Brain, Vol. 123, No. 8, 1722-1732,
August 2000
© 2000 Oxford University Press
Episodic memory in left temporal lobe epilepsy: a functional MRI study
1 Unité d'Epileptologie, 2 Department of Urgences Cérébro-vasculaires, Clinique Neurologique Paul Castaigne, 3 Department of Radiology, 4 LENA, CNRS UPR640, Hôpital de la Pitié-Salpêtrière, Paris and 5 CEA, SHFJ, Orsay, France
Correspondence to:
Sophie Dupont, MD, CEA-SHFJ, 4 Place du Général Leclerc, 91406 Orsay, France E-mail: dupont{at}shfi.cea.fr
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Abstract |
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Left medial temporal lobe epilepsy (MTLE) is associated with verbal memory impairment usually related to hippocampal damage. We used functional MRI (fMRI) to investigate the patterns of functional activity in healthy volunteers and MTLE patients engaged in verbal episodic memory tasks to look for evidence of a reallocation of verbal memory in epileptic patients. fMRI data were collected from seven MTLE patients with left-sided hippocampal sclerosis and 10 healthy right-handed control subjects on a 3T scanner. Subjects were instructed to learn a list of 17 words (encoding) and then to recall them (retrieval) on successive trials. Healthy volunteers and patients both exhibited bilateral activation (right higher than left) of the parahippocampal gyrus during the retrieval. This effect was more marked in the control subjects. In contrast to the control subjects, patients exhibited consistent and extensive left prefrontal activations in all the memory tasks. These findings show that verbal memory tasks did not involve the same functional patterns in patients and healthy volunteers. This may be interpreted as a dysfunctional response due to the epilepsy and left hippocampal sclerosis, and could reflect the early onset and progressive course of the disease.
functional MRI; temporal lobe epilepsy; episodic memory; dysfunction; hippocampal sclerosis
BOLD = blood oxygenation level dependent; EPI = echoplanar; fMRI = functional MRI; LTLE = left temporal lobe epilepsy; MTLE = medial temporal lobe epilepsy; SPM = statistical parametric mapping
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Introduction |
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TopAbstractIntroductionSubjects and methodsResultsDiscussionReferences |
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Medial temporal lobe epilepsy (MTLE) is a surgically remediable syndrome with specific clinical presentation and pathophysiological basis, namely hippocampal sclerosis (Engel, 1996
). Impairment of verbal memory is associated with left-sided MTLE. This impairment seems to be linked to the dysfunction of the hippocampal region. In the literature there is evidence from both human and animal research that the hippocampal complex and the neocortex play distinct, complementary roles in episodic memory. Patients with lesions confined to the hippocampal structures show impairment of new learning but are able to retrieve memories acquired years before (Scoville and Milner, 1957). Studies have suggested that the temporal neocortex is a crucial site for the storage of knowledge and personal experiences (Kapur et al., 1992; Hodges et al., 1994). Furthermore, a number of recent functional imaging studies have identified prefrontal and inferior frontal activations during tasks involving episodic memory retrieval (Tulving et al., 1994; Fletcher et al., 1995; Buckner et al., 1996, 1998a). The significance and specificity of this prefrontal activation remains debated (Thompson-Schill et al., 1997; Buckner et al., 1998b). In this study we used functional MRI (fMRI) to examine the hippocampal and extrahippocampal activations in healthy volunteers and left-sided MTLE patients engaged in verbal memory tasks. The aim of the experiment was to investigate whether left hippocampal damage altered the pattern of neocortical activations during episodic verbal memory. First, in control subjects, we wanted to assess the contribution of medial temporal structures and the neocortex to verbal memory and the relationships between these structures. Secondly, we sought evidence of a reallocation of verbal memory in MTLE patients in order to gain further insight into the mechanisms by which patients attempt to compensate or not for epilepsy and/or hippocampal sclerosis. |
Subjects and methods |
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TopAbstractIntroductionSubjects and methodsResultsDiscussionReferences |
