High frequency oscillations are associated with cognitive processing in human recognition memory

. 2014 Aug ; 137 (Pt 8) : 2231-44. [epub] 20140611

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid24919972

Grantová podpora
R01-NS63039 NINDS NIH HHS - United States
U24-NS063930 NINDS NIH HHS - United States

High frequency oscillations are associated with normal brain function, but also increasingly recognized as potential biomarkers of the epileptogenic brain. Their role in human cognition has been predominantly studied in classical gamma frequencies (30-100 Hz), which reflect neuronal network coordination involved in attention, learning and memory. Invasive brain recordings in animals and humans demonstrate that physiological oscillations extend beyond the gamma frequency range, but their function in human cognitive processing has not been fully elucidated. Here we investigate high frequency oscillations spanning the high gamma (50-125 Hz), ripple (125-250 Hz) and fast ripple (250-500 Hz) frequency bands using intracranial recordings from 12 patients (five males and seven females, age 21-63 years) during memory encoding and recall of a series of affectively charged images. Presentation of the images induced high frequency oscillations in all three studied bands within the primary visual, limbic and higher order cortical regions in a sequence consistent with the visual processing stream. These induced oscillations were detected on individual electrodes localized in the amygdala, hippocampus and specific neocortical areas, revealing discrete oscillations of characteristic frequency, duration and latency from image presentation. Memory encoding and recall significantly modulated the number of induced high gamma, ripple and fast ripple detections in the studied structures, which was greater in the primary sensory areas during the encoding (Wilcoxon rank sum test, P = 0.002) and in the higher-order cortical association areas during the recall (Wilcoxon rank sum test, P = 0.001) of memorized images. Furthermore, the induced high gamma, ripple and fast ripple responses discriminated the encoded and the affectively charged images. In summary, our results show that high frequency oscillations, spanning a wide range of frequencies, are associated with memory processing and generated along distributed cortical and limbic brain regions. These findings support an important role for fast network synchronization in human cognition and extend our understanding of normal physiological brain activity during memory processing.

Komentář v

PubMed

Zobrazit více v PubMed

Axmacher N, Elger CE, Fell J. Ripples in the medial temporal lobe are relevant for human memory consolidation. Brain J Neurol. 2008;131:1806–17. PubMed

Ball T, Kern M, Mutschler I, Aertsen A, Schulze-Bonhage A. Signal quality of simultaneously recorded invasive and non-invasive EEG. Neuroimage. 2009;46:708–16. PubMed

Baker SN, Gabriel C, Lemon RN. EEG oscillations at 600 Hz are macroscopic markers for cortical spike bursts. J Physiol. 2003;550:529–34. PubMed PMC

Barth DS. Submillisecond synchronization of fast electrical oscillations in neocortex. J Neurosci. 2003;23:2502–10. PubMed PMC

Bokil H, Andrews P, Kulkarni JE, Mehta S, Mitra PP. Chronux: a platform for analyzing neural signals. J Neurosci Methods. 2010;192:146–51. PubMed PMC

Bragin A, Engel J, Jr, Wilson CL, Fried I, Buzsáki G. High-frequency oscillations in human brain. Hippocampus. 1999;9:137–42. PubMed

Brinkmann BH, Bower MR, Stengel KA, Worrell GA, Stead M. Large-scale electrophysiology: acquisition, compression, encryption, and storage of big data. J Neurosci Methods. 2009;180:185–92. PubMed PMC

Brovelli A, Lachaux J-P, Kahane P, Boussaoud D. High gamma frequency oscillatory activity dissociates attention from intention in the human premotor cortex. Neuroimage. 2005;28:154–64. PubMed

Burke JF, Zaghloul KA, Jacobs J, Williams RB, Sperling MR, Sharan AD, et al. Synchronous and asynchronous theta and gamma activity during episodic memory formation. J Neurosci. 2013;33:292–304. PubMed PMC

Buzsáki G. Rhythms of the brain. Oxford: Oxford University Press; 2006.

