Klinische Neurophysiologie 2005; 36(2): 49-59
DOI: 10.1055/s-2005-866853
Originalia
© Georg Thieme Verlag KG Stuttgart · New York

Mediotemporale Gamma-Aktivität und deklaratives Gedächtnis

Mediotemporal Gamma Activity and Declarative MemoryJ.  Fell1 , C.  E.  Elger1 , G.  Fernández1 , 2
  • 1Klinik für Epileptologie, Universität Bonn
  • 2F. C. Donders Center for Cognitive Neuroimaging und Klinik für Neurologie, Radboud Univ. Nijmegen, Niederlande
Further Information

Publication History

Publication Date:
01 June 2005 (online)

Zusammenfassung

Einleitung: Für das deklarative Gedächtnis, d. h. das bewusst zugängliche Langzeitgedächtnis für Ereignisse und Fakten, sind der Hippokampus und der rhinale Kortex, zwei Strukturen im medialen Temporallappen (MTL), entscheidend. Bisher gab es noch keine direkte Evidenz für eine Interaktion dieser beiden Strukturen bei der Gedächtnisbildung. Eine transiente Kopplung neuronaler Verbände kann durch Phasensynchronisation der so genannten Gamma-Aktivität, d. h. der EEG-Aktivität im Frequenzbereich oberhalb von 20 Hz, ermöglicht werden. Methodik: Bei einer Gruppe von 9 Patienten mit unilateralen MTL-Epilepsien wurde das mediotemporale ereigniskorrelierte EEG mittels Tiefenelektroden während einer Wort-Gedächtnisaufgabe abgeleitet. Dann wurden die EEG-Antworten des nicht-pathologischen MTL für die später erinnerten und die vergessenen Wörter verglichen. Zusätzlich wurde bei einer Gruppe von 8 Patienten das kontinuierliche EEG während des Schlafes mittels Tiefen- und Oberflächenelektroden abgeleitet. Als Kopplungsmasse wurden die Phasensynchronisation und die spektrale Kohärenz quantifiziert. Ergebnisse: Die erfolgreiche Einspeicherung von Gedächtnisinhalten geht mit einer stimulusbezogenen anfänglichen Erhöhung der Phasensynchronisation zwischen rhinalem Kortex und Hippokampus und einer späteren Desynchronisation einher. Diese gedächtnisbezogenen Synchronisationsänderungen sind interindividuell hoch korreliert mit Erhöhungen der rhinal-hippokampalen Kohärenz im Theta-Band (4 - 7 Hz). Im Vergleich zum Wachzustand beobachteten wir während des Schlafes insbesondere im Gamma-Band eine deutliche Verringerung der rhinal-hippokampalen Kohärenz. Diskussion: Vermutlich spiegeln die Veränderungen der Theta-Kohärenz eine langsam modulierte Konnektivität zwischen rhinalem Kortex und Hippokampus wider, während die Phasensynchronisation im Gamma-Bereich schnelle Kopplungs- und Entkopplungsvorgänge bewerkstelligt, die den Informationsübertrag zwischen den beiden mediotemporalen Strukturen vorbereiten und abschließen. Die verringerte rhinal-hippokampale Kopplung während des Schlafes könnte ein indirektes elektrophysiologisches Korrelat der verminderten Fähigkeit zur Gedächtnisbildung während des Schlafes repräsentieren.

Abstract

Purpose: Human declarative memory, i. e. the consciously accessible long-term memory for events and facts, crucially depends on two structures within the medial temporal lobe (MTL), the rhinal cortex and the hippocampus. However, so far there was no direct evidence for an interaction between these two structures during memory formation. Transient coupling of neural assemblies can be accomplished by phase synchronisation of gamma activity, i. e. EEG activity in the frequency range above 20 Hz. Method: In a group of 9 patients with unilateral MTL-epilepsies the event-related EEG was recorded with depth electrodes during a word-memory task. The EEG responses of the non-pathological MTL for later remembered and forgotten words were compared. Additionally, the continuous EEG was recorded during sleep with depth and scalp electrodes in a group of 8 patients. Phase synchronisation and spectral coherence were quantified as measures for a neural coupling. Results: Successful memory formation is accompanied by an initial stimulus-related increase of phase synchronisation between rhinal cortex and hippocampus and a later decrease. These memory-related synchronisation changes are interindividually correlated with increases of rhinal-hippocampal theta (4 - 7 Hz) coherence. Compared to the waking state rhinal-hippocampal coherence decreases during sleep, most pronounced within the gamma-band. Discussion: The changes of theta coherence probably reflect a slowly modulated connectivity between rhinal cortex and hippocampus, while gamma synchronisation accomplishes the fast coupling and decoupling processes, which initiate and later terminate the information transfer between both structures. The reduced rhinal-hippocampal coupling during sleep may represent an indirect electrophysiological correlate of the diminished ability to encode memories during sleep.