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Subjects
The study population included seven patients (four women and three men; mean age 34.4 years, range 18–53 years) with MTLE who were undergoing presurgical evaluation for anterior temporal lobectomy at the Pitié-Salpêtrière Epilepsy Unit. They were matched with a control group consisting of 10 healthy volunteers (eight women and two men; mean age 25.4 years, range 23–30 years). All subjects gave informed written consent in accordance with the Declaration of Helsinki and the study was approved by the ethics committee of the Hôpital de la Pitié-Salpêtrière, Paris. Six patients underwent presurgical evaluation (Adam et al., 1996
) including medical, neurological and neuropsychological examinations, video-EEG monitoring, brain MRI, [18F]fluorodeoxyglucose (FDG)-PET examinations and an intracarotid amytal test. The seventh patient underwent the same presurgical evaluation, with the exception of the neuropsychological examination and the intracarotid amytal test. The inclusion criteria for our study were the following: right-handed lateralization; surface EEG recordings consistent with left-sided medial temporal lobe seizure onset; neuropsychological examination (Table 1) consistent with a left-sided memory deficit; left hippocampal sclerosis diagnosed on volumetric MRI without any other structural abnormalities; and/or left temporal lobe hypometabolism on interictal FDG-PET.
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fMRI procedures
Blood oxygenation level dependent (BOLD) fMRI data were acquired on a 3-T Bruker system equipped with a prototype fast-gradient system and the standard quadrature head coil. Subjects were placed in a supine position in the MRI scanner. Their heads were immobilized with cushions to reduce motion artefact. The stimuli were projected upside down on to a mirror located at the end of the scanner bore. Subjects were equipped with prism glasses that allowed them to see the projection upright in central vision without image distortion. For each subject a series of conventional structural images was first collected to provide detailed anatomical information. Following the acquisition of these sagittal and axial inversion recovery turbo flash T1-weighted localizer images, gradient echo echoplanar (EPI) fMRI was performed in 22 contiguous 5-mm axial slices (repetition time = 6 s, 64 x 80 matrix, 22 cm2 field of view) covering the whole brain. The entire session, including both structural and functional sequences, lasted 45 min the first day and 50 min the following day.
Memory tasks procedures
Memory tasks included verbal episodic memory encoding and retrieval tasks. Two sessions were performed on consecutive days, but we only report here the relevant memory tasks performed during the first session. A sequential task-activation paradigm was employed, alternating between an experimental condition and a baseline condition (see Fig. 1). The baseline condition was the same for all the experiments and consisted of the fixation of the letter A. Scanning was performed over a 324-s block. Each block included 5 control and four experimental conditions beginning with the control condition. Two memory experimental blocks were performed the first day. The encoding experimental block consisted of learning a supra-span list of 17 abstract words that has been used to demonstrate verbal episodic memory deficits in epileptic patients (Jones-Gotman et al., 1993). In the same block the list of words was presented four times, alternating with baseline condition. The words were displayed at the rate of one word every 2 s. Subjects were instructed to learn the words silently for later recall. At the end of the encoding block, subjects rested for 2 min. During the following retrieval experimental condition, subjects were asked to recall silently the words that they had previously learned. At the end of the session, subjects were tested to establish the efficiency of the retrieval of the verbal information and were asked to recall out loud the words that they had previously learned.
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Image analysis
fMRI data were analysed on SPARC workstations (Sun Microsystems, Mountain View, Calif., USA). Statistical analysis was performed in MATLAB (Mathworks, Natick, Mass., USA) using a statistical parametric mapping (SPM) software package (SPM96) developed by Friston and colleagues (Friston et al., 1995
).
