Functional MRI lateralization of memory in temporal lobe epilepsy

Objective: To determine the feasibility of using functional magnetic resonance imaging (fMRI) to detect asymmetries in the lateralization of memory activation in patients with temporal lobe epilepsy (TLE). Background: Assessment of mesial temporal lobe function is a critical aspect of the preoperative evaluation for epilepsy surgery, both for predicting postoperative memory deficits and for seizure lateralization. fMRI offers several potential advantages over the current gold standard, intracarotid amobarbital testing (IAT). fMRI has already been successfully applied to language lateralization in TLE. Methods: fMRI was carried out in eight normal subjects and 10 consecutively recruited patients with TLE undergoing preoperative evaluation for epilepsy surgery. A complex visual scene encoding task known to activate mesial temporal structures was used during fMRI. Asymmetry ratios for mesial temporal activation were calculated, using regions of interest defined in normals. Patient findings were compared with the results of IAT performed as part of routine clinical evaluation. Results: Task activation was nearly symmetric in normal subjects, whereas in patients with TLE, significant asymmetries were observed. In all nine patients in whom the IAT result was interpretable, memory asymmetry by fMRI concurred with the findings of IAT including two patients with paradoxical IAT memory lateralization ipsilateral to seizure focus. Conclusions: fMRI can be used to detect asymmetries in memory activation in patients with TLE. Because fMRI studies are noninvasive and provide excellent spatial resolution for functional activation, these preliminary results suggest a promising role for fMRI in improving the preoperative evaluation for epilepsy surgery.

[1]  S. Ogawa,et al.  Oxygenation‐sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields , 1990, Magnetic resonance in medicine.

[2]  H. Lüders,et al.  Individual patient prediction of seizure lateralization in temporal lobe epilepsy: A comparison between neuropsychological memory measures and the Intracarotid Amobarbital Procedure , 1997, Journal of the International Neuropsychological Society.

[3]  D. Gadian,et al.  Advances in proton magnetic resonance spectroscopy of the brain , 1993 .

[4]  J. B. Demb,et al.  Functional MRI measurement of language lateralization in Wada-tested patients. , 1995, Brain : a journal of neurology.

[5]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[6]  Jerome Engel,et al.  Surgical treatment of the epilepsies , 1993 .

[7]  T. Rasmussen,et al.  INTRACAROTID INJECTION OF SODIUM AMYTAL FOR THE LATERALIZATION OF CEREBRAL SPEECH DOMINANCE EXPERIMENTAL AND CLINICAL OBSERVATIONS , 1960 .

[8]  T. Rasmussen,et al.  Rasmussen's encephalitis and the new hat , 1996, Neurology.

[9]  J. A. Frost,et al.  Determination of language dominance using functional MRI , 1996, Neurology.

[10]  M. D’Esposito,et al.  Empirical Analyses of BOLD fMRI Statistics , 1997, NeuroImage.

[11]  J. A. Detre,et al.  The Effect of Pacing of Experimental Stimuli on Observed Functional MRI Activity , 1997, NeuroImage.

[12]  Karl Magnus Petersson,et al.  A Dynamic Role of the Medial Temporal Lobe during Retrieval of Declarative Memory in Man , 1997, NeuroImage.

[13]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[14]  W H Theodore,et al.  Functional mapping of human memory using PET: comparisons of conceptual and perceptual tasks. , 1996, Canadian journal of experimental psychology = Revue canadienne de psychologie experimentale.

[15]  G H Glover,et al.  Separate neural bases of two fundamental memory processes in the human medial temporal lobe. , 1997, Science.

[16]  Leslie G. Ungerleider,et al.  Object and spatial visual working memory activate separate neural systems in human cortex. , 1996, Cerebral cortex.

[17]  D. Zaidel,et al.  Effects of semantic organization on the recognition of pictures following temporal lobectomy , 1981, Neuropsychologia.

[18]  F. Craik,et al.  Novelty and familiarity activations in PET studies of memory encoding and retrieval. , 1996, Cerebral cortex.