Literatur

  • 1 Engel A KT, Singer W. Temporal binding and the neural correlates of sensory awareness.  Trends Cog Sci. 2001;  5 16-25
  • 2 Keil A, Gruber T, Müller M M. Functional correlates of macroscopic high-frequency brain activity in the human visual system.  Neurosci Biobehav Rev. 2001;  25 527-534
  • 3 Tallon-Baudry C, Bertrand O. Oscillatory gamma activity in humans and its role in object representation.  Trends Cogn Sci. 1999;  3 151-162
  • 4 Varela F, Lachaux J P, Rodriguez E, Martinerie J. The brainweb: phase synchronization and large-scale integration.  Nat Rev Neurosci. 2001;  2 229-239
  • 5 Barlow H B. Single units and sensation: a neuron doctrine for perceptual psychology?.  Perception. 1972;  1 371-394
  • 6 Malsburg C von der, Schneider W. A neural cocktail-party processor.  Biol Cybern. 1986;  54 29-40
  • 7 Malsburg C von der. The correlation theory of brain function. MPI Biophysical Chemistry, Internal Report 1981 81 - 82
  • 8 Eckhorn R, Bauer R, Jordan W, Brosch M, Kruse W, Munk M, Reitboeck H J. Coherent oscillations: a mechanism of feature linking in the visual cortex? Multiple electrode and correlation analyses in the cat.  Biol Cybern. 1988;  60 121-130
  • 9 Eckhorn R, Frien A, Bauer R, Woelbern T, Kehr H. High frequency (60 - 90 Hz) oscillations in primary visual cortex of awake monkey.  Neuroreport. 1993;  4 243-246
  • 10 Gray C M, König P, Engel A K, Singer W. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties.  Nature. 1989;  338 334-337
  • 11 Engel A K, Kreiter A K, König P, Singer W. Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat.  Proc Natl Acad Sci USA. 1991;  88 6048-6052
  • 12 Engel A K, König P, Kreiter A K, Singer W. Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex.  Science. 1991;  252 1177-1179
  • 13 Frien A, Eckhorn R, Bauer R, Woelbern T, Kehr H. Stimulus-specific fast oscillations at zero phase between visual areas V1 and V2 of awake monkey.  Neuroreport. 1994;  5 2273-2277
  • 14 Lutzenberger W, Pulvermüller F, Elbert T, Birbaumer N. Visual stimulation alters local 40-Hz responses in humans: an EEG-study.  Neurosci Lett. 1995;  183 39-42
  • 15 Müller M M, Bosch J, Elbert T, Kreiter A, Sosa M V, Sosa P V, Rockstroh B. Visually induced gamma-band responses in human electroencephalographic activity - a link to animal studies.  Exp Brain Res. 1996;  112 96-102
  • 16 Desmedt J E, Tomberg C. Transient phase-locking of 40 Hz electrical oscillations in prefrontal and parietal human cortex reflects the process of conscious somatic perception.  Neurosci Lett. 1994;  168 126-129
  • 17 Lebedev M A, Nelson R J. Rhythmically firing (20 - 50 Hz) neurons in monkey primary somatosensory cortex: activity patterns during initiation of vibratory-cued hand movements.  J Comput Neurosci. 1995;  2 313-334
  • 18 Bressler S L. Relation of olfactory bulb and cortex. I. Spatial variation of bulbocortical interdependence.  Brain Res. 1987;  409 285-293
  • 19 Freeman W J. Spatial properties of an EEG event in the olfactory bulb and cortex.  Electroencephalogr Clin Neurophysiol. 1978;  44 586-605
  • 20 Brosch M, Budinger E, Scheich H. Stimulus-related gamma oscillations in primate auditory cortex.  J Neurophysiol. 2002;  87 2715-2725
  • 21 Bullock T H, McClune M C, Achimowicz J Z, Iragui-Madoz V J, Duckrow R B, Spencer S S. EEG coherence has structure in the millimeter domain: subdural and hippocampal recordings from epileptic patients.  Electroencephalogr Clin Neurophysiol. 1995;  95 161-177
  • 22 Menon V, Freeman W J, Cutillo B A, Desmond J E, Ward M F, Bressler S L, Laxer K D, Barbaro N, Gevins A S. Spatio-temporal correlations in human gamma band electrocorticograms.  Electroencephalogr Clin Neurophysiol. 1996;  98 89-102
