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EPILEPSY AND MEMORY David M. Treiman, M.D. Barrow Neurological Institute Phoenix, Arizona

EPILEPSY AND MEMORY David M. Treiman, M.D. Barrow Neurological Institute Phoenix, Arizona. “. . . The commonest failure is loss of memory and that this, if regarded in all degrees, is more frequent than the integrity of that faculty.”

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EPILEPSY AND MEMORY David M. Treiman, M.D. Barrow Neurological Institute Phoenix, Arizona

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  1. EPILEPSY AND MEMORYDavid M. Treiman, M.D.Barrow Neurological InstitutePhoenix, Arizona

  2. “. . . The commonest failure is loss of memory and that this, if regarded in all degrees, is more frequent than the integrity of that faculty.” - J. Russell Reynolds, 1861Epilepsy: its symptoms, treatment and relation to other chronic convulsive diseases. London: John Churchill

  3. Epileptic Seizure Epilepsy A clinical manifestation of a transient, usually hypersynchronous, abnormal electrical discharge in the brain, consisting of sudden and transitory abnormal behavioral phenomena (alterations of consciousness, motor, sensory, autonomic, or psychic events). A neurological disorder characterized by recurrent non-provoked epileptic seizures.

  4. Epileptic SeizureGeneric description • Abrupt onset • Impaired consciousness during event • Amnesia for the event and part of the post-ictal period • Post-ictal depressed consciousness, with gradual recovery

  5. Epilepsy & MemoryIssues for consideration • Ictal amnesia & fugue states • Post-ictal amnesia • Inter-ictal memory deficits

  6. Hx. of Concepts of Memory • Unitary memory • Multiple memory systems • Franz Joseph Gall & phrenology • Maine de Biran • Representative memory - recollection of ideas & events • Mechanical memory - acquisition of habits & skills • Sensitive memory - memory for feelings • 19th C neurologists - memory centers • 1st half of 20th C - back to unitary memory • Post WWII - multiple memory systems again • Much of renewed interest stimulated by case of H.M.

  7. Case of H.M. • 27 yo motor winder, hs grad, szs since age 10 • Possible TBI age 9, nl PEG x2, EEGs non-focal • 9/53 bilateral MT resections, posterior to 8 cm • Post-op no neuro deficit, except memory: • little ability to retain & recollect new information across a delay • no difficulty with immediate or short term retention • could learn new motor skills • remote memories retained • FSIQ 112 (vs 104 pre-op) • Szs persisted, but much less severe & frequent Scoville & Milner, J Neurol Neurosurg Psychiat 20:11, 1957

  8. H.M. Control A amygdala H hippocampus cs calcarine sulcus MMN medial mammillary nucleus EC entorhinal cortex PR perirhinal cortex Post-op MRI from H.M. & Control Corkin et al., J Neurosci 17:3964, 1977

  9. Human Memory SystemsDeclarative or explicit memory: recall • Episodic memory (remembering) • the explicit recollection of incidents that occurred at a particular time and place in one’s personal past • mesial TL damage: impairs new acquisition • prefrontal cortex: impairment of recall of temporal order and of source (when, where) • Semantic memory (knowing) • general knowledge, not linked to time or place • mesial TL damage: impairs new acquisition

  10. Human Memory SystemsNondeclarative or implicit memory: unconscious, no active recall • Perceptual Representation System • Identification of words and objects based on their form and structure, but not their meaning. • Presemantic - not involved in associative or conceptual information, i.e., meaning or function. • Three major subsystems: • visual word form • auditory word form • structural description - relations between parts that determines global structure (what it is). • Not mediated by mesial temporal lobe

  11. Human Memory SystemsImplicit • Procedural memory • Acquisition of skills and habits (knowing how) • Acquired gradually through repetitive practice (e.g., athletes, musicians • Not dependent on mesial temporal structures • Cortical striate system critical (HD patients poor at learning new motor skills, altho intact explicit mem.) • Cerebellum necessary for sequences of movements

