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Alterations in oscillatory cortical activity indicate changes in mnemonic processing during continuous item recognition

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Abstract

The classification of repeating stimuli as either old or new is a general mechanism of everyday perception. However, the cortical mechanisms underlying this process are not fully understood. In general, mnemonic processes are thought to rely on changes in oscillatory brain activity across several frequencies as well as their interaction. Lower frequencies, mainly theta-band (3–7 Hz) and alpha-band (8–14 Hz) activity, are attributed to executive control and resource management, respectively; whereas recent studies revealed higher frequencies, e.g. gamma-band (> 25 Hz) activity, to reflect the activation of cortical object representations. Furthermore, low-frequency phase to high-frequency amplitude coupling (PAC) was recently found to coordinate the involved mnemonic networks. To further unravel the processes behind memorization of repeatedly presented stimuli, we applied a continuous item recognition task with up to five presentations per item (mean time between repetitions ~ 10 s) while recording high-density EEG. We examined spectral amplitude modulations as well as PAC. We observed theta amplitudes reaching a peak at second presentation, a reduction of alpha suppression after second presentation, decreased response time, as well as reduced theta–gamma PAC (3 to 7 to − 30 to 45 Hz) at frontal sites after third presentation. We conclude a shift from an explicit- to an implicit-like mnemonic processing, occurring around third presentation, with theta power to signify encoding of repetition-based episodic information and PAC as a neural correlate of the coordination of local neural networks.

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References

  • Axmacher N, Henseler MM, Jensen O, Weinreich I, Elger CE, Fell J (2010) Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proc Natl Acad Sci 107(7):3228–3233

    Article  Google Scholar 

  • Bertrand O, Pantev C (1994) Stimulus frequency dependence of the transient oscillatory auditory evoked responses (40 Hz) studied by electric and magnetic recordings in human. In: Oscillatory event-related brain dynamics. Springer US, New York, pp 231–242

    Google Scholar 

  • Bertrand O, Tallon-Baudry C (2000) Oscillatory gamma activity in humans: a possible role for object representation. Int J Psychophysiol 38(3):211–223

    Article  CAS  PubMed  Google Scholar 

  • Brainard DH, Vision S (1997) The psychophysics toolbox. Spat Vis 10:433–436

    Article  CAS  PubMed  Google Scholar 

  • Burgess AP, Ali L (2002) Functional connectivity of gamma EEG activity is modulated at low frequency during conscious recollection. Int J Psychophysiol 46(2):91–100

    Article  PubMed  Google Scholar 

  • Canolty RT, Knight RT (2010) The functional role of cross-frequency coupling. Trends Cogn Sci 14(11):506–515

    Article  PubMed  PubMed Central  Google Scholar 

  • Canolty RT, Edwards E, Dalal SS, Soltani M, Nagarajan SS, Kirsch HE, Berger MS, Barbaro NM, Knight RT (2006) High gamma power is phase-locked to theta oscillations in human neocortex. Science 313(5793):1626–1628

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaumon M, Schwartz D, Tallon-Baudry C (2009) Unconscious learning versus visual perception: dissociable roles for gamma oscillations revealed in MEG. J Cogn Neurosci 21(12):2287–2299

    Article  PubMed  Google Scholar 

  • Cowan N (1999) An embedded-processes model of working memory. Models of working memory. Mech Active Maint Exec Control 20:506

    Google Scholar 

  • Cowan N (2008) What are the differences between long-term, short-term, and working memory? Progress Brain Res 169:323–338

    Article  Google Scholar 

  • Craddock M, Martinovic J, Müller MM (2016) Accounting for microsaccadic artifacts in the EEG using independent component analysis and beamforming. Psychophysiology 53(4):553–565

    Article  PubMed  Google Scholar 

  • Curran T (1999) The electrophysiology of incidental and intentional retrieval: erp old/ new effects in lexical decision and recognition memory. Neuropsychologia 37(7):771–785

    Article  CAS  PubMed  Google Scholar 

  • Daume J, Graetz S, Gruber T, Engel AK, Friese U (2017a) Cognitive control during audiovisual working memory engages frontotemporal theta-band interactions. Sci Rep 7(1):12585

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Daume J, Gruber T, Engel AK, Friese U (2017b) Phase-amplitude coupling and long-range phase synchronization reveal frontotemporal interactions during visual working memory. J Neurosci 37(2):313–322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delorme A, Makeig S (2004) EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134(1):9–21