  • 23 Rodriguez E, George N, Lachaux J P, Martinerie J, Renault B, Varela F J. Perception's shadow: long-distance synchronization of human brain activity.  Nature. 1999;  397 430-433
  • 24 Miltner W H, Braun C, Arnold M, Witte H, Taub E. Coherence of gamma-band EEG activity as a basis for associative learning.  Nature. 1999;  397 434-436
  • 25 Pesaran B, Pezaris J S, Sahani M, Mitra P P, Andersen A A. Temporal structure in neuronal activity during working memory in macaque parietal cortex.  Nat Neurosci. 2002;  5 805-811
  • 26 Fries P, Neuenschwader S, Engel A K, Goebel R, Singer W. Rapid feature selective neuronal synchronization through correlated latency shifting.  Nat Neurosci. 2001;  4 194-200
  • 27 Pinel J PJ. Biopsychologie. Heidelberg, Berlin; Spektrum Akademischer Verlag 2001
  • 28 Brewer J B, Zhao Z, Desmond J E, Glover G H, Gabrieli J DE. Making memories, brain activity that predicts how well visual experience will be remembered.  Science. 1998;  281 1185-1187
  • 29 Fernández G, Weyerts H, Schrader-Bölsche M, Tendolkar I, Smid H GOM, Tempelmann C, Hinrichs H, Scheich H, Elger C E, Mangun G R, Heinze H J. Successful verbal encoding into episodic memory engages the posterior hippocampus, a parametrically analyzed functional magnetic resonance imaging study.  J Neurosci. 1998;  18 1841-1847
  • 30 Wagner A D, Schacter D L, Rotte M, Koutstaal W, Maril A, Dale A M, Rosen B R, Buckner R L. Building memories, remembering and forgetting of verbal experiences as predicted by brain activity.  Science. 1998;  281 1188-1191
  • 31 Paller K A, McCarthy G, Roessler E, Allison T, Wood C C. Potentials evoked in human and monkey medial temporal lobe during auditory and visual oddball paradigms.  Electroencephalogr Clin Neurophysiol. 1992;  84 269-279
  • 32 Fernández G, Effern A, Grunwald T, Pezer N, Lehnertz K, Dümpelmann M, Roost D Van, Elger C E. Real-time tracking of memory formation in the human rhinal cortex and hippocampus.  Science. 1999;  285 1582-1585
  • 33 Fell J, Klaver P, Elger C E, Fernández G. The interaction of rhinal cortex and hippocampus in human declarative memory formation.  Rev Neurosci. 2002;  13 299-312
  • 34 Fernández G, Klaver P, Fell J, Grunwald T, Elger C E. Human declarative memory formation: segregating rhinal and hippocampal contributions.  Hippocampus. 2002;  12 514-519
  • 35 Fell J, Klaver P, Lehnertz K, Grunwald T, Schaller C, Elger C E, Fernández G. Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling.  Nat Neurosci. 2001;  4 1259-1264
  • 36 Kreiman G, Koch C, Fried I. Imagery neurons in the human brain.  Nature. 2000;  408 357-361
  • 37 LaBerge D. Attention, awareness, and the triangular circuit.  Conscious Cogn. 1997;  6 149-181
  • 38 Wagner A D. Synchronicity: When you're gone I'm lost without a trace?.  Nat Neurosci. 2001;  4 1159-1160
  • 39 Rheilly C E. Rhinal cortex and hippocampus interact synchronically in human memory formation.  J Neurol. 2002;  249 237-239
  • 40 Otten L J, Rugg M D. The birth of a memory.  Trends Neurosci. 2002;  25 279-281
  • 41 Klimesch W, Doppelmayr M, Russegger H, Pachinger T. Theta band power in the human scalp EEG and the encoding of new information.  Neuroreport. 1996;  7 1235-1240
  • 42 Klimesch W, Doppelmayr M, Schmike H, Ripper B. Theta synchronization and alpha desynchronization in a memory task.  Psychophysiology. 1997;  34 169-176
  • 43 Weiss S, Müller H M, Rappelsberger P. Theta synchronization predicts efficient memory encoding of concrete and abstract nouns.  Neuroreport. 2000;  11 2357-2361
  • 44 Weiss S, Rappelsberger P. Long-range EEG synchronization during word encoding correlates with successful memory performance.  Cogn Brain Res. 2000;  9 299-312