  12. Human Memory Systems • Working memory • short term retention over a period of seconds • way of holding information on-line in service of comprehending, reasoning, problem solving • Three components: • phonological loop - allows recycling of speech-based information - left parietal supramarginal gyrus • visuaospatial sketch pad - short-term retention of visual and spatial information - several sites right hemisphere • central executive or limited capacity work space - prefrontal cortex

  13. Summary of Memory • Explicit memory systems (both episodic and semantic memory) require intact temporal lobe, and thus are at risk in temporal lobe epilepsy. • Implicit memory systems (perceptual representation system, procedural memory, working memory) are localized outside of the mesial temporal lobe, and thus not at risk in temporal lobe epilepsy.

  14. What is the evidence for memory impairment in temporal lobe epilepsy?

  15. Interictal memory deficits • Physician impression • Russell Reynolds’ observation (1861) • Lennox (1942): “…the patient finds it hard to recall events and names, especially those learned recently.” • Loiseau et al. (1988): “…memory deficits in epileptic patients merit special attention since they seek help for these more frequently than for other mental impairments.” • Self-reports of patients • Neuropsychological testing of memory • Many reports, especially in TLE

  16. Factors that may increase riskSummary of older studies • Identified etiology (risk from underlying disorder) • Seizure type (TLE for reasons already cited) • Age of onset/duration of epilepsy • Frequency and severity of seizures • “Ictal time” • Highly disordered EEG • Antiepileptic drugs

  17. Is neuronal damage progressive in chronic intractable epilepsy?

  18. Impairment of hippocampal-dependent spatial memory after SE • Abundant evidence from experimental studies • Scoville & Milner 1957, Morris et al. 1982, Holmes et al. 1988, Stafstrom et al. 1993, Nissinen et al 2000 • Rutten et al 2002 studied development of SE-induced cognitive dysfunction in immature rats • SE induced by Li/pilo age P20 • Water maze performance at P22,P25, P30,P50 • P50 rats exposed to nonenriched or enriched envir. • Water maze performance compared between control and SE rats and in SE rats between environments

  19. Water maze escape latenciesSE at P22, testing P22-50 Rutten et al. Eur J Neurosci 16:501, 2002 * P<0.05; **P<0.01; ***P<0.001

  20. Enriched EnvironmentToys, moving objects, classical music Rutten et al. Eur J Neurosci 16:501, 2002

  21. Effect of enriched environment on water maze escape latency * P<0.05; **P<0.01 Rutten et al. Eur J Neurosci 16:501, 2002

  22. CA3 cell loss Control, P30 SE rat, P30 Supra- granular sprouting SE-induced hippocampal damage Rutten et al. Eur J Neurosci 16:501, 2002

  23. To what extent is memory task- specific in the MT lobes?

  24. Correlations with task specific declarative memory (L > R) • Hippocampal sclerosis • Hippocampal neuronal density • Hippocampal volume • Hippocampal N-acetylaspartate/creatine ratios • NAA/Cr better correlated than volume

  25. MRI, Cr/NAA, Verbal Memory LM% - logical memory percentage retention Cr - creatine NAA - N-acetylaspartate Sawrie et al., Epilepsia 42:1403, 2002

  26. Memory & MRI volumes Pegna et al., Eur Neurol 47:148, 2001

  27. Surgical Treatment of Epilepsy • Types of procedures: • ATL; selective amygdalohippocampectomy • 70% to 90% seizure free • Focal cortical resections • Corpus Callosotomy • Hemispherectomy • Evaluation: • Scalp vido-EEG monitoring to localize seizure onset • Invasive monitoring • depth wire electrodes • intracranial grid electrodes

  28. Risk of TL Surgery to memory • Case of H.M. (cited 1744 times through 2001) • Two cases w/ right MTL EEG s and amnesia after LT lobectomy w/ lg hippocampal removal • Penfield & Milner, 1958 • Right MTL pathology verified at autopsy • Penfield & Mathieson, 1974 • Subsequent reports by others of memory deficits after unilateral TL lobectomy with contralateral pathology