    Article  PubMed  Google Scholar 

  • Fries P, Nikolić D, Singer W (2007) The gamma cycle. Trends Neurosci 30(7):309–316

    Article  CAS  PubMed  Google Scholar 

  • Friese U, Supp GG, Hipp JF, Engel AK, Gruber T (2012a) Oscillatory MEG gamma band activity dissociates perceptual and conceptual aspects of visual object processing: a combined repetition/conceptual priming study. Neuroimage 59(1):861–871

    Article  PubMed  Google Scholar 

  • Friese U, Rahm B, Hassler U, Kaiser J, Gruber T (2012b) Repetition suppression and effects of familiarity on blood oxygenation level dependent signal and gamma-band activity. Neuroreport 23(13):757–761

    Article  PubMed  Google Scholar 

  • Friese U, Köster M, Hassler U, Martens U, Trujillo-Barreto N, Gruber T (2013) Successful memory encoding is associated with increased cross-frequency coupling between frontal theta and posterior gamma oscillations in human scalp-recorded EEG. Neuroimage 66:642–647

    Article  PubMed  Google Scholar 

  • Gevins A, Smith ME, McEvoy L, Yu D (1997) High-resolution EEG mapping of cortical activation related to working memory: effects of task difficulty, type of processing, and practice. Cereb Cortex (New York, NY: 1991) 7(4):374–385

    Google Scholar 

  • Graf P, Schacter DL (1985) Implicit and explicit memory for new associations in normal andamnesic subjects. J Exp Psychol Learn Mem Cogn 11(3):501

    Article  CAS  PubMed  Google Scholar 

  • Gruber T, Müller MM (2006) Oscillatory brain activity in the human EEG during indirect and direct memory tasks. Brain Res 1097(1):194–204

    Article  CAS  PubMed  Google Scholar 

  • Gruber T, Tsivilis D, Montaldi D, Müller MM (2004) Induced gamma band responses: an early marker of memory encoding and retrieval. Neuroreport 15(11):1837–1841

    Article  PubMed  Google Scholar 

  • Gruber T, Tsivilis D, Giabbiconi CM, Müller MM (2008) Induced electroencephalogram oscillations during source memory: familiarity is reflected in the gamma band, recollection in the theta band. J Cogn Neurosci 20(6):1043–1053

    Article  PubMed  Google Scholar 

  • Hanslmayr S, Staudigl T (2014) How brain oscillations form memories—a processing based perspective on oscillatory subsequent memory effects. Neuroimage 85:648–655

    Article  PubMed  Google Scholar 

  • Hanslmayr S, Spitzer B, Bäuml KH (2008) Brain oscillations dissociate between semantic and nonsemantic encoding of episodic memories. Cereb Cortex 19(7):1631–1640

    Article  PubMed  Google Scholar 

  • Hassler U, Trujillo-Barreto N, Gruber T (2011) Induced gamma band responses in human EEG after the control of miniature saccadic artifacts. Neuroimage 57(4):1411–1421

    Article  PubMed  Google Scholar 

  • Hassler U, Friese U, Martens U, Trujillo-Barreto N, Gruber T (2013) Repetition priming effects dissociate between miniature eye movements and induced gamma-band responses in the human electroencephalogram. Eur J Neurosci 38(3):2425–2433

    Article  PubMed  Google Scholar 

  • Headley DB, Paré D (2017) Common oscillatory mechanisms across multiple memory systems. npj Sci Learn 2(1):1

    Article  PubMed  PubMed Central  Google Scholar 

  • Heusser AC, Poeppel D, Ezzyat Y, Davachi L (2016) Episodic sequence memory is supported by a theta–gamma phase code. Nat Neurosci 19(10):1374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacobs J, Hwang G, Curran T, Kahana MJ (2006) EEG oscillations and recognition memory: theta correlates of memory retrieval and decision making. Neuroimage 32(2):978–987

    Article  PubMed  Google Scholar 

  • Jensen O, Colgin LL (2007) Cross-frequency coupling between neuronal oscillations. Trends Cogn Sci 11(7):267–269

    Article  PubMed  Google Scholar 

  • Jensen O, Mazaheri A (2010) Shaping functional architecture by oscillatory alpha activity: gating by inhibition. Front Hum Neurosci 4:186

    Article  PubMed  PubMed Central  Google Scholar 

  • Jensen O, Kaiser J, Lachaux JP (2007) Human gamma-frequency oscillations associated with attention and memory. Trends Neurosci 30(7):317–324