Buzsáki G, Horváth Z, Urioste R, Hetke J, Wise K. High-frequency network oscillation in the hippocampus. Science. 1992;256:1025–7. PubMed

Buzsáki G, da Silva FL. High frequency oscillations in the intact brain. Prog Neurobiol. 2012;98:241–9. PubMed PMC

Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, et al. High gamma power is phase-locked to theta oscillations in human neocortex. Science. 2006;313:1626–8. PubMed PMC

Crone NE, Sinai A, Korzeniewska A. High frequency gamma oscillations and human brain mapping with electrocorticography. Prog Brain Res. 2006;159:275–95. PubMed

Curio G. Linking 600 Hz ‘spikelike’ EEG/MEG wavelets (‘sigma-bursts’) to cellular substrates: concepts and caveats. J Clin Neurophysiol. 2000;17:337–96. PubMed

David O, Kilner JM, Friston KJ. Mechanisms of evoked and induced responses in MEG/EEG. Neuroimage. 2006;31:1580–91. PubMed

Dragoi G, Tonegawa S. Preplay of future place cell sequences by hippocampal cellular assemblies. Nature. 2011;469:397–401. PubMed PMC

Engel AK, Moll CKE, Fried I, Ojemann GA. Invasive recordings from the human brain: clinical insights and beyond. Nat Rev Neurosci. 2005;6:35–47. PubMed

Engel J., Jr Biomarkers in epilepsy: introduction. Biomark Med. 2011;5:537–44. PubMed

Foster DJ, Wilson MA. Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature. 2006;440:680–3. PubMed

Fries P. Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu Rev Neurosci. 2009;32:209–24. PubMed

Gaona CM, Sharma M, Freudenburg ZV, Breshears JD, Bundy DT, Roland J, et al. Nonuniform high-gamma (60–500 Hz) power changes dissociate cognitive task and anatomy in human cortex. J Neurosci. 2011;31:2091–100. PubMed PMC

Harris KD, Csicsvari J, Hirase H, Dragoi G, Buzsáki G. Organization of cell assemblies in the hippocampus. Nature. 2003;424:552–6. PubMed

Howard MW, Rizzuto DS, Caplan JB, Madsen JR, Lisman J, Aschenbrenner-Scheibe R, et al. Gamma oscillations correlate with working memory load in humans. Cereb Cortex. 2003;13:1369–74. PubMed

Issa EB, Papanastassiou AM, DiCarlo JJ. Large-scale, high-resolution neurophysiological maps underlying fMRI of macaque temporal lobe. J Neurosci. 2013;33:15207–19. PubMed PMC

Jacobs J, Kahana MJ. Direct brain recordings fuel advances in cognitive electrophysiology. Trends Cogn Sci. 2010;14:162–71. PubMed PMC

Jadhav SP, Kemere C, German PW, Frank LM. Awake hippocampal sharp-wave ripples support spatial memory. Science. 2012;336:1454–8. PubMed PMC

Jensen O, Kaiser J, Lachaux JP. Human gamma-frequency oscillations associated with attention and memory. Trends Neurosci. 2007;30:317–24. PubMed

Jerbi K, Ossandón T, Hamamé CM, Senova S, Dalal SS, Jung J, et al. Task-related gamma-band dynamics from an intracerebral perspective: review and implications for surface EEG and MEG. Hum Brain Mapp. 2009;30:1758–71. PubMed PMC

Kovach CK, Tsuchiya N, Kawasaki H, Oya H, Howard MA, Adolphs R. Manifestation of ocular-muscle EMG contamination in human intracranial recordings. Neuroimage. 2011;54:213–33. PubMed PMC

Lachaux JP, Axmacher N, Mormann F, Halgren E, Crone NE. High-frequency neural activity and human cognition: past, present and possible future of intracranial EEG research. Prog Neurobiol. 2012;98:279–301. PubMed PMC

Lang PJ, Bradley MM, Cuthbert BN. International Affective Picture System (IAPS): technical manual and affective ratings. 1997.

Le Van Quyen M. High frequency oscillations in cognition and epilepsy. Prog Neurobiol. 2012;98:239–40. PubMed

Le Van Quyen M, Bragin A, Staba R, Crépon B, Wilson CL, Engel J., Jr Cell type-specific firing during ripple oscillations in the hippocampal formation of humans. J Neurosci. 2008;28:6104–10. PubMed PMC

Le Van Quyen M, Staba R, Bragin A, Dickson C, Valderama M, Fried I, et al. Large-scale micro-electrode recordings of high-frequency gamma oscillations in human cortex during sleep. J Neurosci. 2010;30:7770–82. PubMed PMC

Liu H, Agam Y, Madsen JR, Kreiman G. Timing, timing, timing: fast decoding of object information from intracranial field potentials in human visual cortex. Neuron. 2009;62:281–90. PubMed PMC

Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A. Neurophysiological investigation of the basis of the fMRI signal. Nature. 2001;412:150–7. PubMed

Manning JR, Jacobs J, Fried I, Kahana MJ. Broadband shifts in local field potential power spectra are correlated with single-neuron spiking in humans. J Neurosci. 2009;29:13613–20. PubMed PMC

Matsumoto A, Brinkmann BH, Stead SM, Matsumoto J, Kucewicz M, Marsh WR, et al. Pathological and physiological high frequency oscillations in focal human epilepsy. J Neurophysiol. 2013a;110:1958–64. PubMed PMC

Matsumoto JY, Stead M, Kucewicz MT, Matsumoto AJ, Peters PA, Brinkmann BH, et al. Network oscillations modulate interictal epileptiform spike rate during human memory. Brain. 2013b;136:2444–56. PubMed PMC

Mishkin M, Ungerleider LG, Macko KA. Object vision and spatial vision: two cortical pathways. Trends Neurosci. 1983;6:414–7.