  • 45 Mölle M, Marshall L, Fehm H L, Born J. EEG theta synchronization conjoined with alpha desynchronization indicate intentional encoding.  Eur J Neurosci. 2002;  15 923-928
  • 46 Jensen O, Tesche C D. Frontal theta activity in humans increases with memory load in a working memory task.  Eur J Neurosci. 2002;  15 1395-1399
  • 47 Kahana M J, Sekuler R, Caplan J, Kirschen M, Madsen J R. Human theta oscillations exhibit task dependence during virtual maze navigation.  Nature. 1999;  399 781-784
  • 48 Tesche C D, Karhu J. Theta oscillations index human hippocampal activation during a working memory task.  Proc Natl Acad Sci USA. 2000;  97 919-924
  • 49 Caplan J B, Madsen J R, Raghavachari S, Kahana M J. Distinct patterns of brain oscillations underlie two basic parameters of human maze learning.  J Neurophysiol. 2001;  86 368-380
  • 50 Raghavachari S, Kahana M J, Rizzuto D S, Caplan J B, Kirschen M P, Bourgeois B, Madsen J R, Lisman J E. Gating of human theta oscillations by a working memory task.  J Neurosci. 2001;  21 3175-3183
  • 51 Chrobak J J, Buzsáki G. Operational dynamics in the hippocampal-entorhinal axis.  Neurosci Biobehav Rev. 1998;  22 303-310
  • 52 Chrobak J J, Buzsáki G. Gamma oscillations in the entorhinal cortex of the freely behaving rat.  J Neurosci. 1998;  18 388-398
  • 53 O'Keefe J, Recce M L. Phase relationship between hippocampal place units and the EEG theta rhythm.  Hippocampus. 1993;  3 317-330
  • 54 Skaggs W E, McNaughton B L, Wilson M A, Barnes C A. Theta phase precession in hippocampal neuronal populations and the compression of temporal sequences.  Hippocampus. 1996;  6 149-172
  • 55 Buzsáki G. The hippocampo-neocortical dialogue.  Cereb Cortex. 1996;  6 81-92
  • 56 Jensen O, Idiart M AP, Lisman J E. Physiologically realistic formation of autoassociative memory in networks with theta/gamma oscillations: Role of fast NMDA channels.  Learn Mem. 1996;  3 243-256
  • 57 Jensen O, Lisman J E. Theta/gamma networks with slow NMDA channels learn sequences and encode episodic memory: role of NMDA channels in recall.  Learn Mem. 1996;  3 264-278
  • 58 Fell J, Klaver P, Elfadil H, Schaller C, Elger C E, Fernández G. Rhinal-hippocampal theta coherence during declarative memory formation: interaction with gamma synchronization?.  Eur J Neurosci. 2003;  17 1082-1088
  • 59 Sarnthein J, Petsche H, Rappelsberger P, Shaw G L, Stein A Von. Synchronization between prefrontal and posterior association cortex during human working memory.  Proc Natl Acad Sci USA. 1998;  95 7092-7096
  • 60 Hobson J A, Pace-Schott E F, Stickgold R. Dreaming and the brain: toward a cognitive neuroscience of conscious states.  Behav Brain Sci. 2000;  23 793-842
  • 61 Goodenough D R. Dream recall: history and current status of the field. In: Ellman SJ, Antrobus JS (eds) The mind in sleep: psychology and psychophysiology. New York; Wiley & Sons 1991: 143-171
  • 62 Fosse M J, Fosse R, Hobson J A, Stickgold R J. Dreaming and episodic memory: a functional dissociation?.  J Cogn Neurosci. 2003;  15 1-9
  • 63 Stickgold R, Pace-Schott E F, Hobson J A. Subjective estimates of dream duration and dream recall process.  Sleep Res. 1997;  26 279
  • 64 Fell J, Staedtgen M, Burr W, Kockelmann E, Helmstaedter C, Schaller C, Elger C E, Fernández G. Rhinal-hippocampal EEG coherence is reduced during human sleep.  Eur J Neurosci. 2003;  18 1711-1716
  • 65 Rechtschaffen A, Kales A. A manual of standarized terminology, technics, and scoring system for sleep stages of human subjects. Public Health Service, NIH Publication No. 204. Washington D. C.; U. S. Government Printing Office 1968
  • 66 Mann K, Röschke J. Different phase relationships between EEG frequency bands during NREM and REM sleep.  Sleep. 1997;  20 753-756