    Article  CAS  PubMed  Google Scholar 

  • Johnson DR, Gronlund SD (2009) Individuals lower in working memory capacity are particularly vulnerable to anxiety’s disruptive effect on performance. Anxiety Stress Coping 22(2):201–213

    Article  PubMed  Google Scholar 

  • Johnson JD, Muftuler LT, Rugg MD (2008) Multiple repetitions reveal functionally and anatomically distinct patterns of hippocampal activity during continuous recognition memory. Hippocampus 18(10):975–980

    Article  PubMed  PubMed Central  Google Scholar 

  • Jokisch D, Jensen O (2007) Modulation of gamma and alpha activity during a working memory task engaging the dorsal or ventral stream. J Neurosci 27(12):3244–3251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jutras MJ, Buffalo EA (2010) Synchronous neural activity and memory formation. Curr Opin Neurobiol 20(2):150–155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kleiner M, Brainard D, Pelli D, Ingling A, Murray R, Broussard C (2007) What’s new in Psychtoolbox-3. Perception 36(14):1

    Google Scholar 

  • Klimesch W, Doppelmayr M, Schwaiger J, Winkler T, Gruber W (2000) Theta oscillations and the ERP old/new effect: independent phenomena? Clin Neurophysiol 111(5):781–793

    Article  CAS  PubMed  Google Scholar 

  • Klimesch W, Sauseng P, Hanslmayr S (2007) EEG alpha oscillations: the inhibition-timing hypothesis. Brain Res Rev 53(1):63–88

    Article  PubMed  Google Scholar 

  • Köster M, Friese U, Schöne B, Trujillo-Barreto N, Gruber T (2014) Theta–gamma coupling during episodic retrieval in the human EEG. Brain Res 1577:57–68

    Article  PubMed  CAS  Google Scholar 

  • Kramer MA, Tort AB, Kopell NJ (2008) Sharp edge artifacts and spurious coupling in EEG frequency comodulation measures. J Neurosci Methods 170(2):352–357

    Article  PubMed  Google Scholar 

  • LaRocque JJ, Lewis-Peacock JA, Drysdale AT, Oberauer K, Postle BR (2013) Decoding attended information in short-term memory: an EEG study. J Cogn Neurosci 25(1):127–142

    Article  PubMed  PubMed Central  Google Scholar 

  • Lewis-Peacock JA, Drysdale AT, Oberauer K, Postle BR (2012) Neural evidence for a distinction between short-term memory and the focus of attention. J Cogn Neurosci 24(1):61–79

    Article  PubMed  Google Scholar 

  • Lisman JE, Jensen O (2013) The theta-gamma neural code. Neuron 77(6):1002–1016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mormann F, Fell J, Axmacher N, Weber B, Lehnertz K, Elger CE, Fernández G (2005) Phase/amplitude reset and theta–gamma interaction in the human medial temporal lobe during a continuous word recognition memory task. Hippocampus 15(7):890–900

    Article  PubMed  Google Scholar 

  • Nolan H, Whelan R, Reilly RB (2010) FASTER: fully automated statistical thresholding for EEG artifact rejection. J Neurosci Methods 192(1):152–162

    Article  CAS  PubMed  Google Scholar 

  • Nyhus E, Curran T (2010) Functional role of gamma and theta oscillations in episodic memory. Neurosci Biobehav Rev 34(7):1023–1035

    Article  PubMed  PubMed Central  Google Scholar 

  • Osipova D, Takashima A, Oostenveld R, Fernández G, Maris E, Jensen O (2006) Theta and gamma oscillations predict encoding and retrieval of declarative memory. J Neurosci 26(28):7523–7531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roux F, Uhlhaas PJ (2014) Working memory and neural oscillations: alpha–gamma versus theta–gamma codes for distinct WM information? Trends Cogn Sci 18(1):16–25

    Article  PubMed  Google Scholar 

  • Ruchkin DS, Grafman J, Cameron K, Berndt RS (2003) Working memory retention systems: a state of activated long-term memory. Behav Brain Sci 26(6):709–728

    Article  PubMed  Google Scholar 

  • Rugg MD, Curran T (2007) Event-related potentials and recognition memory. Trends Cogn Sci 11(6):251–257

    Article  PubMed  Google Scholar 

  • Sarnthein J, Petsche H, Rappelsberger P, Shaw GL, Von Stein A (1998) Synchronization between prefrontal and posterior association cortex during human working memory. Proc Natl Acad Sci 95(12):7092–7096

