Brain Advance Access originally published online on September 30, 2004
Brain 2004 127(11):2419-2426; doi:10.1093/brain/awh293
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Brain Vol. 127 No. 11 © Guarantors of Brain 2004; all rights reserved
Pre-operative verbal memory fMRI predicts post-operative memory decline after left temporal lobe resection
1 Department of Clinical and Experimental Epilepsy and 2 Wellcome Department of Imaging Neuroscience, Institute of Neurology, University College London, and 3 National Society for Epilepsy Chalfont Centre, Chalfont St Peter, UK
Correspondence to: Dr Mark Richardson, Box 29, Institute of Neurology, Queen Square, London WC1N 3BG UK E-mail: m.richardson{at}ion.ucl.ac.uk
Received May 6, 2004. Revised July 9, 2004. Accepted July 10, 2004.
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Functional MRI (fMRI) of cognitive tasks depends on technology widely available in the clinical sphere, but has yet to show a role in the investigation of patients. We report here the first demonstration of a clinically valuable role for cognitive fMRI. Temporal lobe epilepsy (TLE) is commonly caused by hippocampal sclerosis and is frequently resistant to drug treatment. Surgical resection of the left hippocampus in this setting can cure seizures, but may produce significant verbal memory decline, which is hard to predict. We report 10 right-handed TLE patients with left hippocampal sclerosis who underwent left hippocampal resection. We compared currently used data for the prediction of post-operative verbal memory decline in such patients with a novel fMRI assessment of verbal memory encoding. Multiple regression analyses showed that fMRI provided the strongest independent predictor of memory outcome after surgery. At the individual subject level, the fMRI data had high positive predictive value for memory decline.
Key Words: fMRI; memory; hippocampus; epilepsy; surgery
Abbreviations: fMRI = functional MRI; IAP = intracarotid amytal procedure; MTLE = mesial temporal lobe epilepsy
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Introduction |
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Epilepsy is the most prevalent serious neurological disorder, with a prevalence of 0.5–1% (Hauser, 1998
). Approximately 30% of people with epilepsy continue to have seizures despite antiepileptic drug treatment; the majority suffer from focal epilepsy (Crawford, 2000). In this context, neurosurgery to resect the epileptic focus is an important and under-used treatment option. The first randomized trial of surgery versus optimal drug treatment in temporal lobe epilepsy (Wiebe et al., 2001) demonstrated a seven-fold increase in the likelihood of being seizure-free in the surgically treated group, with an associated highly significant improvement in quality of life.
The most frequent pathology identified in drug resistant epilepsy patients is hippocampal sclerosis, giving rise to the common syndrome of mesial temporal lobe epilepsy (MTLE). Despite a seizure-free outcome, many patients suffer a significant decline in memory ability after temporal lobe resection, especially for verbal memory following left-sided resection in right-handed patients. Decline correlates inversely with severity of hippocampal sclerosis in the surgical resection specimen (Hermann et al., 1992; Sass et al., 1994) and with severity of hippocampal sclerosis assessed by left hippocampal volume measured on pre-operative MRI (Trenerry et al., 1993).
Pre-operative memory performance is also a predictor of post-operative memory decline, with better performance predicting worse decline (Helmstaedter and Elger, 1996; Jokeit et al., 1997). Concern about memory decline and current limitations in its prediction play an important role in limiting the number of patients undergoing potentially seizure-curing surgery. Memory may suffer in this context because hippocampus and related mesial temporal lobe (MTL) structures are crucial to long-term episodic memory function (Squire and Zola-Morgan, 1991; Squire, 1992; Lepage et al., 1998; Cabeza and Nyberg, 2000).
Patients judged at risk of post-operative amnesia undergo the intracarotid amytal procedure (IAP or ‘Wada test’), during which sodium amytal is injected into each internal carotid artery in turn, allowing selective anaesthesia of each cerebral hemisphere. The ensuing period of unilateral hemispheric anaesthesia enables the memory capacity of the un-anaesthetized hemisphere to be examined in isolation. This test is crude and limited due to of the brevity of the anaesthesia, dysphasia during dominant hemisphere injection and patient sedation. It is also highly invasive and carries a significant risk of adverse outcomes, including stroke. Although IAP provides a reasonable index of the risk for amnesia, it is a poor predictor of the extent of verbal memory decline, although some studies have shown modest predictive value (Loring et al., 1995; Jokeit et al., 1997; Lee et al., 2003).