Statistical analysis
For each subject we performed a stereotaxic reorientation of the images along the bicommissural line. Images were then coregistered and resliced to correct movement and further spatially transformatted to standard stereotaxic coordinates to correct for anatomical variance across subjects. Analysis of the translation and rotation movements across the images was similar for controls and patients. The standard reference space used in SPM96 is based on the Talairach and Tournoux stereotaxic atlas (Talairach and Tournoux, 1988). The resulting images were convolved with a three-dimensional gaussian filter to suppress noise. The data were then analysed statistically on a voxel-by-voxel basis using a two temporal basis functions model. We first performed an individual analysis for each subject and then a multi-subject analysis using a similar method. Since our aim was to investigate the global changes in neocortical activations caused by hippocampal damage, we focused our study on the group analysis and only report here the results of the multi-subject study. For the multi-subject analysis, a given voxel was considered to be significantly activated if, on comparison with a reference task, there was an increase in the haemodynamic response function at P < 0.0001, with P < 0.01 corrected for multiple comparison. These values correspond to Z-scores of 3.72 and above in this study. A region was considered to be activated if a spatially contiguous set of voxels were all independently significant at a level of P < 0.003.
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Results |
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Memory test performance
As expected, the retrieval performance of control subjects was uniformly high compared with that of left temporal lobe epilepsy (LTLE) patients, in whom it was significantly impaired. During the retrieval experimental condition, control subjects recalled 10.3 ± 4.4 words (mean ± standard deviation), whereas the LTLE patients recalled only 3.1 ± 2.5 words. The difference between the performances of the two groups was significant P < 0.0007 (see Fig. 2
).
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Within-group comparisons of haemodynamic response
Control subjects (activation minus baseline)
Figure 3
shows the SPM activation maps during the encoding and retrieval tasks for the 10 healthy volunteers. Table 2 indicates the coordinates of the areas of significant activation (P < 0.0001, corrected for multiple comparison). During the encoding task, control subjects exhibited significant activation in five cerebral regions: the occipital cortex (Brodmann areas 17 and 18) and the fusiform gyrus bilaterally; the left parietal cortex at the junction between Brodmann areas 40 and 7; the superior temporal cortex (Brodmann area 22 corresponding to Wernicke's area) on the left; and the ventrolateral frontal cortex (Brodmann areas 44 and 45) bilaterally (left greater than right). A broadly similar activation pattern was observed during the retrieval task with, however, three notable differences. First, there was a slight decrease in occipital activation during the retrieval task, whereas left occipitotemporal activation was present only during this retrieval task. Secondly, there was an apparent increase in the spatial extent of the regions showing significant activation during the encoding task, particularly in the left superior temporal cortex and the left ventrolateral frontal cortex. Thirdly, a significant activation was detected during retrieval in both inferomedial temporal cortices bilaterally and the left frontal medial cingular cortex. The inferomedial temporal cortex activation mainly concerned the parahippocampal gyrus. This parahippocampal activation clearly predominated on the right side (see Fig. 4) in terms of number of activation peaks and Z-scores. No hippocampal activation was detected.
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LTLE patients
As depicted in Fig. 5
and Table 3, the LTLE patient activation pathway included five cerebral regions: the parietal cortex (Brodmann areas 40 and 7) bilaterally; the left superior temporal cortex, i.e. Wernicke's area; the left ventrolateral frontal cortex, i.e. Broca's area; the medial frontal cortex (Brodmann areas 6 and 8) bilaterally; and the dorsolateral frontal cortex (Brodmann areas 9, 10, and 46) bilaterally (left greater than right). We showed four major differences in epileptic patients compared with controls: a decrease in occipital and occipitotemporal cortical activation; a decrease in left temporal cortex activation; a dramatic increase in frontal cortex activation (see Fig. 6); and a decrease in limbic activation. First, we noted the absence of primary occipital cortex activation during the encoding task compared with the controls. Similary, no activation was detected in the lateral occipitotemporal cortex during the retrieval task, whereas we noted a decrease in the activation of the medial occipitotemporal cortex (i.e. lingual and fusiform gyrus) in terms of size (decrease of the peak number) and significance (decrease in Z-scores). Secondly, the left superior temporal cortex, i.e. Wernicke's area, was less activated during the retrieval task. Thirdly, a dramatic activation of the frontal cortex was noted during both the encoding and retrieval tasks. Ventrolateral frontal cortex activation was similar in epileptic patients and control subjects, but a new and extensive activation was noted in LTLE patients in the dorsolateral and medial frontal cortex. Lastly, a medial temporal activation was detected during retrieval but this activation was less significant (lower Z-scores) and less extensive than in controls (see Fig. 4
). In addition, we detected no anterior cingulate activation during the retrieval task.