    Article  Google Scholar 

  • Sauseng P, Klimesch W, Doppelmayr M, Hanslmayr S, Schabus M, Gruber WR (2004) Theta coupling in the human electroencephalogram during a working memory task. Neurosci Lett 354(2):123–126

    Article  CAS  PubMed  Google Scholar 

  • Sauseng P, Klimesch W, Schabus M, Doppelmayr M (2005) Fronto-parietal EEG coherence in theta and upper alpha reflect central executive functions of working memory. Int J Psychophysiol 57(2):97–103

    Article  PubMed  Google Scholar 

  • Sauseng P, Griesmayr B, Freunberger R, Klimesch W (2010) Control mechanisms in working memory: a possible function of EEG theta oscillations. Neurosci Biobehav Rev 34(7):1015–1022

    Article  PubMed  Google Scholar 

  • Sederberg PB, Kahana MJ, Howard MW, Donner EJ, Madsen JR (2003) Theta and gamma oscillations during encoding predict subsequent recall. J Neurosci 23(34):10809–10814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sederberg PB, Gauthier LV, Terushkin V, Miller JF, Barnathan JA, Kahana MJ (2006) Oscillatory correlates of the primacy effect in episodic memory. NeuroImage 32(3):1422–1431

    Article  PubMed  Google Scholar 

  • Sirota A, Montgomery S, Fujisawa S, Isomura Y, Zugaro M, Buzsáki G (2008) Entrainment of neocortical neurons and gamma oscillations by the hippocampal theta rhythm. Neuron 60(4):683–697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tallon-Baudry C, Bertrand O (1999) Oscillatory gamma activity in humans and its role in object representation. Trends Cogn Sci 3(4):151–162

    Article  CAS  PubMed  Google Scholar 

  • Tort AB, Komorowski R, Eichenbaum H, Kopell N (2010) Measuring phase-amplitude coupling between neuronal oscillations of different frequencies. J Neurophysiol 104(2):1195–1210

    Article  PubMed  PubMed Central  Google Scholar 

  • Tulving E, Schacter DL (1990) Priming and human memory systems. Science 247(4940):301–306

    Article  CAS  PubMed  Google Scholar 

  • Vidal JR, Chaumon M, O’Regan JK, Tallon-Baudry C (2006) Visual grouping and the focusing of attention induce gamma-band oscillations at different frequencies in human magnetoencephalogram signals. J Cogn Neurosci 18(11):1850–1862

    Article  PubMed  Google Scholar 

  • Wiggs CL, Martin A (1998) Properties and mechanisms of perceptual priming. Curr Opin Neurobiol 8(2):227–233

    Article  CAS  PubMed  Google Scholar 

  • Wixted JT (2007) Dual-process theory and signal-detection theory of recognition memory. Psychol Rev 114(1):152

    Article  PubMed  Google Scholar 

  • Xu Y (2017) Reevaluating the sensory account of visual working memory storage. Trends Cogn Sci 21(10):794–815

    Article  PubMed  Google Scholar 

  • Yassa MA, Stark CE (2008) Multiple signals of recognition memory in the medial temporal lobe. Hippocampus 18(9):945–954

    Article  PubMed  Google Scholar 

  • Yonelinas AP (2002) The nature of recollection and familiarity: a review of 30 years of research. J Mem Lang 46(3):441–517

    Article  Google Scholar 

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Acknowledgements

This work was supported by grants from the German Research Foundation (GR2684/5-1). We thank Moritz Köster for helpful methodological discussions, and Simeon Platte, Sophia Sylvester and Marlene Wessels for assistance in data recording.

Funding

This work was supported by grants from the German Research Foundation (GR2684/5-1).

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Authors and Affiliations

  1. Experimental Psychology I, Institute of Psychology, Osnabrück University, Neuer Graben 29, 49074, Osnabrück, Germany

    Sebastian Graetz, Uwe Friese & Thomas Gruber

  2. Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, Martinistraße 52, 20246, Hamburg, Germany

    Jonathan Daume

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  1. Sebastian Graetz
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  2. Jonathan Daume
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  3. Uwe Friese
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Correspondence to Sebastian Graetz.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the Osnabrück University and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. This study was reviewed and approved by the local ethics committee of Osnabrück University.

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Graetz, S., Daume, J., Friese, U. et al. Alterations in oscillatory cortical activity indicate changes in mnemonic processing during continuous item recognition. Exp Brain Res 237, 573–583 (2019). https://doi.org/10.1007/s00221-018-5439-4

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