Working memory in temporal lobe epilepsy: an event-related potential study.

Event-related potentials (ERPs) were recorded to a digit-probe identification and matching task (modified 'Sternberg paradigm') in 29 patients with temporal lobe epilepsy (TLE) and 26 healthy subjects. Our main aim was to identify the neurophysiological correlates of abnormal short term memory function in patients with TLE. Neuropsychological tests allowed the definition and comparison of two patient groups according to the presence or absence of memory dysfunction. These two groups did not differ significantly in mean age, education years, IQ, seizure duration, seizure frequency, anti-epileptic drug (AED) regimes, or on findings on neuroimaging. ERPs recorded under different levels of memory load were analysed both by conventional component identification and by an objective computer method of determining mean amplitudes of multiple 50 ms epochs (MMA analysis). We found that some significant abnormalities were common to both groups of patients; these included slow reaction times, a reduced amplitude of the N170 wave (and the corresponding 157-210 ms epoch in the MMA analysis) and a broad late negative shift between 577 and 735 ms. Other findings, including a significantly reduced performance accuracy as the level of memory load increased, were restricted to patients with abnormal memory function. The ERP changes that were specific to these patients occurred within a latency band of 200-420 ms and included a relatively preserved, but delayed P250 component and a delayed and attenuated N290 wave. When compared with either healthy subjects or with patients with normal memory, the responses in patients with abnormal memory showed an abnormal 'positive shift' between 262 and 315 ms after probe presentation and a further positive shift between 315 and 420 ms as memory load increased. These abnormalities of 'memory scanning' ERPs in patients with TLE which paralleled neuropsychological and behavioural evidence of memory dysfunction, and which occurred in the section of the response that is sensitive to memory loading in healthy subjects, provide further objective evidence that abnormalities of short term memory processes contribute to the memory deficits of TLE.

[1]  N. Adam,et al.  Late components of the visual evoked potential to search in short-term memory. , 1978, Electroencephalography and clinical neurophysiology.

[2]  G. Stores,et al.  Inattentiveness in Schoolchildren with Epilepsy , 1978, Epilepsia.

[3]  C D Binnie,et al.  Selective cognitive impairment during focal and generalized epileptiform EEG activity. , 1984, Brain : a journal of neurology.

[4]  R. Elwes,et al.  A Comparative Study of the Cognitive Effects of Phenytoin and Carbamazepine in New Referrals with Epilepsy , 1986, Epilepsia.

[5]  C. C. Wood,et al.  The ɛ-Adjustment Procedure for Repeated-Measures Analyses of Variance , 1976 .

[6]  P. Loiseau,et al.  Learning Impairment in Epileptic Patients , 1983, Epilepsia.

[7]  R. Bornstein,et al.  WAIS‐R Factor Structure in Epileptic Patients , 1988, Epilepsia.

[8]  W Ritter,et al.  Event-related brain potential evidence for a verbal working memory deficit in multiple sclerosis. , 1994, Brain : a journal of neurology.

[9]  C C Wood,et al.  Intracranial recordings of endogenous ERPs in humans. , 1985, Electroencephalography and clinical neurophysiology. Supplement.

[10]  M. Onofrj,et al.  P3 recordings in patients with bilateral temporal lobe lesions , 1992, Neurology.

[11]  M. Shenton,et al.  Electrical source analysis of auditory ERPs in medial temporal lobe amnestic syndrome. , 1993, Electroencephalography and clinical neurophysiology.

[12]  D. Master,et al.  Memory selectivity and unilateral cerebral dysfunction , 1986, Psychological Medicine.

[13]  L. Pelosi,et al.  Is "memory-scanning" time in the Sternberg paradigm reflected in the latency of event-related potentials? , 1995, Electroencephalography and clinical neurophysiology.

[14]  J. Ford,et al.  Event-related potentials recorded from young and old adults during a memory retrieval task. , 1979, Electroencephalography and clinical neurophysiology.

[15]  A. D. Fisk,et al.  The effects of practice and task structure on components of the event-related brain potential. , 1986, Psychophysiology.

[16]  H Pratt,et al.  Brain potentials in a memory-scanning task. III. Potentials to the items being memorized. , 1989, Electroencephalography and clinical neurophysiology.

[17]  Memory Disorders: Research and Clinical Practice , 1991 .

[18]  H Pratt,et al.  Brain potentials in a memory-scanning task. I. Modality and task effects on potentials to the probes. , 1989, Electroencephalography and clinical neurophysiology.

[19]  B. Rockstroh.  Slow cortical potentials and behavior , 1989 .

[20]  L. Pelosi,et al.  Abnormalities of early "memory-scanning" event-related potentials in patients with temporal lobe epilepsy. , 1994, Behavioural neurology.

[21]  D. Wechsler.  A Standardized Memory Scale for Clinical Use , 1945 .

[22]  E. Halgren,et al.  Brain generators of evoked potentials: the late (endogenous) components. , 1982, Bulletin of the Los Angeles neurological societies.

[23]  R. Mattson,et al.  Gist Recall in Temporal Lobe Seizure Patients (A Study Of Adaptive Memory Skills) , 1988, Cortex.

[24]  H L Hamburger,et al.  Cognition in epilepsy: a multichannel event related potential (P300) study , 1992, Acta neurologica Scandinavica.

[25]  L D Blumhardt,et al.  Event-related potential (ERP) correlates of performance of intelligence tests. , 1992, Electroencephalography and clinical neurophysiology.

