Advertisement

Accelerated long-term forgetting: A newly identified memory impairment in epilepsy

      Abstract

      Recently, a pattern referred to as accelerated long-term forgetting (ALF) has been described in patients with epilepsy. In ALF, acquisition and retention over standard delayed recall intervals (up to 30 minutes) tend to be intact, but there is an abnormally rapid rate of forgetting over delays of days or weeks. ALF is associated with everyday memory complaints as well as impairments in autobiographical memory, but goes largely undetected by traditional neuropsychological measures. We consider here the characteristics of ALF and possible contributors to its underlying pathophysiology. Overall, a better understanding of this relatively newly recognised memory disorder should improve clinical treatment.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Journal of Clinical Neuroscience
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Thompson P.
        • Corcoran R.
        Everyday memory failures in people with epilepsy.
        Epilepsia. 1992; 33: S18-20
      1. Milner B. Psychological aspects of focal epilepsy and its neurosurgical management. Raven Press, New York1975
        • Miller L.A.
        • Munoz D.G.
        • Finmore M.
        Hippocampal sclerosis and human memory.
        Arch Neurol. 1993; 50: 391-394
        • Sass K.
        • Spencer D.
        • Kim J.
        • et al.
        Verbal memory impairment correlates with hippocampal pyramidal cell density.
        Neurology. 1990; 40: 1694-1697
        • Milner B.
        Complementary functional specializations of the human cerebral hemispheres.
        in: Levi-Montalcini R. Nerve cells, transmitters and behaviour. Pontificia Academia Scientiarum, Vatican City, Italy1980: 601-625
        • Miller L.A.
        • Lai R.
        • Munoz D.G.
        Contributions of the entorhinal cortex, amygdala and hippocampus to human memory.
        Neuropsychologia. 1998; 36: 1247-1256
        • Smith M.L.
        • Milner B.
        Right hippocampal impairment in the recall of spatial location: encoding deficit or rapid forgetting?.
        Neuropsychologia. 1989; 27: 71-81
        • Butler C.R.
        • Graham K.S.
        • Hodges J.R.
        • et al.
        The syndrome of transient epileptic amnesia.
        Ann Neurol. 2007; 61: 587-598
        • Manes F.
        • Graham K.S.
        • Zeman A.
        • et al.
        Autobiographical amnesia and accelerated forgetting in transient epileptic amnesia.
        J Neurol Neurosurg Psychiatry. 2005; 76: 1387-1391
        • Kapur N.
        • Millar J.
        • Colbourn C.
        • et al.
        Very long-term amnesia in assoication with temporal lobe epilpesy: evidence for multiple-stage consolidation processes.
        Brain Cognit. 1997; 35: 58-70
        • Kapur N.
        • Scholey K.
        • Moore E.
        • et al.
        Long-term retention deficits in two cases of disproportionate retrograde amnesia.
        J Cogn Neurosci. 1996; 8: 416-435
        • Mayes A.
        • Isaac C.
        • Holdstock J.
        • et al.
        Long-term amnesia: a review and detailed illustrative case study.
        Cortex. 2003; 39: 567-603
        • Bengner T.
        • Malina T.
        • Lindenau M.
        • et al.
        Face memory in MRI-positive and MRI-negative temporal lobe epilepsy.
        Epilepsia. 2006; 47: 1904-1914
        • Djordjevic J.
        • Smith M.L.
        • Sziklas V.
        • et al.
        The Story Learning and Memory (SLAM) test: equivalence of three forms and sensitivity to left temporal lobe dysfunction.
        Epilepsy Behav. 2011; 20: 518-523
        • Martin R.C.
        • Loring D.W.
        • Meador K.J.
        • et al.
        Impaired long-term retention despite normal verbal learning in patients with temporal lobe dysfunction.
        Neuropsychology. 1991; 5: 3-12
        • Muhlert N.
        • Milton F.
        • Butler C.R.
        • et al.
        Accelerated forgetting of real-life events in Transient Epileptic Amnesia.
        Neuropsychologia. 2010; 48: 3235-3244
        • O’Connor M.
        • Sieggreen M.A.
        • Ahern G.
        • et al.
        Accelerated forgetting in association with temporal lobe epilepsy and paraneoplastic encephalitis.
        Brain Cogn. 1997; 35: 71-84
        • Lucchelli F.
        • Spinnler H.
        Ephemeral new traces and evaporated remote engrams: a form of neocortical temporal lobe amnesia? A preliminary case report.
        Neurocase. 1998; 4: 447-459
        • Fitzgerald Z.
        • Thayer Z.
        • Mohamed A.
        • et al.
        Examining factors related to accelerated long-term forgetting in epilepsy using ambulatory EEG monitoring.
        Epilepsia. 2013; 54: 819-827
        • Cronel-Ohayon S.
        • Zesiger P.
        • Davidoff V.
        • et al.
        Deficit in memory consolidation (abnormal forgetting rate) in childhood temporal lobe epilepsy: pre and postoperative long-term observation.
        Neuropediatrics. 2006; 37: 317-324
        • De Renzi E.
        • Lucchelli F.