Functional MRI (fMRI) is attractive as a tool to examine memory in patients because of its wide availability and minimal risks. A small number of studies has shown patients with left MTLE preferentially activate right hippocampus in tasks assumed to require left or bilateral hippocampal function (Detre et al., 1998; Dupont et al., 2000; Jokeit et al., 2001; Golby et al., 2002). None of these studies used a design that allowed memory specifically to be examined in isolation.
Only one previous study from our group (Richardson et al., 2003) has shown that right-handed patients with left hippocampal sclerosis preferentially activate the right hippocampal formation in a verbal memory encoding task. We also showed that, in left hippocampal sclerosis patients, there is a distribution of activity between left and right hippocampi during this verbal encoding task that reflects the severity of left hippocampal sclerosis. Thus, patients with mildly affected left hippocampi showed relatively greater activity in left hippocampus than right hippocampus while patients with more severe pathology showed relatively more activity in right than left hippocampus (Richardson et al., 2004).
Two studies have revealed the potential for fMRI of a memory-related task to predict clinical outcomes in MTLE patients: (i) fMRI combined with IAP correctly predicted which patients undergoing anterior temporal lobe resection would become seizure-free (Killgore et al., 1999); and (ii) in the same group of patients, there was a correlation between mesial temporal fMRI activity and recognition memory change following surgery (Casasanto et al., 2001).
To date, there are no clear demonstrations that fMRI has a better predictive value for clinical outcomes compared with other established tests in any neurological field. Our aim in this study was to investigate the utility of event-related fMRI as a predictor of verbal memory decline in right-handed patients with left hippocampal sclerosis undergoing left anterior temporal lobe resection and to compare fMRI with existing techniques.
We previously recruited 26 right-handed patients with left hippocampal sclerosis who underwent evaluation for possible surgery in our centre (the pre-operative data for 24 of these were reported previously (Richardson et al., 2003, 2004). Ten of these subjects underwent surgery, became seizure-free and had histopathologically proven hippocampal sclerosis. The predictive value of pre-operative fMRI for post-operative memory decline in these subjects is reported here.
In this study, we examined encoding of neutral words. We show that the severity of post-operative verbal memory decline is strongly predicted by a multiple regression model which includes left hippocampal volume, pre-operative verbal memory score and the difference in successful encoding activity between left and right hippocampus. We show that hippocampal encoding activity difference is the strongest independent predictor and has high predictive value at the level of individual patients.
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Subjects
Twenty-six consecutive subjects with an MRI-based diagnosis of left hippocampal sclerosis were recruited prospectively from the epilepsy surgery programme of the National Hospital for Neurology and Neurosurgery, London, UK. All 26 subjects underwent an fMRI study during evaluation for surgery.
Inclusion criteria for the 10 subjects reported here were: drug treatment resistant MTLE; right-handed; normal right hippocampal imaging parameters; first language English; seizure-free at least 6 months following left temporal lobe resection; and histopathology of the resection specimen showed hippocampal sclerosis. We included all the subjects who fulfilled these criteria. In the other 16 subjects, surgery was deferred because of a number of factors, which included: significant risk of substantial memory decline or amnesia (according to structural imaging, neuropsychometry and IAP); patient choice; and substantial improvement in seizure control following a change in antiepileptic drug treatment. Participants gave written consent and the study was approved by the Joint Research Ethics Committee of the Institute of Neurology and National Hospital for Neurology and Neurosurgery.
Pre-operative neuropsychometry
To assess verbal memory, we used the List Learning and Story Recall subtests of the Adult Memory and Information Processing Battery (Coughlan and Hollows, 1985) as part of a larger neuropsychometric test battery used for routine pre-surgical evaluation. The List Learning test has an initial registration component (maximum score = 75) and a delayed component (maximum score = 15). The Story Recall Test compares immediate and delayed recall of a story and yields a percent retained score (maximum score = 100). We obtained three clinical neuropsychological measures: (i) list learning—immediate (pre-operative immediate list recall); (ii) list learning—delayed (pre-operative delayed list recall); and (iii) story recall (pre-operative story recall).
Pre-operative structural imaging
Structural MRI was carried out at 1.5 T (Horizon Echospeed, General Electric, Wilwaukee, WI, USA) as part of routine pre-surgical evaluation, including T1 volume and dual-echo whole brain T2-map (Duncan et al., 1996). Hippocampal volumetry was carried out according to a previously published protocol (Van Paesschen et al., 1995).
Pre-operative functional imaging
Functional imaging was performed according to a previously described method (Richardson et al., 2003, 2004). In brief, subjects were scanned at 2 T (Siemens VISION, Siemens, Erlangen, Germany), acquiring T2*-weighted image echo planar imaging (EPI) volumes, providing blood-oxygenation-dependent (BOLD) contrast [33 slices; whole brain; voxel dimensions =3 x 3 x 3.67 mm; TE (echo time) = 40 ms; TR (repetition time) =2.5 s]. SPM99 was used for image analysis (Friston et al., 1995). The images were realigned, corrected for slice timing differences, transformed to the standard anatomical volume and smoothed (8 mm kernel).