[19]  R. Turner,et al.  Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[20]  A. Siegel,et al.  Relationships between MR-imaged total amount of tissue removed, resection scores of specific mediobasal limbic subcompartments and clinical outcome following selective amygdalohippocampectomy , 1990, Epilepsy Research.

[21]  F M Miezin,et al.  Activation of the hippocampus in normal humans: a functional anatomical study of memory. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[22]  Jerome Engel,et al.  Outcome with respect to epileptic seizures. , 1993 .

[23]  L. Squire.  Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. , 1992, Psychological review.

[24]  S. Udenfriend,et al.  Expression cloning of a Na(+)-independent neutral amino acid transporter from rat kidney. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[25]  V S Caviness,et al.  Functional MRI Localization of Language in a 9-Year-Old Child , 1996, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[26]  B L Ehrenberg,et al.  Lateralization of memory for the visual attributes of objects , 1994, Neurology.

[27]  A. Saykin,et al.  Predictors of outcome after anterior temporal lobectomy , 1994, Neurology.

[28]  M. D’Esposito,et al.  The parahippocampus subserves topographical learning in man , 1996, NeuroImage.

[29]  J. R. Baker,et al.  The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[30]  R. Gur,et al.  Neuropsychological Changes after Anterior Temporal Lobectomy Acute Effects on Memory, Language, and Music , 1992 .

[31]  J. A. Frost,et al.  Functional MRI demonstrates left medial temporal lobe activation during verbal episodic memory encoding , 1996, NeuroImage.

[32]  P. Doubilet,et al.  Improved prediction of intrauterine growth retardation with use of multiple parameters. , 1988, Radiology.

[33]  R. S. J. Frackowiak,et al.  The Activity in Human Areas V1/V2, V3, and V5 during the Perception of Coherent and Incoherent Motion , 1996, NeuroImage.

[34]  John R. Hodges,et al.  Progressive prosopagnosia associated with selective right temporal lobe atrophy. A new syndrome? , 1995, Brain : a journal of neurology.

[35]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited—Again , 1995, NeuroImage.

[36]  Gregory P. Lee,et al.  Wada memory performance predicts seizure outcome following anterior temporal lobectomy , 1994, Neurology.

[37]  E C Wong,et al.  Processing strategies for time‐course data sets in functional mri of the human brain , 1993, Magnetic resonance in medicine.

[38]  M. D’Esposito,et al.  Empirical Analyses of BOLD fMRI Statistics , 1997, NeuroImage.

[39]  J. G. Snodgrass,et al.  Pragmatics of measuring recognition memory: applications to dementia and amnesia. , 1988, Journal of experimental psychology. General.

[40]  L. Squire,et al.  The medial temporal lobe memory system , 1991, Science.

[41]  T. Hammeke,et al.  Functional Magnetic Resonance Imaging in Partial Epilepsy , 1994, Epilepsia.

[42]  M. Weinand,et al.  Surface cortical cerebral blood flow monitoring and single photon emission computed tomography: prognostic factors for selecting temporal lobectomy candidates , 1994, Seizure.

[43]  M. D’Esposito,et al.  Empirical analyses of BOLD fMRI statistics. I. Spatially unsmoothed data collected under null-hypothesis conditions. , 1997, NeuroImage.

[44]  Leslie G. Ungerleider,et al.  Changes in limbic and prefrontal functional interactions in a working memory task for faces. , 1996, Cerebral cortex.

[45]  Brenda Milner,et al.  Memory for different aspects of complex visual scenes after unilateral temporal- or frontal-lobe resection , 1993, Neuropsychologia.

[46]  C. Jack,et al.  Selective posterior cerebral artery Amytal test for evaluating memory function before surgery for temporal lobe seizure. , 1988, Radiology.

[47]  Karl J. Friston,et al.  Activation of Human Hippocampal Formation During Memory for Faces: A Pet Study , 1995, Cortex.

[48]  Ravi S. Menon,et al.  Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[49]  D. Spencer,et al.  Surgery for epilepsy. , 1985, Neurologic clinics.

[50]  Andrew J. Saykin,et al.  Neural organization of material-specific memory functions in temporal lobe epilepsy patients as assessed by the intracarotid amobarbital test. , 1995 .