        Are semantic systems separately represented in the brain? The case living category impairment.
        Cortex. 1994; 30: 3-25
        • Holdstock J.
        • Mayes A.
        • Isaac C.
        • et al.
        Differential involvement of the hippocampus and temporal lobe cortices in rapid and slow learning of new semantic information.
        Neuropsychologia. 2002; 40: 748-768
        • Jansari A.S.
        • Davis K.
        • McGibbon T.
        • et al.
        When “long-term memory” no longer means “forever”: analysis of accelerated long-term forgetting in a patient with temporal lobe epilepsy.
        Neuropsychologia. 2010; 48: 1707-1715
        • Smith C.N.
        • Frascino J.C.
        • Kripke D.J.
        • et al.
        Losing memories overnight: a unique form of human amnesia.
        Neuropsychologia. 2010; 48: 2833-2840
        • Kemp S.
        • Illman N.A.
        • Moulin C.J.
        • et al.
        Accelerated long-term forgetting (ALF) and transient epileptic amnesia (TEA): two cases of epilepsy-related memory disorder.
        Epilepsy Behav. 2012; 24: 382-388
        • Gallassi R.
        • Sambati L.
        • Poda R.
        • et al.
        Accelerated long-term forgetting in temporal lobe epilepsy: evidence of improvement after left temporal pole lobectomy.
        Epilepsy Behav. 2011; 22: 793-795
        • McGibbon T.
        • Jansari A.S.
        Detecting the onset of accelerated long-term forgetting: evidence from temporal lobe epilepsy.
        Neuropsychologia. 2013; 51: 114-122
        • Butler C.R.
        • Zeman A.Z.
        Recent insights into the impairment of memory in epilepsy: transient epileptic amnesia, accelerated long-term forgetting and remote memory impairment.
        Brain. 2008; 131: 2243-2263
        • Bell B.
        WMS-III logical memory performance after a two-week delay in temporal lobe epilepsy and control groups.
        J Clin Exp Neuropsychol. 2006; 28: 1435-1443
        • Bell B.
        • Fine J.
        • Dow C.
        • et al.
        Temporal lobe epilepsy and the selective reminding test: the conventional 30-minute delay suffices.
        Psychol Assess. 2005; 17: 103-109
        • Blake R.V.
        • Wroe S.J.
        • Breen E.K.
        • et al.
        Accelerated forgetting in patients with epilepsy: evidence for an impairment in memory consolidation.
        Brain. 2000; 123: 472-483
        • Giovagnoli A.R.
        • Casazza M.
        • Avanzini G.
        Visual learning on a selective reminding procedure and delayed recall in patients with temporal lobe epilepsy.
        Epilepsia. 1995; 36: 704-711
        • Helmstaedter C.
        • Hauff M.
        • Elger C.E.
        Ecological validity of list-learning on a selective reminding procedure and self-reported memory in healthy individuals and those with temporal lobe epilepsy.
        J Clin Exp Neuropsychol. 1998; 20: 365-375
        • Mameniskiene R.
        • Jatuzis D.
        • Kaubrys G.
        • et al.
        The decay of memory between delayed and long-term recall in patients with temporal lobe epilepsy.
        Epilepsy Behav. 2006; 8: 278-288
        • Wilkinson H.
        • Holdstock J.S.
        • Baker G.
        • et al.
        Long-term accelerated forgetting of verbal and non-verbal information in temporal lobe epilepsy.
        Cortex. 2011; 48: 317-332
        • Tramoni E.
        • Felician O.
        • Barbeau E.J.
        • et al.
        Long-term consolidation of declarative memory: insight from temporal lobe epilepsy.
        Brain. 2011; 134: 816-831
        • Deak M.C.
        • Stickgold R.
        • Pietras A.C.
        • et al.
        The role of sleep in forgetting in temporal lobe epilepsy: a pilot study.
        Epilepsy Behav. 2011; 21: 462-466
        • Narayanan J.
        • Duncan R.
        • Greene J.
        • et al.
        Accelerated long-term forgetting in temporal lobe epilepsy: verbal, nonverbal and autobiographical memory.
        Epilepsy Behav. 2012; 25: 622-630
        • Muhlert N.
        • Grunewald R.A.
        • Hunkin N.M.
        • et al.
        Accelerated long-term forgetting in temporal lobe but not idiopathic generalised epilepsy.
        Neuropsychologia. 2011; 49: 2417-2426
        • Puetz J.
        • Grohmann S.
        • Metternich B.
        • et al.
        Impaired memory consolidation during sleep in patients with functional memory disorder.
        Biol Psychol. 2011; 86: 31-38
        • Lah S.
        • Meierotto E.
        • Diamond K.
        • et al.
        Autobiographical memory in patients with partial epilepsy: impact of accelerated forgetting.
        J Int Neuropsychol Soc. 2009; 15: 58
        • Midorikawa A.
        • Kawamura M.
        Recovery of long-term anterograde amnesia, but not retrograde amnesia, after initiation of an anti-epileptic drug in a case of transient epileptic amnesia.
        Neurocase. 2007; 13: 385-389
        • Bergin P.S.
