Elsevier

Revue Neurologique

Volume 173, Issues 7–8, July–August 2017, Pages 490-497
Revue Neurologique

Neuropsychology
Long-term memory deficits in temporal lobe epilepsy

https://doi.org/10.1016/j.neurol.2017.06.011Get rights and content

Abstract

Memory complaints and deficits are common in patients with epilepsy, especially temporal lobe epilepsy (TLE), where memory-related brain structures are directly involved in the epileptic process. In recent years, substantial progress has been made in delineating memory impairment in TLE, challenging the traditional neuropsychological approach of the disorder. In particular, several lines of evidence have suggested that, beyond the apparent deficit demonstrable by standardized neuropsychological evaluations, TLE may also negatively interact with long-term memory, producing considerable loss of information of the patient's autobiographical history and an inability to maintain newly acquired information over a period of time. These observations have led to the development of innovative assessment techniques, and prompted a new domain of investigation focused on the relationships between interictal epileptiform activities and the integrity of anatomo-functional systems. The present paper reviews the available evidence for long-term memory deficits in TLE with respect to remote and very long-term memory, and discusses their putative pathophysiological mechanisms and the developing potential strategies to improve memory functioning.

Introduction

Memory complaints and deficits are commonly seen in patients with epilepsy, especially temporal lobe epilepsy (TLE), where memory-related brain structures are directly involved by seizures. Numerous studies and reviews have delineated the clinical neuropsychology of TLE, particularly with respect to lateralization of seizures within the classic visual/verbal memory framework and in comparisons of pre- and post-surgery memory performance, in attempts to reliably predict postsurgical outcomes [1]. The material-specific model of memory relies on the idea that, in right-handers, the left temporal lobe sustains verbal memories, while the right temporal lobe sustains non-verbal memories (for a recent review, see Willment and Golby [2]). However, over the years, neuropsychological and neuroimaging studies have progressively challenged this model. For instance, non-verbal deficits have been less consistently associated with right TLE than verbal memory has been with left TLE, and aberrant lateralization of activation patterns have been demonstrated during material-specific memory tasks in functional neuroimaging studies.

In recent years, additional issues challenging the traditional neuropsychological approach to TLE have emerged. First, the severity of memory complaints has not been consistently captured by standardized neuropsychological assessment, with many TLE patients performing at average levels or above [3]. Standardized memory tests typically assess the ability to retain new information over relatively short (from 20 min to 1 h) delays [4], whereas several lines of evidence suggest that TLE may also interfere with long-term consolidation, with successfully memorized information after short delays progressively fading over periods of days or weeks. Second, paralleling the progress in our understanding of declarative memory organization, the possibility that TLE memory deficits might be analyzed beyond the scope of the verbal/visual dichotomy has been raised [5], leading to the development of complementary assessment paradigms (for reviews, see Bell and Giovagnoli [6] and Butler and Zeman [7]). Finally, characterization of memory impairment in seizure-free patients has stimulated the development of a new area of research, focusing on the relationships between interictal activities and functional deficits.

Thus, the present report reviews all the available evidence on long-term memory deficits in TLE and discusses some of their putative pathophysiological mechanisms, along with potential strategies aimed at optimalizing memory functioning.

Section snippets

Remote memory in TLE

Remote memory deficits can have a considerable impact on psychological well-being and may represent one of the main complaints of TLE sufferers [8]. However, while the ability to acquire new information (anterograde memory) has been investigated in detail in TLE, relatively few studies have focused on remote memory, which is multifaceted, comprising memories encoded in the relatively distant past [7], [9], with episodic and semantic components. Episodic memory is typically autobiographical,

Accelerated forgetting

In “typical” cases of amnesia following brain insults, anterograde memory impairment is usually demonstrated within seconds or minutes of information exposure [39], [40]. Over the past two decades, however, a different pattern of amnesia has been identified in TLE patients, who demonstrate normal learning and retention of information over relatively brief delays, but an accelerated rate of forgetting over days or weeks. This slowly developing form of amnesia, only apparent over extended periods

A role of interictal spikes in memory disturbances?

Interictal spikes (ISs) are defined as high-amplitude (> 50 μV) fast EEG transients usually followed by a slow wave lasting several hundreds of ms. In intracellular recordings, this pattern is associated with an intracellular discharge, a paroxysmal depolarizing shift, characterized by a rapid sequence of fast action potentials superimposed on a slow depolarizing potential. ISs are followed by a refractory period lasting a few seconds and generally attributed to a post-spike inhibitory phenomenon

Impact of AEDs on memory functioning in TLE

Following the onset of treatment, a subjective improvement of memory is sometimes reported [8], [21], [22], but remains inconsistent. With regard to objective measures, few studies have provided direct comparisons of pre- and post-treatment memory performance in TLE. In a study of three TEA patients, a persistent decline in remote autobiographical memory was reported despite full resolution of amnestic seizures [87]. In a subset of our present patients for whom longitudinal data were available,

Impact of a non-pharmacological intervention on memory functioning in TLE

Several non-pharmacological protocols to alleviate the memory disturbances associated with epilepsy have been evaluated. Some studies focusing on psychosocial failures [88], [89], [90] have suggested that generic psychological support or psychotherapy may help to overcome psychosocial handicaps and seizure-related distress [91], [92]. Cognitive rehabilitation targeting specific cognitive impairments has been tried in addition to clinical care. However, the lack of homogeneity in methods of

Conclusion

The present report has reviewed the large body of evidence that TLE produces memory impairment with distinctive characteristics and features, with a particular impact on remote personal memory and very long-term storage of information. This form of memory disorder appears to be closely associated with the anatomical focus of epilepsy, especially in cases originating from MTL structures. Although the pathophysiological mechanisms have yet to be established, the role of interictal activities in

Disclosure of interest

The authors declare that they have no competing interest.