  • 67 Gross D W, Gotman J. Correlation of high-frequency oscillations with the sleep-wake cycle and cognitive activity in human.  Neurosci. 1999;  94 1005-1018
  • 68 Dumermuth G, Lange B, Lehmann D, Meier C A, Dinkelmann R, Molinari L. Spectral analysis of all-night sleep EEG in healthy adults.  Eur Neurol. 1983;  22 322-339
  • 69 Nielsen T, Abel A, Lorrain D, Montplaisir J. Interhemispheric EEG coherence during sleep and wakefulness in left- and right-handed subjects.  Brain Cogn. 1990;  14 113-125
  • 70 Achermann P, Borbely A A. Coherence analysis of the human sleep electroencephalogram.  Neuroscience. 1998;  85 1195-1208
  • 71 Llinas R, Ribary U. Coherent 40-Hz oscillations characterized dream state in humans.  Proc Natl Acad Sci USA. 1993;  90 2078-2081
  • 72 Amaral D G, Insausti R. Hippocampal formation. In: Paxinos G (ed) The human nervous system. San Diego; Academic Press 1990: 711-755
  • 73 Moser M-B, Moser E I. Functional differentiation in the hippocampus.  Hippocampus. 1998;  8 608-619
  • 74 Niedermeyer E, Lopes Da Silva F. Electroencephalography: Basic Principles, Clinical Applications, and related fields. 4th Edition. Philadelphia; Williams and Wilkins 1999
  • 75 Steriade M, Nunez A, Amzica F. Intracellular analysis of relations between the slow (< 1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram.  J Neurosci. 1993;  13 3266-3283
  • 76 Abeles M. Role of the cortical neuron: integrator or coincidence detector?.  Israel J Med Sci. 1982;  18 83-92
  • 77 König P, Engel A K, Singer W. Integrator or coincidence detector? The role of the cortical neuron revisited.  Trends Neurosci. 1996;  19 130-137
  • 78 Malsburg C von der. The what and why of binding: the modeler's perspective.  Neuron. 1999;  24 95-104
  • 79 Azouz R, Gray C M. Dynamic spike threshold reveals a mechanism for synaptic coincidence detection in cortical neurons in vivo.  Proc Natl Acad Sci USA. 2000;  97 8110-8115
  • 80 Alonso J M, Usrey W M, Reid R C. Precisely correlated firing in cells of the lateral geniculate nuclues.  Nature. 1996;  383 815-819
  • 81 Roy S A, Alloway K D. Coincidence detection or temporal integration? What the neurons in somatosensory cortex are doing.  J Neurosci. 2001;  21 2462-2473
  • 82 Usrey W M, Alonso J M, Reid R C. Synaptic interactions between thalamic inputs to simple cells in cat visual cortex.  J Neurosci. 2000;  20 5461-5467
  • 83 Fell J, Fernández G, Klaver P, Elger C E, Fries P. Is synchronized gamma activity relevant for selective attention?.  Brain Res Rev. 2003;  42 265-272
  • 84 Crick F, Koch C. Are we aware of activity in the primary visual cortex?.  Nature. 1995;  375 121-123
  • 85 Engel A K, Fries P, Singer W. Dynamic predictions: oscillations and synchrony in top-down processing.  Nat Rev Neurosci. 2001;  2 704-716
  • 86 Müller M M, Gruber T. Induced gamma-band responses in the human EEG are related to attentional information processing.  Vis Cogn. 2001;  8 579-592
  • 87 Hebb D O. The organisation of behavior. New York; Wiley & Sons 1949
  • 88 Abbott L F, Nelson S B. Synaptic plasticity: taming the beast.  Nat Neurosci. 2000;  3 1178-1183
  • 89 Markram H, Lübke J, Frotscher M, Sakmann B. Regulation of synaptic efficacy by coincidence of postsynaptic Aps and EPSPs.  Science. 1997;  275 213-215
  • 90 Sommer F T, Wennekers T. Associative memory in networks of spiking neurons.  Neural Netw. 2001;  14 825-834
  • 91 Fernández G, Fell J, Fries P. Response: the birth of a memory.  Trends Neurosci. 2002;  25 281-282
  • 92 Herrmann C S, Munk M H, Engel A K. Cognitive functions of gamma-band activity: memory match and utilization.  Trends Cogn Sci. 2004;  8 347-355

Dr. Jürgen Fell

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