Gamma-band activity reflects multisensory matching in working memory

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.

[1]  Daniel Lenz,et al.  What's that sound? Matches with auditory long-term memory induce gamma activity in human EEG. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[2]  J. Pernier,et al.  Induced gamma-band activity during the delay of a visual short-term memory task in humans. , 1998, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  Werner Lutzenberger,et al.  Dynamics of Gamma-Band Activity during an Audiospatial Working Memory Task in Humans , 2002, The Journal of Neuroscience.

[4]  B. Argall,et al.  Integration of Auditory and Visual Information about Objects in Superior Temporal Sulcus , 2004, Neuron.

[5]  Matthias M. Müller,et al.  Induced gamma band responses: an early marker of memory encoding and retrieval , 2004, Neuroreport.

[6]  R. Elliott,et al.  Differential Neural Responses during Performance of Matching and Nonmatching to Sample Tasks at Two Delay Intervals , 1999, The Journal of Neuroscience.

[7]  Werner Lutzenberger,et al.  Hearing lips: gamma-band activity during audiovisual speech perception. , 2005, Cerebral cortex.

[8]  Daniel Senkowski,et al.  Good times for multisensory integration: Effects of the precision of temporal synchrony as revealed by gamma-band oscillations , 2007, Neuropsychologia.

[9]  A. Engel,et al.  Cognitive functions of gamma-band activity: memory match and utilization , 2004, Trends in Cognitive Sciences.

[10]  John J. Foxe,et al.  Oscillatory beta activity predicts response speed during a multisensory audiovisual reaction time task: a high-density electrical mapping study. , 2005, Cerebral cortex.

[11]  O. Jensen,et al.  Modulation of Gamma and Alpha Activity during a Working Memory Task Engaging the Dorsal or Ventral Stream , 2007, The Journal of Neuroscience.

[12]  Kara D. Federmeier,et al.  Electrophysiology reveals semantic memory use in language comprehension , 2000, Trends in Cognitive Sciences.

[13]  Catherine Tallon-Baudry,et al.  Induced γ-Band Activity during the Delay of a Visual Short-Term Memory Task in Humans , 1998, The Journal of Neuroscience.

[14]  W. Singer,et al.  Modulation of Neuronal Interactions Through Neuronal Synchronization , 2007, Science.

[15]  John J. Foxe,et al.  Multisensory visual-auditory object recognition in humans: a high-density electrical mapping study. , 2004, Cerebral cortex.

[16]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[17]  Guido Orgs,et al.  Conceptual priming for environmental sounds and words: An ERP study , 2006, Brain and Cognition.

[18]  Joseph A Maldjian,et al.  Cross‐modal sensory processing in the anterior cingulate and medial prefrontal cortices , 2003, Human brain mapping.

[19]  Burkhard Maess,et al.  Memory-matches evoke human gamma-responses , 2004, BMC Neuroscience.

[20]  M. Kutas,et al.  Reading between the lines: Event-related brain potentials during natural sentence processing , 1980, Brain and Language.

[21]  Daniel Senkowski,et al.  Multisensory processing and oscillatory gamma responses: effects of spatial selective attention , 2005, Experimental Brain Research.

[22]  Jonathan Grainger,et al.  An electrophysiological study of cross-modal repetition priming. , 2005, Psychophysiology.

[23]  P. Holcomb,et al.  Cross-modal semantic priming: A time-course analysis using event-related brain potentials , 1993 .

[24]  Stefan Debener,et al.  Multisensory identification of natural objects in a two-way crossmodal priming paradigm. , 2008, Experimental psychology.

[25]  Asif A. Ghazanfar,et al.  Integration of Bimodal Looming Signals through Neuronal Coherence in the Temporal Lobe , 2008, Current Biology.

[26]  John J. Foxe,et al.  Crossmodal binding through neural coherence: implications for multisensory processing , 2008, Trends in Neurosciences.

[27]  J. Kaiser,et al.  Human gamma-frequency oscillations associated with attention and memory , 2007, Trends in Neurosciences.

[28]  C. Schroeder,et al.  Neuronal Oscillations and Multisensory Interaction in Primary Auditory Cortex , 2007, Neuron.

[29]  D. Guthrie,et al.  Significance testing of difference potentials. , 1991, Psychophysiology.

[30]  John J. Foxe,et al.  Multisensory processing of naturalistic objects in motion: A high-density electrical mapping and source estimation study , 2007, NeuroImage.

[31]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[32]  A. Engel,et al.  What is novel in the novelty oddball paradigm? Functional significance of the novelty P3 event-related potential as revealed by independent component analysis. , 2005, Brain research. Cognitive brain research.

[33]  M. Fabiani,et al.  Naming norms for brief environmental sounds: effects of age and dementia. , 1996, Psychophysiology.

[34]  D. Tucker,et al.  Scalp electrode impedance, infection risk, and EEG data quality , 2001, Clinical Neurophysiology.

[35]  N. Logothetis,et al.  Visual modulation of neurons in auditory cortex. , 2008, Cerebral cortex.

[36]  Robert Oostenveld,et al.  Enhanced EEG gamma-band activity reflects multisensory semantic matching in visual-to-auditory object priming , 2008, NeuroImage.

[37]  Jean Vroomen,et al.  Neural Correlates of Multisensory Integration of Ecologically Valid Audiovisual Events , 2007, Journal of Cognitive Neuroscience.

[38]  M. Tervaniemi,et al.  Binding symbols and sounds: evidence from event-related oscillatory gamma-band activity. , 2007, Cerebral cortex.

[39]  A. Engel,et al.  High-frequency activity in human visual cortex is modulated by visual motion strength. , 2007, Cerebral cortex.

[40]  M. Kutas,et al.  Reading senseless sentences: brain potentials reflect semantic incongruity. , 1980, Science.