A verbal encoding task was used. During scanning subjects were visually presented with 255 single words, including 36 emotionally aversive words (e.g. ‘cancer’, ‘rape’, ‘terrorist’) (Strange et al., 2000), one every 4.5 s. The word pool from which these were drawn is available on request. Subjects pressed a right-hand button to indicate whether the word was ‘living’ or ‘non-living’, and were not asked to memorize the words. Ninety minutes after scanning, subjects performed a surprise recognition memory test (not scanned): subjects were asked to indicate whether the word was definitely remembered (R response); if the word seemed familiar (K response); or was new (N response) (Tulving, 1985). The encoding stimuli were then conditionalized according to subjects' recognition responses. Recognition accuracy (D') was calculated for stimuli labelled ‘R’ as (hit rate) – (false alarm rate).
To test for subsequent memory effects, imaging data were analysed within a two-level random-effects analysis employing an event-related design (Friston et al., 1998). At the first level, trial-specific responses were modelled and each subject's movement parameters were included as confounds. Contrasts of parameter estimates were calculated to produce a ‘contrast image’ for each subject of R minus K for neutral items only; we have showed previously that the responses to emotional words were dependent on amygdala pathology, which was not correlated with hippocampal pathology (Richardson et al., 2004).
We created for each patient a voxel-by-voxel image of left minus right encoding activity (R minus K) difference; these ‘encoding asymmetry’ images were used for further analyses. At the second level, simple regression was used to examine effects within the group. We chose P < 0.05 corrected for peak height both across the whole brain and within the small volume of left hippocampus using a 5 mm radius sphere centred on the peak activation in the left hippocampus in normal subjects in our previous study (Richardson et al., 2003) as the threshold for significance.
Post-operative neuropsychometry
At 3 months post surgery, each subject was tested on parallel versions of the List Learning and Story Recall; these parallel versions have standardized equivalent difficulty. We again collected three neuropsychological measures: (i) list learning—immediate (post-operative immediate list recall); (ii) list learning—delayed (post-operative delayed list recall); and (iii) story recall (post-operative story recall). Using these three measures, performed pre-operatively and repeated post-operatively, we calculated measures of verbal memory change between the first pre-operative and second post-operative assessment (pre-operative—post-operative change in immediate list recall, pre-operative—post-operative change in delayed list recall, pre-operative—post-operative change in story recall).
Data reduction
We expected that there would be a high degree of intercorrelation amongst the measures of memory. Therefore, we used principal components analysis to identify a factor accounting for the largest component of variance amongst these scores. Thus, the three pre-operative measures (pre-operative immediate list recall, pre-operative delayed list recall, pre-operative story recall) were entered into a principal components analysis, from which the first principal component was extracted. Likewise, the three memory change measures (pre-operative—post-operative change in immediate list recall, pre-operative—post-operative change in delayed list recall, pre-operative—post-operative change in story recall) were entered into a principal components analysis, from which the first principal component was extracted.
Prediction of change in memory score: model optimization
We entered the variables predictive of verbal memory outcome into a stepwise linear regression to identify the most important predictive variables.
Hypotheses to be tested
We tested the following hypotheses:
- Pre-operative verbal memory predicts verbal memory decline after surgery.
- Left hippocampal volume predicts verbal memory decline after surgery.
- Encoding asymmetry (derived from fMRI data) predicts verbal memory decline after surgery.
- Encoding asymmetry (derived from fMRI data) is the best predictor of verbal memory decline after surgery.
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Results |
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Demographic, clinical and memory data are summarized in Table 1. Nine of the 10 patients showed decline in at least two of the three memory measures between pre-operative scores and post-operative scores. There was decline in immediate list recall in six patients, no change in two and a slight improvement in two (mean change between pre-operative and post-operative scores was a decline of 5.7 points, ranging from a decline of 17 points to an improvement of 3 points; P = 0.028, paired t-test, 2-tailed). The delayed list recall showed decline in all but one, who had no change (mean change between pre-operative and post-operative scores was a decline of 3.6 points, ranging from a decline of 9 points to zero decline, P = 0.002, paired t-test, 2-tailed). There was decline in story recall in six patients and improvement in four, although overall this change was not significant across the group (mean change between pre-operative and post-operative scores was a decline of 14.2 points, ranging from a decline of 72 points to an improvement of 93 points, P = 0.4 paired t-test, 2-tailed).
