with epilepsy (P = 0.001). A time gradient was observed, with worse memory for PEs of the 1990s and for PEs that occurred after onset of illness. Our data support the key role of the temporal lobe in remote declarative memory. With patients with TLE remembering fewer PEs from the period after onset of epilepsy, the deficits can be partly attributed to unsuccessful consolidation rather than retrieval difficulties alone.     

Self-report of memory function in patients with temporal lobe epilepsy and temporal lobectomy

Thirty-one surgical candidates with a unilateral temporal lobe seizure focus, 72 temporal lobectomy patients, 63 non-epileptic controls and their relatives, respectively, filled in the Memory Observation Questionnaire. The two patient groups rated their current memory similarly, but significantly worse than controls rated their own memory. Memory status was judged to be improved approximately three years after a temporal lobectomy. The relatives' ratings agreed with those of the patients. Thus patients who underwent surgical resection for relief of temporal lobe epilepsy did not report further subjective deterioration in memory compared to pre-operative cases. Laterality of excision did not affect self-report of general memory function. Nevertheless, a brief Verbal memory subscale yielded the expected material specific pattern after unilateral temporal lobectomy.     

Recognition and identification of famous faces in patients with unilateral temporal lobe epilepsy.

We examined the performance of 21 patients with unilateral temporal lobe epilepsy (TLE) and hippocampal damage (10 lefts, and 11 rights) and 10 age-matched controls on the recognition and identification (name and occupation) of well-known faces. Famous face stimuli were selected from four time periods; 1970s, 1980s, 1990-1994, and 1995-1996. Differential patterns of performance were observed for the left and right TLE group across distinct face processing components. The left TLE group showed a selective impairment in naming famous faces while they performed similar to the controls in face recognition and semantic identification (i.e. occupation). In contrast, the right TLE group was impaired across all components of face memory; face recognition, semantic identification, and face naming. Face naming impairment in the left TLE group was characterized by a temporal gradient with better naming performance for famous faces from more distant time periods. Findings are discussed in terms of the role of the temporal lobe system for the acquisition, retention, and retrieval of face semantic networks, and the differential effects of lateralized temporal lobe lesions in this process.