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Discussion |
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TopAbstractIntroductionSubjects and methodsResultsDiscussionReferences |
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In this study we examined the patterns of cerebral activity in epileptic patients and controls engaged in verbal episodic memory tasks. The major finding of this study is that LTLE patients and control subjects show different patterns of brain activations during the acquisition and retrieval of verbal episodic information, especially in the frontal cortex.
Memory encoding in normal subjects
During the encoding task, control subjects activated an occipitotemporoparietal network suggesting visual and word processing, with a predominant left-sided lateralization. No specific temporolimbic activation was detected. The ventrolateral frontal cortex was markedly activated, predominantly on the left side. Although damage to the human lateral frontal cortex does not usually result in a global memory disorder, recent functional studies have demonstrated the involvement of the lateral frontal cortex in episodic memory (Kapur et al., 1994; Tulving et al., 1994; Fletcher et al., 1995). These functional imaging studies suggest a predominant involvement of the anterior prefrontal cortex (Buckner et al., 1995; Grady et al., 1995; Haxby et al., 1996; Schacter et al., 1996), especially the anterior part of Brodmann area 10 (Buckner et al., 1996). The consistent observation of prefrontal activation during explicit memory tasks has been conceptualized as the hemispheric encoding/retrieval (HERA) model (Tulving et al., 1994). This model proposes that left prefrontal cortical regions are preferentially involved in encoding novel aspects of information into episodic memory, whereas right prefrontal cortical regions are preferentially involved in episodic memory retrieval. This dichotomy does, however, remain the subject of debate and some authors have demonstrated that the left prefrontal cortex could also be involved in retrieval tasks (Thompson-Schill et al., 1997), suggesting that left or right prefrontal activations are part of a more general prefrontal system that is required for the selection of responses from memory. In our study the ventrolateral activation of the frontal cortex involved Broca's area. This activation may be related to semantic processing during word encoding and appears to be critical for encoding.
Memory retrieval in normal subjects
The retrieval task was characterized by an increase in the spatial extent of the regions that had been activated during the encoding task, especially the left superior temporal neocortex and the left ventrolateral cortex, as shown in Fig. 5 and Table 3. Another difference with the encoding condition was the parahippocampal activation detected during the retrieval task. This activation clearly predominated on the right side. A right-side lateralization of the medial temporal lobe has already been described during a word retrieval task (Squire et al., 1992; Schacter et al., 1996). This finding underlines the role played by the parahippocampal formations in retrieval of episodic information. Experimental studies in animals have demonstrated that lesions of perirhinal and parahippocampal cortex, sparing the amygdala and hippocampal formation, can produce severe memory impairment in primates (Zola-Morgan et al., 1989; Suzuki et al., 1993). Parahippocampal activations have also been found in many functional studies that examined explicit memory (Stern et al., 1996; Gabrieli et al., 1997). Gabrieli and colleagues have suggested that parahippocampal activation mediates memory processes which discriminate novel from familiar visual stimuli via strong projections from high-level visual areas (Gabrieli et al., 1997). However, in apparent contradiction with this hypothesis, we found that the parahippocampal gyrus was activated during the retrieval tasks and not during the encoding task, which could have required discrimination between novel and familiar stimuli.