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Co-variation between memory scores
The recognition memory score derived from the recognition test carried out following pre-operative fMRI (D') correlated strongly with pre-operative verbal learning (pre-operative immediate list recall), P = 0.005 (Fig. 1A). The first principal component derived from the pre-operative memory scores (‘pre-operative verbal memory’) correlated strongly with pre-operative immediate list recall (R2 = 0.72, P = 0.002) and with pre-operative delayed list recall (R2 = 0.65, P = 0.005), but not with pre-operative story recall (R2 = 0.017). Similarly, the first principal component derived from the pre-operative—post-operative memory change scores (‘post-operative verbal memory change’) correlated strongly with pre-operative—post-operative change in immediate list recall (R2 = 0.97, P < 0.001) and with pre-operative—post-operative change in delayed list recall (R2 = 0.38, P = 0.05) but not with pre-operative—post-operative change in story recall (R2 = 0.051).
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Prediction of memory outcome by structural imaging parameters
Post-operative verbal memory change was strongly predicted by left hippocampal volume (R2 = 0.53, P = 0.017) (Fig. 1B).
Prediction of memory outcome by pre-operative memory scores
Post-operative verbal memory change was predicted by pre-operative verbal memory (R2 = 0.50, P = 0.021) (Fig. 1C).
Prediction of memory outcome by functional imaging parameters (figure 2)
At the group level, a single mesial temporal region showed a correlation between left–right encoding activity difference and post-operative verbal memory change. This region corresponded to the left hippocampus [(–36 –20 –22), Z = 3.64, uncorrected P < 0.001, small-volume corrected P = 0.016]. Across the whole brain, no other regions survived the threshold chosen.
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From a clinical perspective, the power of any predictive test is most relevant at the single subject level. Thus, on an individual subject basis we examined sensitivity, specificity and positive predictive value of pre-operative fMRI in predicting memory decline. We took the simplest approach to this by defining a ‘normal’ test result as predominant left hippocampal activation [as we previously reported for normal subjects (Richardson et al., 2003)] and an ‘abnormal’ test result as predominant right hippocampal activation [as we previously reported for patients with more severe left HS (Richardson et al., 2004)]. We defined memory outcome either as ‘decline’ in memory test score or as ‘no decline’. We used two different thresholds to show decline: either any decline greater than zero, or as a decline greater than one standard deviation from the group baseline values. We used a 2x2 contingency-table approach to examine the ability of an ‘abnormal’ test result to predict ‘decline’ (Table 2).
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Prediction of memory outcome: model optimization by stepwise linear regression
Three predictor variables were entered into a model with ‘post-operative verbal memory change’ as the dependent variable: (i) left–right hippocampal encoding activity difference; (ii) pre-operative verbal memory; and (iii) left hippocampal volume. This model predicted post-operative verbal memory change (R2 = 0.92, P < 0.001). Stepwise linear regression showed only left—right hippocampal encoding activity difference made a significant contribution (significance R2 change, P > 0.1 for the other variables).
To put this into a clinical context, we constructed an analogous model to predict pre-operative—post-operative change in immediate list recall (using left–right hippocampal encoding activity difference, pre-operative immediate list recall and left hippocampal volume as predictors). This model predicted pre-operative—post-operative change in immediate list recall (R2 = 0.84, P = 0.008). In this model, stepwise linear regression again showed that only left–right hippocampal encoding activity difference made a significant contribution (R2 = 0.74, P = 0.001).
Finally, we constructed a model to predict pre-operative—post-operative change in delayed list recall (using left–right hippocampal encoding activity difference, pre-operative delayed list recall and left hippocampal volume as predictors). This model predicted pre-operative–post-operative change in delayed list recall (R2 = 0.58, P = 0.13). As in the other models, stepwise linear regression again showed only left-right hippocampal encoding activity difference made a significant contribution (R2 = 0.55, P = 0.015).
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Discussion |
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In this study, we confirmed previous findings that left hippocampal volume and pre-operative verbal memory function predict the extent of verbal memory decline in right-handed subjects with left hippocampal sclerosis undergoing left anterior temporal lobe resection because of intractable MTLE. Our novel finding is that relatively greater verbal memory encoding activity in left hippocampus compared with right hippocampus—as measured using fMRI—predicts the extent of verbal memory decline in the same subjects. Importantly, fMRI was by far the strongest independent predictor of memory decline and a powerful predictor of outcome for individual patients. We show these effects for two different standard clinical measures of verbal memory and even more strongly for a derivative (first principal component) of a range of standard clinical measures, which best accounts for the variability in measures within the patients studied. This is the first time fMRI has shown a predictive value in a clinical setting over and above currently used tests.