Mormann F, Kornblith S, Quiroga RQ, Kraskov A, Cerf M, Fried I, et al. Latency and selectivity of single neurons indicate hierarchical processing in the human medial temporal lobe. J Neurosci. 2008;28:8865–72. PubMed PMC

Mumford D. On the computational architecture of the neocortex. Biol Cybern. 1992;66:241–51. PubMed

Niessing J, Ebisch B, Schmidt KE, Niessing M, Singer W, Galuske RA. Hemodynamic signals correlate tightly with synchronized gamma oscillations. Science. 2005;309:948–51. PubMed

O’Neill J, Senior TJ, Allen K, Huxter JR, Csicsvari J. Reactivation of experience-dependent cell assembly patterns in the hippocampus. Nat Neurosci. 2008;11:209–15. PubMed

Quian Quiroga R, Kraskov A, Koch C, Fried I. Explicit encoding of multimodal percepts by single neurons in the human brain. Curr Biol. 2009;19:1308–13. PubMed PMC

Quiroga RQ, Reddy L, Kreiman G, Koch C, Fried I. Invariant visual representation by single neurons in the human brain. Nature. 2005;435:1102–7. PubMed

Ray S, Crone NE, Niebur E, Franaszczuk PJ, Hsiao SS. Neural correlates of high-gamma oscillations (60-200 Hz) in macaque local field potentials and their potential implications in electrocorticography. J Neurosci. 2008;28:11526–36. PubMed PMC

Roux F, Wibral M, Mohr HM, Singer W, Uhlhaas PJ. Gamma-band activity in human prefrontal cortex codes for the number of relevant items maintained in working memory. J Neurosci. 2012;32:12411–20. PubMed PMC

Sederberg PB, Schulze-Bonhage A, Madsen JR, Bromfield EB, McCarthy DC, Brandt A, et al. Hippocampal and neocortical gamma oscillations predict memory formation in humans. Cereb Cortex. 2007;17:1190–6. PubMed

Silva FL. EEG and MEG: relevance to neuroscience. Neuron. 2013;80:1112–28. PubMed

Singer AC, Carr MF, Karlsson MP, Frank LM. Hippocampal SWR activity predicts correct decisions during the initial learning of an alternation task. Neuron. 2013;77:1163–73. PubMed PMC

Singer W, Gray CM. Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci. 1995;18:555–86. PubMed

Staba RJ. Normal and pathologic high-frequency oscillations. Epilepsia. 2010;51:21. PubMed

Staba RJ, Wilson CL, Bragin A, Fried I, Engel J., Jr Quantitative analysis of high-frequency oscillations (80–500 Hz) recorded in human epileptic hippocampus and entorhinal cortex. J Neurophysiol. 2002;88:1743–52. PubMed

Sullivan D, Csicsvari J, Mizuseki K, Montgomery S, Diba K, Buzsaki G. Relationships between hippocampal sharp waves, ripples and fast gamma oscillation: influence of dentate and entorhinal cortical activity. J Neurosci. 2011;31:8605–16. PubMed PMC

Tallon-Baudry C. The roles of gamma-band oscillatory synchrony in human visual cognition. Front Biosci (Landmark Ed) 2009;14:321–32. PubMed

Tallon-Baudry C, Bertrand O. Oscillatory gamma activity in humans andits role in object representation. Trends Cogn Sci. 1999;3:151–62. PubMed

Telenczuk B, Baker SN, Herz AVM, Curio G. High-frequency EEG covaries with spike burst patterns detected in cortical neurons. J Neurophysiol. 2011;105:2951–9. PubMed PMC

Traub RD, Whittington MA. Cortical oscillations in health and disease. Oxford University Press; 2010.