  29. Corkin Nat Rev Neurosci 3:153, 2002

  30. Intracarotid Na+ AmobarbitalWada Test • Wada (1949) used intracarotid Amytal to assess lateralization of speech dominance • Milner et al. (1962) modified Wada test to study memory competence • Now used routinely for pre-operative assessment of patients in whom TL lobectomy or selective amygdalo-hippocampectomy is planned

  31. IAP Protocol • Transfemoral cerebral angiogram to evaluate vascular anatomy/degree of cross-flow • Arms are elevated, patient counts backward from 20 • Amytal injected by hand (usually 100-125 mg) until contralateral arm drops and slowing is seen on EEG • Memory items presented and patient asked to name them to assess language • Memory tested after drug effect is gone, assessed by normalization of behavior & EEG

  32. UCLA IAP Experience IAP result Amnesia No # of present amnesia surgeries Positive 1 0 1* Negative 0 214 214 * A total of four patients had positive IAP results, but only one underwent hippocampal removal Rauch Epi Res Suppl 5:77, 1992

  33. Risk to verbal memory after ATLSRB scores in patients with R & L HS Left ATL N = 68 Right ATL N = 47 Martin et.al., Arch Neurol 59:1895, 2002

  34. Lateralized topographic & memory deficits in temporal lobectomy patients Left ATL (N= 13) Right ATL (N = 17) Spiers et al., Brain 123:2476, 2001

  35. Comparison of IAT & fMRI in memory lateralization Golhy et al., Epilepsia 43:855, 2002

  36. Memory-activated fMRI lateralizes TLE Mean left-right asymmetry ratios Jokeit et al, Neurology 57:1786, 2001

  37. Memory-activated fMRI lateralizes TLE Mean # activated voxels in controls & TLE Jokeit et al, Neurology 57:1786, 2001

  38. Memory-activated fMRI lateralizes TLE Scatterplot # activated pixels L MTL vs R MTL  RIGHT TLE  LEFT TLE Jokeit et al, Neurology 57:1786, 2001

  39. Memory-activated fMRI lateralizes TLE Representative examples L TLE & R TLE 31 yo F w/ left HS 34 yo M w/ right T/L cavernoma Jokeit et al, Neurology 57:1786, 2001

  40. Follow-up on HM • Now 76 years old • Continues to be unable to acquire new memories • Intelligence normal and no deficits in perception, abstract thinking, reasoning • Language ok: can repeat & transform sentences with complex syntax, get the point of jokes, even those turning on semantic ambiguity • Social behavior appropriate & courteous • Original 1957 paper cited 1744 times thru 2002 • Physically still in good health, except mobility markedly reduced from osteoporosis as a complication of chronic long-term PHT • Brain will be examined when H.M. dies

  41. SUMMARY • Memory problems associated with epilepsy have been recognized for > 150 years • Unitary vs multiple memory systems considered; case of HM renewed interest in multiple memory systems • Current thinking: • Explicit memory systems (both episodic and semantic memory) require intact temporal lobe, and thus are at risk in temporal lobe epilepsy. • Implicit memory systems (perceptual representation system, procedural memory, working memory) are localized outside of the mesial temporal lobe, and thus not at risk in temporal lobe epilepsy.

  42. SUMMARY • Many reports of memory deficits in TLE • Suggestion of progressive deficits, but evidence is limited • Abundant animal data, especially from SE studies • Memory deficits may be at least partially task-specific • Unilateral temporal lobectomy 70% - 90% success, but need to avoid disasters of memory impairment • Wada test useful in lateralizing language, memory • fMRI shows promise to replace Wada test (IAT) • Suggestion of progressive deficits emphasize importance of early consideration for TL, if TLE is refractory to AEDs

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