[26]  N. Motomura,et al.  Event‐related potential (P300) in epilepsy , 1990, Acta neurologica Scandinavica.

[27]  Richard S. J. Frackowiak,et al.  The neural correlates of the verbal component of working memory , 1993, Nature.

[28]  D. Benson,et al.  Interictal memory and language impairment in temporal lobe epilepsy , 1980, Neurology.

[29]  E. Warrington,et al.  Cognitive impairment in patients with clinically isolated lesions of the type seen in multiple sclerosis. A psychometric and MRI study. , 1989, Brain : a journal of neurology.

[30]  C. Dodrill.  Neuropsychological aspects of epilepsy. , 1992, The Psychiatric clinics of North America.

[31]  R. Bornstein,et al.  Effects of seizure type and waveform abnormality on memory and attention. , 1988, Archives of neurology.

[32]  R. Mattson,et al.  Short Term Retention with Lateralized Temporal Lobe Epilepsy , 1986, Cortex.

[33]  L. Deecke,et al.  Localization of brain activity during auditory verbal short-term memory derived from magnetic recordings , 1991, Brain Research.

[34]  M. Drake,et al.  Long-latency auditory event-related potentials in epilepsy. , 1986, Clinical EEG.

[35]  G R Marsh,et al.  Age differences in evoked potential correlates of a memory scanning process. , 1975, Experimental aging research.

[36]  M. Trimble,et al.  Anticonvulsant Drugs and Cognitive Functions , 1982, Epilepsia.

[37]  F. E. Gomer,et al.  Evoked potential correlates of visual item recognition during memory-scanning tasks. , 1976 .

[38]  E. Halgren,et al.  Neuronal activity in the human medial temporal lobe during recognition memory. , 1990, Brain : a journal of neurology.

[39]  M. Kutas,et al.  Electrophysiology of cognitive processing. , 1983, Annual review of psychology.

[40]  H Glowinski,et al.  COGNITIVE DEFICITS IN TEMPORAL LOBE EPILEPSY: An Investigation of Memory Functioning , 1973, The Journal of nervous and mental disease.

[41]  Brenda Milner,et al.  Visual recognition and recall after right temporal-lobe excision in man , 1968 .

[42]  E. Halgren,et al.  Intracerebral potentials to rare target and distractor auditory and visual stimuli. II. Medial, lateral and posterior temporal lobe. , 1995, Electroencephalography and clinical neurophysiology.

[43]  W. Roth,et al.  The contingent negative variation during a memory retrieval task. , 1975, Electroencephalography and clinical neurophysiology.

[44]  C. Matthews,et al.  Effect of Major Motor Seizure Frequency upon Cognitive‐Intellectual Functions in Adults , 1977, Epilepsia.

[45]  Narinder Kapur,et al.  Memory Disorders in Clinical Practice , 1988 .

[46]  A. Puce,et al.  Scalp and Limbic P3 Event‐Related Potentials in the Assessment of Patients with Temporal Lobe Epilepsy , 1991, Epilepsia.

[47]  E Halgren,et al.  Dissociation of recognition memory components following temporal lobe lesions. , 1989, Journal of experimental psychology. Learning, memory, and cognition.

[48]  E. Halgren,et al.  10 Human Endogenous Limbic Potentials: Cross-Modality and Depth/Surface Comparisons in Epileptic Subjects , 1983 .

[49]  R. Johnson,et al.  Auditory and visual P300s in temporal lobectomy patients: evidence for modality-dependent generators. , 1989, Psychophysiology.

[50]  L D Blumhardt,et al.  Wave form variations in auditory event-related potentials evoked by a memory-scanning task and their relationship with tests of intellectual function. , 1992, Electroencephalography and clinical neurophysiology.

[51]  D. Potter,et al.  Normal P300 following extensive damage to the left medial temporal lobe. , 1991, Journal of neurology, neurosurgery, and psychiatry.

[52]  D. Potter,et al.  Event-related potentials related to recognition memory. Effects of unilateral temporal lobectomy and temporal lobe epilepsy. , 1991, Brain : a journal of neurology.

[53]  T. Picton,et al.  The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. , 1987, Psychophysiology.

[54]  A. Starr,et al.  Disordered auditory short-term memory in man and event-related potentials. , 1987, Brain : a journal of neurology.

[55]  M. Trimble.  11. Epilepsy and behaviour , 1991, Epilepsy Research.

[56]  P. Thompson.  Antiepileptic Drugs and Memory , 1992, Epilepsia.

[57]  E. Halgren,et al.  Human medial temporal lobe potentials evoked in memory and language tasks. , 1986, Electroencephalography and clinical neurophysiology.

[58]  K. Meador,et al.  Relationship of limbic evoked potentials to recent memory performance , 1988, Neurology.

[59]  A. Wyler,et al.  Memory Function and Verbal Learning Ability in Patients with Complex Partial Seizures of Temporal Lobe Origin , 1987, Epilepsia.

[60]  D. Wechsler.  Manual for the Wechsler Adult Intelligence Scale. , 1955 .

[61]  H. Begleiter,et al.  A neurophysiologic correlate of visual short-term memory in humans. , 1993, Electroencephalography and clinical neurophysiology.

[62]  C Umiltà,et al.  Hemisphere‐dependent Cognitive Performances in Epileptic Patients , 1979, Epilepsia.