Uhlhaas PJ, Singer W. Neuronal dynamics and neuropsychiatric disorders: toward a translational paradigm for dysfunctional large-scale networks. Neuron. 2012;75:963–80. PubMed

Van Vugt MK, Sederberg PB, Kahana MJ. Comparison of spectral analysis methods for characterizing brain oscillations. J Neurosci Methods. 2007;162:49–63. PubMed PMC

Wilson MA, McNaughton BL. Recativation of hippocampal ensemble memories during sleep. Science. 1994;265:676–9. PubMed

Worrell GA, Gardner AB, Stead SM, Hu S, Goerss S, Cascino GJ, et al. High-frequency oscillations in human temporal lobe: simultaneous microwire and clinical macro-electrode recordings. Brain. 2008;131:928–37. PubMed PMC

Worrell G, Gotman J. High-frequency oscillations and other electrophysiological biomarkers of epilepsy: clinical studies. Biomark Med. 2011;5:557–66. PubMed PMC

Worrell GA, Jerbi K, Kobayashi K, Lina JM, Zelmann R, Le Van Quyen M. Recording and analysis techniques for high-frequency oscillations. Prog Neurobiol. 2012;98:265–278. PubMed PMC

Worrell GA, Parish L, Cranstoun SD, Jonas R, Baltuch G, Litt B. High-frequency oscillations and seizure generation in neocortical epilepsy. Brain. 2004;127:1496–506. PubMed

Yuval-Greenberg S, Tomer O, Keren AS, Nelken I, Deouell LY. Transient induced gamma-band response in EEG as a manifestation of miniature saccades. Neuron. 2008;58:429–41. PubMed

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

High frequency oscillations in human memory and cognition: a neurophysiological substrate of engrams?

. 2024 Sep 03 ; 147 (9) : 2966-2982.

Phase-Amplitude Coupling Localizes Pathologic Brain with Aid of Behavioral Staging in Sleep

. 2023 May 15 ; 13 (5) : . [epub] 20230515

Intracranial electrophysiological recordings from the human brain during memory tasks with pupillometry

. 2022 Jan 13 ; 9 (1) : 6. [epub] 20220113

Cognitive Processing Impacts High Frequency Intracranial EEG Activity of Human Hippocampus in Patients With Pharmacoresistant Focal Epilepsy

. 2020 ; 11 () : 578571. [epub] 20201027

High frequency oscillations in epileptic and non-epileptic human hippocampus during a cognitive task

. 2020 Oct 23 ; 10 (1) : 18147. [epub] 20201023

Multicenter intracranial EEG dataset for classification of graphoelements and artifactual signals

. 2020 Jun 16 ; 7 (1) : 179. [epub] 20200616

Unsupervised machine-learning classification of electrophysiologically active electrodes during human cognitive task performance

. 2019 Nov 22 ; 9 (1) : 17390. [epub] 20191122

Multi-feature localization of epileptic foci from interictal, intracranial EEG

. 2019 Oct ; 130 (10) : 1945-1953. [epub] 20190805

Human Verbal Memory Encoding Is Hierarchically Distributed in a Continuous Processing Stream

. 2019 Jan-Feb ; 6 (1) : . [epub] 20190304

Physiological and pathological high frequency oscillations in focal epilepsy

. 2018 Sep ; 5 (9) : 1062-1076. [epub] 20180809

Pupil size reflects successful encoding and recall of memory in humans

. 2018 Mar 21 ; 8 (1) : 4949. [epub] 20180321

Spatial variation in high-frequency oscillation rates and amplitudes in intracranial EEG

. 2018 Feb 20 ; 90 (8) : e639-e646. [epub] 20180124

Electrical Stimulation Modulates High γ Activity and Human Memory Performance

. 2018 Jan-Feb ; 5 (1) : . [epub] 20180202

The CS algorithm: A novel method for high frequency oscillation detection in EEG

. 2018 Jan 01 ; 293 () : 6-16. [epub] 20170830

Progress and Remaining Challenges in the Application of High Frequency Oscillations as Biomarkers of Epileptic Brain

. 2017 Dec ; 4 () : 87-96. [epub] 20170922

Update on the mechanisms and roles of high-frequency oscillations in seizures and epileptic disorders

. 2017 Aug ; 58 (8) : 1330-1339. [epub] 20170706

The functional organization of human epileptic hippocampus

. 2016 Jun 01 ; 115 (6) : 3140-5. [epub] 20160330

Interictal high-frequency oscillations in focal human epilepsy

. 2016 Apr ; 29 (2) : 175-81.

Impact of cognitive stimulation on ripples within human epileptic and non-epileptic hippocampus

. 2015 Jul 25 ; 16 () : 47. [epub] 20150725

Gamma oscillations precede interictal epileptiform spikes in the seizure onset zone

. 2015 Feb 10 ; 84 (6) : 602-8. [epub] 20150114

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace