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Gamma-band activity reflects multisensory matching in working memory

Experimental Brain Research volume 198, pages 363–372 (2009)Cite this article

Abstract

In real-world situations, the integration of sensory information in working memory (WM) is an important mechanism for the recognition of objects. Studies in single sensory modalities show that object recognition is facilitated if bottom-up inputs match a template held in WM, and that this effect may be linked to enhanced synchronization of neurons in the gamma-band (>30 Hz). Natural objects, however, frequently provide inputs to multiple sensory modalities. In this EEG study, we examined the integration of semantically matching or non-matching visual and auditory inputs using a delayed visual-to-auditory object-matching paradigm. In the event-related potentials (ERPs) triggered by auditory inputs, effects of semantic matching were observed after 120–170 ms at frontal and posterior regions, indicating WM-specific processing across modalities, and after 250–400 ms over medial-central regions, possibly reflecting the contextual integration of sensory inputs. Additionally, total gamma-band activity (GBA) with medial-central topography after 120–180 ms was larger for matching compared to non-matching trials. This demonstrates that multisensory matching in WM is reflected by GBA and that dynamic coupling of neural populations in this frequency range might be a crucial mechanism for integrative multisensory processes.

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References

  • Beauchamp MS, Lee KE, Argall BD, Martin A (2004) Integration of auditory and visual information about objects in superior temporal sulcus. Neuron 41:809–823

    Article  PubMed  CAS  Google Scholar 

  • Debener S, Makeig S, Delorme A, Engel AK (2005) What is novel in the novelty oddball paradigm? Functional significance of the novelty P3 event-related potential as revealed by independent component analysis. Brain Res Cogn Brain Res 22:309–321

    Article  PubMed  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 134:9–21

    Article  PubMed  Google Scholar 

  • Elliott R, Dolan RJ (1999) Differential neural responses during performance of matching and nonmatching to sample tasks at two delay intervals. J Neurosci 19:5066–5073

    PubMed  CAS  Google Scholar 

  • Engel AK, Fries P, Singer W (2001) Dynamic predictions: oscillations and synchrony in top–down processing. Nat Rev Neurosci 2:704–716

    Article  PubMed  CAS  Google Scholar 

  • Fabiani M, Kazmerski VA, Cycowicz YM, Friedman D (1996) Naming norms for brief environmental sounds: effects of age and dementia. Psychophysiology 33:462–475

    Article  PubMed  CAS  Google Scholar 

  • Ferree TC, Luu P, Russel GS, Tucker DM (2001) Scalp electrode impedance, infection risk, and EEG data quality. Clin Neurophysiol 112:536–544

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Guthrie D, Buchwald JS (1991) Significance testing of difference potentials. Psychophysiology 28:240–244

    Article  PubMed  CAS  Google Scholar 

  • Herrmann CS, Lenz D, Junge S, Busch NA, Maess B (2004a) Memory-matches evoke human gamma-responses. BMC Neurosci 5:13

    Article  PubMed  Google Scholar 

  • Herrmann CS, Munk MH, Engel AK (2004b) Cognitive functions of gamma-band activity: memory match and utilization. Trends Cogn Sci 8:347–355

    Article  PubMed  Google Scholar 

  • Holcomb PJ, Anderson JE (1993) Cross-modal semantic priming: a time-course analysis using event-related potentials. Lang Cogn Process 8:33

    Google Scholar 

  • Holcomb PJ, Anderson J, Grainger J (2005) An electrophysiological study of cross-modal repetition priming. Psychophysiology 42:493–507

    PubMed  Google Scholar 

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

    Article  PubMed  CAS  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 27:3244–3251

    Article  PubMed  CAS  Google Scholar 

  • Kaiser J, Hertrich I, Ackermann H, Mathiak K, Lutzenberger W (2005) Hearing lips: gamma-band activity during audiovisual speech perception. Cereb Cortex 15:646–653

    Article  PubMed  Google Scholar 

  • Kayser C, Petkov C, Logothetis NK (2008) Visual modulation of neurons in auditory cortex. Cereb Cortex 18:1560–1574

    Article  PubMed  Google Scholar 

  • Kutas M, Federmeier KD (2000) Electrophysiology reveals semantic memory use in language comprehension. Trends Cogn Sci 4:463–470

    Article  PubMed  Google Scholar 

  • Kutas M, Hillyard SA (1980a) Reading between the lines: event-related brain potentials during natural sentence processing. Brain Lang 11:354–373

    Article  PubMed  CAS  Google Scholar 

  • Kutas M, Hillyard SA (1980b) Reading senseless sentences: brain potentials reflect semantic incongruity. Science 207:203–205

    Article  PubMed  CAS  Google Scholar 

  • Lakatos P, Chen CM, O’Connell MN, Mills A, Schroeder CE (2007) Neuronal oscillations and multisensory interaction in primary auditory cortex. Neuron 53:279–292

    Article  PubMed  CAS  Google Scholar 

  • Laurienti PJ, Wallace MT, Maldjian JA, Susi CM, Stein BE, Burdette JH (2003) Cross-modal sensory processing in the anterior cingulate and medial prefrontal cortices. Hum Brain Mapp 19:213–223

    Article  PubMed  Google Scholar 

  • Lenz D, Schadow J, Thaerig S, Busch NA, Herrmann CS (2007) What’s that sound? Matches with auditory long-term memory induce gamma activity in human EEG. Int J Psychophysiol 64:31–38

    Article  PubMed  Google Scholar 

  • Lutzenberger W, Ripper B, Busse L, Birbaumer N, Kaiser J (2002) Dynamics of gamma-band activity during an audiospatial working memory task in humans. J Neurosci 22:5630–5638

    PubMed  CAS  Google Scholar 

  • Maier JX, Chandrasekaran C, Ghazanfar AA (2008) Integration of bimodal looming signals through neuronal coherence in the temporal lobe. Curr Biol 18:963–968

    Article  PubMed  CAS  Google Scholar 

  • Molholm S, Ritter W, Javitt DC, Foxe JJ (2004) Multisensory visual-auditory object recognition in humans: a high-density electrical mapping study. Cereb Cortex 14:452–465

    Article  PubMed  Google Scholar 

  • Orgs G, Lange K, Dombrowski JH, Heil M (2006) Conceptual priming for environmental sounds and words: an ERP study. Brain Cogn 62:267–272

    Article  PubMed  Google Scholar 

  • Schneider T, Engel AK, Debener S (2008a) Multisensory identification of natural objects in a two-way crossmodal priming paradigm. Exp Psychol 55:121–132

    PubMed  Google Scholar 

  • Schneider TR, Debener S, Oostenveld R, Engel AK (2008b) Enhanced EEG gamma-band activity reflects multisensory semantic matching in visual-to-auditory object priming. Neuroimage 42:1244–1254

    Article  PubMed  Google Scholar 

  • Senkowski D, Talsma D, Herrmann CS, Woldorff MG (2005) Multisensory processing and oscillatory gamma responses: effects of spatial selective attention. Exp Brain Res 3–4:411–426

    Article  Google Scholar 

  • Senkowski D, Molholm S, Gomez-Ramirez M, Foxe JJ (2006) Oscillatory beta activity predicts response speed during a multisensory audiovisual reaction time task: a high-density electrical mapping study. Cereb Cortex 16:1556–1565

    Article  PubMed  Google Scholar 

  • Senkowski D, Saint-Amour D, Kelly SP, Foxe JJ (2007a) Multisensory processing of naturalistic objects in motion: a high-density electrical mapping and source estimation study. Neuroimage 36:877–888

    Article  PubMed  Google Scholar 

  • Senkowski D, Talsma D, Grigutsch M, Herrmann CS, Woldorff MG (2007b) Good times for multisensory integration: effects of the precision of temporal synchrony as revealed by gamma-band oscillations. Neuropsychologia 45:561–571

    Article  PubMed  Google Scholar 

  • Senkowski D, Schneider TR, Foxe JJ, Engel AK (2008) Crossmodal binding through neural coherence: implications for multisensory processing. Trends Neurosci 31:401–409

    Article  PubMed  CAS  Google Scholar 

  • Siegel M, Donner TH, Oostenveld R, Fries P, Engel AK (2007) High-frequency activity in human visual cortex is modulated by visual motion strength. Cereb Cortex 17:732–741

    Article  PubMed  Google Scholar 

  • Stekelenburg JJ, Vroomen J (2007) Neural correlates of multisensory integration of ecologically valid audiovisual events. J Cogn Neurosci 19:1964–1973

    Article  PubMed  Google Scholar 

  • Tallon-Baudry C, Bertrand O, Peronnet F, Pernier J (1998) Induced gamma-band activity during the delay of a visual short-term memory task in humans. J Neurosci 18:4244–4254

    PubMed  CAS  Google Scholar 

  • Widmann A, Gruber T, Kujala T, Tervaniemi M, Schroger E (2007) Binding symbols and sounds: evidence from event-related oscillatory gamma-band activity. Cereb Cortex 17:2696

    Article  PubMed  Google Scholar 

  • Womelsdorf T, Schoffelen JM, Oostenveld R, Singer W, Desimone R, Engel AK, Fries P (2007) Modulation of neuronal interactions through neuronal synchronization. Science 316:1609–1612

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank Kriemhild Saha and Inga Fitzner for help during data acquisition and Inga Schepers and Hanna Krause for help during data acquisition and analysis. D.S. received support from a NARSAD 2006 young investigator award and the German Research Foundation (SE 1859/1-1). A.K.E. acknowledges support by the European Union (IST-2005-027268, NEST-PATH-043457, HEALTH-F2-2008-200728), the German Research Foundation (GRK 1247/1), the German Federal Ministry of Education and Research (01GW0561) and the Volkswagen Foundation (II/80609).

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Authors and Affiliations

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

    Daniel Senkowski, Till R. Schneider, Frithjof Tandler & Andreas K. Engel

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  1. Daniel Senkowski
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  2. Till R. Schneider
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  3. Frithjof Tandler
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  4. Andreas K. Engel
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Correspondence to Daniel Senkowski.

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Daniel Senkowski and Till R. Schneider contributed equally to the manuscript.

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Senkowski, D., Schneider, T.R., Tandler, F. et al. Gamma-band activity reflects multisensory matching in working memory. Exp Brain Res 198, 363–372 (2009). https://doi.org/10.1007/s00221-009-1835-0

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  • DOI: https://doi.org/10.1007/s00221-009-1835-0

Keywords

  • Multisensory
  • Crossmodal
  • Working memory
  • Gamma
  • EEG