        • Thompson P.J.
        • Fish D.R.
        • et al.
        The effect of seizures on memory for recently learned material.
        Neurology. 1995; 45: 236-240
      2. Fitzgerald Z, Thayer Z, Mohamed A, et al. Accelerated long-term forgetting in epilepsy: using ambulatory EEG monitoring to determine the pathophysiology. Combined Abstracts of 2011 Australian Psychology Conferences 2011: 274.

        • Jokeit H.
        • Daamen M.
        • Zang H.
        • et al.
        Seizures accelerate forgetting in patients with left-sided temporal lobe epilepsy.
        Neurology. 2001; 57: 125-126
        • Binnie C.D.
        Cognitive impairment during epileptiform discharges: is it ever justifiable to treat the EEG?.
        Lancet Neurol. 2003; 2: 725-730
        • Zeman A.
        • Boniface S.J.
        • Hodges J.R.
        Transient epileptic amnesia: a description of the clinical, and neuropsychological features in 10 cases and a review of the literature.
        J Neurol Neurosurg Psychiatry. 1998; 64: 435-443
        • Holmes G.L.
        • Lenck-Santini P.P.
        Role of interictal epileptiform abnormalities in cognitive impairment.
        Epilepsy Behav. 2006; 8: 504-515
        • Fitzgerald Z.
        • Thayer Z.
        • Mohamed A.
        • et al.
        Examining factors related to accelerated long-term forgetting in epilepsy using ambulatory EEG monitoring.
        Epilepsia. 2013; 54: 819-827
        • Gascoigne M.B.
        • Barton B.
        • Webster R.
        • et al.
        Accelerated long-term forgetting in children with idiopathic generalized epilepsy.
        Epilepsia. 2012; 53: 2135-2140
        • Davidson M.
        • Dorris L.
        • O’Regan M.
        • et al.
        Memory consolidation and accelerated forgetting in children with idiopathic generalised epilepsy.
        Epilepsy Behav. 2007; 11: 394-400
        • Motamedi G.K.
        • Meador K.J.
        Antiepileptic drugs and memory.
        Epilepsy Behav. 2004; 5: 435-439
        • Lah S.
        • Lee T.
        • Grayson S.
        • et al.
        Effects of temporal lobe epilepsy on retrograde memory.
        Epilepsia. 2006; 47: 615-625
        • Butler C.R.
        • Bhaduri A.
        • Acosta-Cabronero J.
        • et al.
        Transient epileptic amnesia: regional brain atrophy and its relationship to memory deficits.
        Brain. 2009; 132: 357-368
        • Lah S.
        • Mohamed A.
        • Thayer Z.
        • et al.
        Accelerated long-term forgetting of verbal information in patients with temporal and extratemporal partial epilepsy.
        J Int Neuropsyhcol Soc. 2012; 18: 64-65
        • Lopez-Gomariz E.
        • Hoyo-Rodrigo B.
        • Rodrigues-Nieto I.
        The effects of epileptic seizures on sleep architecture.
        Rev Neurol. 2004; 38: 176-180
        • Diekelmann S.
        • Wilhelm I.
        • Born J.
        The whats and whens of sleep-dependent memory consolidation.
        Sleep Med Rev. 2009; 13: 309-321
        • Ellenbogen J.M.
        • Hulbert J.C.
        • Stickgold R.
        • et al.
        Interfering with theories of sleep and memory: sleep, declarative memory, and associative interference.
        Curr Biol. 2006; 16: 1290-1294
        • Gais S.
        • Born J.
        Declarative memory consolidation: mechanisms acting during human sleep.
        Learn Mem. 2004; 11: 679-685
        • Ficca G.
        • Lombardo P.
        • Rossi L.
        • et al.
        Morning recall of verbal material depends on prior sleep organization.
        Behav Brain Res. 2000; 112: 159-163
        • Bell B.
        • Giovagnoli A.R.
        Recent innovative studies of memory in temporal lobe epilepsy.
        Neuropsychol Rev. 2007; 17: 455-476
        • Ho J.
        • Epps A.
        • Parry L.
        • et al.
        Rehabilitation of everyday memory deficits in paediatric brain injury: self-instruction and diary training.
        Neuropsychol Rehabil. 2011; 21: 183-207
        • Radford K.
        • Lah S.
        • Thayer Z.
        • et al.
        Effective group-based memory training for patients with epilepsy.
        Epilepsy Behav. 2011; 22: 272-278
        • Helmstaedter C.
        • Loer B.
        • Wohlfahrt R.
        • et al.
        The effects of cognitive rehabilitation on memory outcome after temporal lobe epilepsy surgery.
        Epilepsy Behav. 2008; 12: 402-409
        • Engelberts N.H.
        • Klein M.
        • Ader H.J.
        • et al.
        The effectiveness of cognitive rehabilitation for attention deficits in focal seizures: a randomized controlled study.
        Epilepsia. 2002; 43: 587-595
        • Dewar M.
        • Alber J.
        • Butler C.
        • et al.
        Brief wakeful resting boosts new memories over the long term.
        Psychol Sci. 2012; 23: 955-960