The relationship of medial temporal lobe epilepsy with the declarative memory system

Publications

Share / Export Citation / Email / Print / Text size:

Journal of Epileptology

Foundation of Epileptology

Subject: Medicine

GET ALERTS

eISSN: 2300-0147

DESCRIPTION

2
Reader(s)
6
Visit(s)
0
Comment(s)
0
Share(s)

SEARCH WITHIN CONTENT

FIND ARTICLE

Volume / Issue / page

Archive
Volume 26 (2018)
Volume 25 (2017)
Volume 24 (2016)
Volume 23 (2015)
Volume 22 (2014)
Volume 21 (2013)
Related articles

VOLUME 24 , ISSUE 2 (December 2016) > List of articles

The relationship of medial temporal lobe epilepsy with the declarative memory system

Péter Halász *

Keywords : Medial temporal lobe epilepsy, memory consolidation, hippocampal memory, slow wave sleep sharp wave ripple, sleep spiking effect

Citation Information : Journal of Epileptology. Volume 24, Issue 2, Pages 157-165, DOI: https://doi.org/10.1515/joepi-2016-0011

License : (CC BY 4.0)

Received Date : 03-October-2016 / Accepted: 10-November-2016 / Published Online: 22-November-2016

ARTICLE

ABSTRACT

Introduction. Medial temporal lobe of epilepsy (MTLE) is considered as local/regional epilepsy. However, as was discussed in Part I of this review (Halasz, 2016a) there is more evidence regarding the involvement of both temporal lobes so as to consider MTLE as one of the typical bilateral system epilepsies.

Aim. To provide contemporary review of MTLE in relation to the declarative memory system and the newly recognized hippocampo-frontal memory consolidation during slow wave sleep.

Methods. A review of the available literature on experimental and clinical data and also the authors own studies in MTLE patients.

Review, discussion and results. New experimental and clinical neurophysiological data have shown that MTLE is closely linked to the hippocampal memory system. It is likely that hippocampal spiking is the epileptic variations of the normal sharp wave ripple events mediating the encoding and consolidation of memory engrams by a hippocampo-frontal dialogue during slow wave sleep.

Conclusions. The source of memory impairment in MTLE patients is not merely the cell loss and synaptic transformation of the hippocampal structure, but the every night interference with memory consolidation due to interictal spiking.

Content not available PDF Share

FIGURES & TABLES

REFERENCES

Bancaud J., Brunet-Bourgin F., Chauvel P., Halgren E.: Anatomical origin of déjà vu and vivid ‘memories’ in human temporal lobe epilepsy. Brain, 1994, 117: 71–90.

 

Baxendale S.A., van Paesschen W., Thompson P.J., Connelly A., Duncan J.S, Harknes W.F.., Shorvon S.D.: The relationship between quantitative MRI and neuropsychological functioning in temporal lobe epilepsy. Epilepsia, 1998, 39: 158–166.

 

Bellesi M., Riedner B.A., Garcia-Molina G.N., Cirelli C., Tononi G.: Enhancement of sleep slow waves: underlying mechanisms and practical consequences. Front. Syst. Neurosci., 2014, 8: 208.

 

Bliss T., Lomo T.: Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol., 1973, 232: 331–356.

 

Born J., Rasch B., Gais S.: Sleep to remember. Neuroscientist, 2006, 12: 410–424.

 

Born J.: Slow-wave sleep and the consolidation of long-term memory. World J. Biol. Psychiatry, 2010, 1: 16–21.

 

Buzsaki G.: Hippocampal sharp waves: their origin and significance. Brain Res., 1986, 398: 242–252.

 

Buzsaki G.: The hippocampo-neocortical dialogue. Cereb. Cortex, 1996, 6: 81–89.

 

Buzsaki G.: Memory consolidation during sleep: a neurophysiological perspective. J. Sleep Res., 1998, 1: 17–23.

 

Buzsaki G.: Hippocampal sharp wave-ripple: a cognitive biomarker for episodic memory and planning. Hippocampus, 2015, 25: 1073–1188.

 

Cantero J.L., Atienza M., Madsen J.R., Stickgold R.: Gamma EEG dynamics in neocortex and hippocampus during human wakefulness and sleep. Neuroimage, 2004, 22: 1271–1280.

 

Castro L.H., Silva L.C., Adda C.C., Banaskiwitz N.H., Xavier A.B., Jorge C.L. et al.: Low prevalence but high specificity of material-specific memory impairment in epilepsy associated with hippocampal sclerosis. Epilepsia, 2013, 54: 1735–1742.

 

Cheng S., Frank L.M.: New experiences enhance coordinated neural activity in the hippocampus. Neuron, 2008, 57: 303–313.

 

Chrobak J.J., Buzsaki G.: High-frequency oscillations in the output networks of the hippocampal-entorhinal axis of the freely behaving rat. J. Neurosci., 1996, 16: 3056–3066.

 

Chrobak J.J., Buzsaki G.: Operational dynamics in the hippocampal- entorhinal axis. Neurosci. Biobehav. Rev., 1998, 22: 303–310.

 

Clemens Z., Janszky J., Szucs A., Bekesy M., Clemens B., Halasz P.: Interictal epileptic spiking during sleep and wakefulness in mesial temporal lobe epilepsy: a comparative study of scalp and foramen ovale electrodes. Epilepsia, 2003, 44: 186–192.

 

Clemens Z., Molle M., Erőss L., Jakus R., Rasonyi G., Halasz P. et al.: Fine-tuned coupling between human parahippocampal ripples and sleep spindles. Eur. J. Neurosci., 2011, 33: 511–520.

 

Csicsvari J., Hirase H., Czurko A., Mamiya A., Buzsaki G.: Oscillatory coupling of hippocampal pyramidal cells and interneurons in the behaving Rat. J. Neurosci.,1999, 19: 274–287.

 

Diekelmann S., Born J.: The memory function of sleep. Nat. Rev. Neurosci., 2010, 11: 114–126.

 

Feld G.B., Diekelmann S.: Sleep smart-optimizing sleep for declarative learning and memory. Front. Psychol., 2015, 6: 622.

 

Fell J., Klaver P., Lehnertz K., Grunwald T., Schaller C., Elger C.E., Fernandez G.: Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nat. Neurosci., 2001, 4: 1259–1264.

 

Fell J., Staedtgen M., Burr W., Kockelmann E., Helmstaedter C., Schaller C. et al.: Rhinal-hippocampal EEG coherence is reduced during human sleep. Eur. J. Neurosci., 2003, 18: 1711–1716.

 

Fogel S.M., Smith C.T.: Learning-dependent changes in sleep spindles and Stage 2 sleep. J. Sleep Res., 2006, 15: 250–255.

 

Foster D.J., Wilson M.A.: Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature, 2006, 440: 680–683.

 

Frauscher B., Bernasconi N., Caldairou B., von Ellenrieder N., Bernasconi A., Gotman J., Dubeau F.: Interictal Hippocampal Spiking Influences the Occurrence of Hippocampal Sleep Spindles. Sleep, 2015, 38: 1927–1933.

 

Gais S., Molle M., Helms K.: Born Learning-dependent increases in sleep spindle density. J. Neurosci., 2002, 22: 6830–6834.

 

Gelinas J.N., Khodagholy D., Thesen T., Devinsky O., Buzsaki G.: Interictal epileptiform discharges induce hippocampalcortical coupling in temporal lobe epilepsy. Nat. Med., 2016, 22: 641–648.

 

Girardeau G., Benchenane K., Wiener S.I., Buzsaki G., Zugaro M.B.: Selective suppression of hippocampal ripples impairs spatial memory. Nat. Neurosci., 2009, 12: 1222–1223.

 

Gulyas A.I., Freund T.T.: Generation of physiological and pathological high frequency oscillations: the role of perisomatic inhibition in sharp-wave ripple and interictal spike generation. Curr. Opin. Neurobiol., 2015, 31: 26–32.

 

Halasz P.: The medial temporal lobe epilepsy is a bilateral disease – novel aspects. Journal of Epileptology, 2016a, 24: 141–155.

 

Hasselmo M.E.: The role of acetylcholine in learning and memory. Curr. Opin. Neurobiol., 2006, 16: 710–715.

 

Hebb D.O.: Organization of Behavior: a Neuropsychological Theory. John Wiley, New York 1949.

 

Helmstaedter C., Kurthen M., Elger C.E.: Sex differences in material-specific cognitive functions related to language dominance: an intracarotid amobarbital study in left temporal lobe epilepsy. Laterality, 1999, 4: 51–63.

 

Jackson J.H.: Selected writings of John Hughlings Jackson. Volumes 1 and 2, J. Taylor (ed.). Staples Press, London 1958.

 

Ji D., Wilson M.A.: Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat. Neurosci., 2007, 10: 100–107.