References (96)

  • A.R. Mayes et al.

    Long-term amnesia: a review and detailed illustrative case study

    Cortex

    (2003)
  • M. O’Connor et al.

    Accelerated forgetting in association with temporal lobe epilepsy and paraneoplastic encephalitis

    Brain Cogn

    (1997)
  • L. Manning et al.

    [selective memory impairment for public events associated with accelerated forgetting in a patient with left temporal lobe epilepsy]

    Rev Neurol (Paris)

    (2006)
  • S. Kemp et al.

    Accelerated long-term forgetting (alf) and transient epileptic amnesia (tea): two cases of epilepsy-related memory disorder

    Epilepsy Behav

    (2012)
  • S. Hoefeijzers et al.

    Accelerated long-term forgetting in transient epileptic amnesia: an acquisition or consolidation deficit?

    Neuropsychologia

    (2013)
  • A. Cassel et al.

    Forgetting in temporal lobe epilepsy: when does it become accelerated?

    Cortex

    (2016)
  • M. Dewar et al.

    Impaired picture recognition in transient epileptic amnesia

    Epilepsy Behav

    (2015)
  • A.S. Jansari 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)
  • K. Nader

    Memory traces unbound

    Trends Neurosci

    (2003)
  • Y. Dudai

    Reconsolidation: the advantage of being refocused

    Curr Opin Neurobiol

    (2006)
  • G. Elliott et al.

    Measuring forgetting: a critical review of accelerated long-term forgetting studies

    Cortex

    (2014)
  • J. Narayanan et al.

    Accelerated long-term forgetting in temporal lobe epilepsy: verbal, nonverbal and autobiographical memory

    Epilepsy Behav

    (2012)
  • N. Muhlert et al.

    Accelerated forgetting of real-life events in transient epileptic amnesia

    Neuropsychologia

    (2010)
  • H. Wilkinson et al.

    Long-term accelerated forgetting of verbal and non-verbal information in temporal lobe epilepsy

    Cortex

    (2012)
  • Z. Fitzgerald et al.

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

    J Clin Neurosci

    (2013)
  • A. Zeman et al.

    Novel forms of forgetting in temporal lobe epilepsy

    Epilepsy Behav

    (2013)
  • G.L. Holmes et al.

    Role of interictal epileptiform abnormalities in cognitive impairment

    Epilepsy Behav

    (2006)
  • P. Peigneux et al.

    Are spatial memories strengthened in the human hippocampus during slow wave sleep?

    Neuron

    (2004)
  • T.N. Shatskikh et al.

    Electrical induction of spikes in the hippocampus impairs recognition capacity and spatial memory in rats

    Epilepsy Behav

    (2006)
  • K.E. Atherton et al.

    Sleep-dependent memory consolidation and accelerated forgetting

    Cortex

    (2014)
  • M.C. Deak et al.

    The role of sleep in forgetting in temporal lobe epilepsy: a pilot study

    Epilepsy Behav

    (2011)
  • T. McGibbon et al.

    Detecting the onset of accelerated long-term forgetting: evidence from temporal lobe epilepsy

    Neuropsychologia

    (2013)
  • K.E. Atherton et al.

    Slow wave sleep and accelerated forgetting

    Cortex

    (2016)
  • M. de Curtis et al.

    Interictal spikes in focal epileptogenesis

    Prog Neurobiol

    (2001)
  • M. Moscovitch et al.

    Consolidation and the hippocampal complex revisited: in defense of the multiple-trace model

    Curr Opin Neurobiol

    (1998)
  • A. Gramstad et al.

    The impact of affectivity dispositions, self-efficacy and locus of control on psychosocial adjustment in patients with epilepsy

    Epilepsy Res

    (2001)
  • S. Tedman et al.

    Development of a scale to measure core beliefs and perceived self efficacy in adults with epilepsy

    Seizure

    (1995)
  • R.J. Mittan

    Psychosocial treatment programs in epilepsy: a review

    Epilepsy Behav

    (2009)
  • E. Farina et al.

    Cognitive rehabilitation in epilepsy: an evidence-based review

    Epilepsy Res

    (2015)
  • P.J. Thompson et al.

    Optimizing memory function in temporal lobe epilepsy

    Seizure

    (2016)
  • A. Liu et al.

    Exploring the efficacy of a 5-day course of transcranial direct current stimulation (tdcs) on depression and memory function in patients with well-controlled temporal lobe epilepsy

    Epilepsy Behav

    (2016)
  • N. Kapur et al.

    Unexpected amnesia: are there lessons to be learned from cases of amnesia following unilateral temporal lobe surgery?

    Brain

    (2003)
  • K.C. Willment et al.

    Hemispheric lateralization interrupted: material-specific memory deficits in temporal lobe epilepsy

    Front Hum Neurosci

    (2013)
  • S. Suresh et al.

    Temporal lobe epilepsy in patients with nonlesional mri and normal memory: an seeg study

    J Neurosurg

    (2015)
  • B.P. Hermann et al.

    Neuropsychological characteristics of the syndrome of mesial temporal lobe epilepsy

    Arch Neurol

    (1997)
  • E. Tramoni et al.

    Long-term consolidation of declarative memory: insight from temporal lobe epilepsy

    Brain

    (2011)
  • B.D. Bell et al.

    Recent innovative studies of memory in temporal lobe epilepsy

    Neuropsychol Rev

    (2007)
  • C.R. Butler et al.

    Recent insights into the impairment of memory in epilepsy: transient epileptic amnesia, accelerated long-term forgetting and remote memory impairment

    Brain

    (2008)
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