Two functional imaging studies have shown prediction of memory outcome in patients undergoing temporal lobe resection for intractable MTLE. One study used blood-flow PET, a technique not generally available in clinical settings and, due to its poor temporal resolution, incapable of resolving activity associated with single events (Henke et al., 2003). Furthermore, only three of their subjects had left MTLE (the group in whom verbal memory decline is anticipated) and none of these experienced any decline in verbal memory. Hence, the study by Henke and colleagues primarily addressed non-verbal memory decline, which is less disabling and less easy to demonstrate, using a method which is not transferable to the clinical environment. This study, like the study we present here, did not address the issue of whether a change in memory test scores is reflected by a subjective change in memory ability which is symptomatic for the patient.
A second study, reported in abstract form, also included a mixed group of eight left and three right MTLE patients (Casasanto et al., 2001). These subjects underwent a task requiring explicit encoding of visual scenes presented in a block design, with a repeated ‘scrambled’ image as the baseline condition; this design does not allow subsequent memory effects to be revealed. However, the authors undertook a recognition memory test following scanning; a similar visual scene encoding and recognition memory test was also undertaken following subsequent anterior temporal lobe resection. Asymmetry of activation between ipsilateral and contralateral sides in a region of interest (ROI) at the boundary between the hippocampal formation and the lingual gyrus was determined. This asymmetry was strongly correlated with change in recognition memory score between the pre-operative and post-operative assessments. This study therefore also primarily addressed non-verbal memory. In it, memory improvement was seen following surgery in several patients, emphasizing the non-disabling nature of non-verbal memory change in many such patients. In the same group of patients, asymmetry of fMRI activity in the same ROI showed similar efficiency to the IAP for determining seizure outcome (Killgore et al., 1999).
Functional MRI is now a widely used methodology in basic neuroscience, but has yet to show it can provide information useful in clinical settings. Pre-operative localization of motor function is regularly undertaken in some centres to aid neurosurgery in the vicinity of the motor cortex. Although it is often asserted that such an approach provides for a better outcome, there are few supportive data. There is evidence that fMRI of motor function correlates with the sites of motor function determined using electrical stimulation of the cortex during surgery, but the correlation is often imperfect, subject to artefacts in fMRI data, difficult to integrate with other imaging during surgery and possibly requiring subjective interpretation (Stapleton et al., 1997; Krings et al., 2001, 2002; Roux et al., 2001; Liu et al., 2003).
In particular, many brain regions may be activated, especially in patients with lesions, and there is no means to determine which of a number of brain regions activated during an fMRI study is necessary and sufficient for normal function (Krings et al., 2002; Baciu et al., 2003). One study showed a strong prediction from pre-operative data of an immediate post-operative motor deficit following resection of medial frontal lesions if tissue activated in the medial frontal cortex during fMRI was resected, but there was no correlation with outcome a few weeks or months later (Krainik et al., 2001).
Mapping cortex responsible for language function in patients has shown a very strong correlation with IAP findings in the same subjects (Binder et al., 1996; Benson et al., 1999; Springer et al., 1999; Lehericy et al., 2000), although single subject studies are insufficiently sensitive to do more than lateralize language to one hemisphere and more detailed localization has been uncertain. The optimal choice of language task during fMRI remains unclear. An alternative may be to identify the sum total of all regions activated across a range of language tasks (Rutten et al., 2002). In a similar patient group to that presented here, fMRI of a language task showed a predictive value of similar magnitude to the IAP for confrontation naming deficit following left temporal lobe resection (Sabsevitz et al., 2003), but the authors did not present data to show that fMRI was a significantly better predictor of naming outcome compared with IAP.
Our findings have immediate relevance in the evaluation of MTLE patients for possible left anterior temporal lobe resection. There are important further avenues to explore, particularly patients with bilateral pathology and pathology other than hippocampal sclerosis, in whom prediction of verbal memory decline may be difficult. We anticipate that the robust prognostic data provided by our fMRI approach will stimulate the development of further valuable clinical tools utilizing fMRI.
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Acknowledgements |
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We wish to thank Mr William Harkness, neurosurgeon, Dr Maria Thom, histopathologist, and the radiographers of the National Society for Epilepsy MRI Unit for their contributions to this study. We also wish to thank Dr Sanjay Sisodiya and Professor Ley Sander for referring patients. M.P.R. is supported by the Medical Research Council, J.S.D. by the National Society for Epilepsy and R.J.D. by the Wellcome Trust.
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