 

Lewis P.A., Durrant S.J.: Overlapping memory replay during sleep builds cognitive schemata. Trends Cogn. Sci., 2011, 15: 343–351.

 

Llinas R., Ribary U.: Coherent 40-Hz oscillation characterizes dream state in humans. Proc. Natl. Acad. Sci. USA, 1993, 90: 2078–2081.

 

Margerison J.H., Corsellis J.A.: Epilepsy and the temporal lobes. A clinical, electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain, 1966, 89: 499–530.

 

Molle M., Born J.: Slow oscillations orchestrating fast oscillations and memory consolidation. Prog. Brain Res., 2011, 193: 93–110.

 

Nadasdy Z.: Spike sequences and their consequences. J. Physiol. Paris, 2000, 94: 505–524.

 

O’Neill J., Senior T.J., Allen K., Huxter J.R., Csicsvari J.: Reactivation of experience-dependent cell assembly patterns in the hippocampus. Nat. Neurosci., 2008, 11: 209–215.

 

O’Neill J., Pleydell-Bouverie B., Dupret D., Csicsvari J.: Play it again: reactivation of waking experience and memory. Trends Neurosci., 2010, 33: 220–229.

 

Ozkara C., Hanoğlu L., Keskinkilic C., Yeni N., Aysal F., Uzan M. et al.: Memory in patients with drug-responsive mesial temporal lobe epilepsy and hippocampal sclerosis. Epilepsia, 2004, 45: 1392–1396.

 

Payne J.D., Kensinger E.A.: Sleep leads to changes in the emotional memory trace: evidence from FMRI. J. Cogn. Neurosci., 2011, 23: 1285–1297.

 

Penfield W., Jasper H.: Epilepsy and the Functional anatomy of the Human Brain. Little Brown and Company, Boston 1954.

 

Ramon y Cajal S.: The Croonian Lecture: La Fine Structure des Centres Nerveux. Royal Society of London, 1894, 55: 444–468.

 

Sano K., Malamud N.: Clinical significance of sclerosis of the cornu ammonis: ictal psychic phenomena. AMA Arch. Neurol. Psychiatry, 1953, 70: 40–53.

 

Sawrie S.M., Martin R.C., Knowlton R., Faught E., Gilliam F., Kuzniecky R.: Relationships among hippocampal volumetry, proton magnetic resonance spectroscopy, and verbal memory in temporal lobe epilepsy. Epilepsia, 2001, 42: 1403–1407.

 

Schabus M., Gruber G., Parapatics S., Sauter C., Klosch G., Anderer P. et al.: Sleep spindles and their significance for declarative memory consolidation. Sleep, 2004, 27: 1479–1485.

 

Schlingloff D., Kali S., Freund T.F., Hajos N., Gulyas A.I.: Mechanisms of initiation and ripple generation sharp wave. J. Neurosci., 2014, 34: 11385–11398.

 

Scoville W.B., Milner B.: Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry, 1957, 20: 11–21.

 

Shatskikh T.N., Raghavendra M., Zhao Q., Cui Z., Holmes G.L.: Electrical induction of spikes in the hippocampus impairs recognition capacity and spatial memory in rats. Epilepsy Behav., 2006, 9: 549–556.

 

Siapas A.G., Wilson M.A.: Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron, 1998, 21: 1123–1128.

 

Skaggs W.E., McNaughton B.L.: Replay of neuronal firing sequences in rat hippocampus during sleep following spatial experience. Science, 1996, 271: 1870–1873.

 

Staresina B.P., Bergmann T.O., Bonnefond M., van der Meij R., Jensen O., Deuker L. et al.: Hierarchical nesting of slow oscillations, spindles and ripples in the human hippocampus during sleep. Nat. Neurosci., 2015, 18: 1679–1686

 

Stickgold R., Walker M.P.: Sleep-dependent memory triage: evolving generalization through selective processing. Nat. Neurosci., 2013, 16: 139–145.

 

Wilson M.A., McNaughton B.L.: Reactivation of hippocampal ensemble memories during sleep. Science, 1994, 265: 676–679.

 

Witt J.A., Coras R., Schramm J., Becker A.J., Elger C.E., Blumcke I., Helmstaedter C.: The overall pathological status of the left hippocampus determines preoperative verbal memory performance in left mesial temporal lobe epilepsy. Hippocampus, 2014, 24: 446–454.

 

EXTRA FILES

COMMENTS