Differences in memory processing between epileptic patients and controls
In our study the pattern of activations in patients differed from that in controls. LTLE patients exhibited a decreased activation in the parahippocampal and posterior occipitoparietal regions and a dramatic new activation located in the dorsolateral frontal cortex. These differences may reflect either a dysfunction or a reorganization of normal memory processing linked to epilepsy. We could hypothesize that the failure of the left medial temporal lobe system led LTLE patients to use a compensatory strategy, resulting in a larger activation of the frontal cortex. This extended activation could then represent a cortical reallocation secondary to a functional reorganization of episodic memory. However, the performance of the patients in this study was poor, suggesting that this reallocation is not efficient. We may therefore postulate that the performance variability between patients and controls results from an activation variability within the brain, leading to the hypothesis that the bad memory performances observed in LTLE patients reflect a cortical dysfunction rather than a reorganization. The abnormal activation of the dorsolateral frontal cortex may reflect an alteration of normal memory strategies dealing with the demands of the task. Numerous reports suggest that the prefrontal cortex is made up of several different anatomical and functional areas with a particular role in conscious awareness and attentional, supervisory and strategic functions (Stuss and Benson, 1986; Squire, 1987). LTLE patients could therefore change their memory strategy to deal with the demands of a difficult task requiring an increased load of selective attention. The activation of the dorsolateral frontal cortex would therefore reflect a dysfunction of cerebral memory processing.
Dysfunction of verbal episodic memory and epilepsy
This dysfunction of verbal episodic memory in epileptic patients may result either from the hippocampal dysfunction or from the epileptogenic process. MTLE associated with hippocampal sclerosis is a pathology that alters the temporal lobe system at an early stage. In most of the patients reported in the literature, an early event of febrile convulsions is noted (French et al., 1993) and the epilepsy usually begins in early childhood, around the age of 4–8 years (Adam et al., 1996). Furthermore, some lines of evidence suggest that a subtle pre-existing hippocampal malformation could contribute to the development of subsequent hippocampal sclerosis (Baulac et al., 1998; Fernandez et al., 1998). These data suggest that MTLE is associated with hippocampal damage or dysfunction at an early stage of development. This hypothesis is also supported by the fact that verbal memory deficit is known to be correlated with several indices of hippocampal integrity such as the MRI measurement of the hippocampal volume (Trenerry et al., 1996) or the postoperative histological analysis of the hippocampal pyramidal cell density (Sass et al., 1990). On the other hand, MTLE cannot be considered as a model of pure hippocampal dysfunction (Spencer, 1998). The neuropsychological impairment may be attributable to the more diffuse neurobiological consequences associated with an increasing number of years of intractable seizure activity in the temporal lobe and with the propagation of the epileptic discharges into extratemporal regions. Corticohippocampal neural networks are modified by the ictal and interictal epileptogenic activity. A decline in memory performances may result from the interference between these epileptic networks and the normal cognitive networks. We can therefore speculate that the specific involvement of the prefrontal region in LTLE patients reflects the interaction between the normal memory networks and the epileptic network.
In conclusion, complex neuroanatomical circuits subserve memory. In healthy subjects, verbal episodic memory is mediated by a specific system of related neocortical and medial temporal brain regions. The parahippocampal formations, temporal neocortex and ventrolateral frontal cortex seem to play a crucial role in this memory system. In epileptic patients, we have demonstrated a reallocation of these cognitive and cortical resources, which may be caused either by hippocampal dysfunction or by epileptogenesis. This reallocation might be considered alternatively as an alteration of the normal memory strategies, resulting in bad memory performances. A more detailed study of the precise nature of these neural pathways and their neurochemical substrates should lead to a better understanding of their pathophysiology and may well lead to the development of new therapeutic strategies.
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Received October 14, 1999. Revised January 2, 2000. Accepted February 28, 2000.
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