Decreased beta-band activity is correlated with disambiguation of hidden figures

Insight is commonly described as sudden comprehension, sometimes called an "Aha! moment." In everyday life, we apply the process of insight to problems that are difficult to solve at first glance or that we perceive as ambiguous; however the brain dynamics underlying the disambiguation process remains elusive. Beta-band oscillatory brain activity has been hypothesized to reflect the transition of cognitive states. To elucidate the neural mechanism of insight, we recorded electroencephalograms while subjects were presented with hidden figures followed by unambiguous, gray images. We identified oscillatory activity to detect temporal changes, and compared brain activity that occurred during a perceptual transition with activity that occurred when no perceptual transition occurred. Statistical comparison confirmed stronger beta-power decrease during perceptual transition. Source analysis indicated that the beta-power decrease was around the parietal-posterior regions, mainly in the precuneus. We propose that beta-band desynchronization in the parietal-posterior regions reflects the disambiguation process, and our findings provide additional support for the theory that beta-band activity is related to the transition of cognitive state.

[1]  Gert Pfurtscheller,et al.  SHORT COMMUNICATIONS: Semantic memory retrieval: cortical couplings in object recognition in the N400 window , 2005, The European journal of neuroscience.

[2]  Bhavin R. Sheth,et al.  Posterior Beta and Anterior Gamma Oscillations Predict Cognitive Insight , 2009, Journal of Cognitive Neuroscience.

[3]  Pejman Sehatpour,et al.  A human intracranial study of long-range oscillatory coherence across a frontal–occipital–hippocampal brain network during visual object processing , 2008, Proceedings of the National Academy of Sciences.

[4]  Masato Yumoto,et al.  Perceptual change in response to a bistable picture increases neuromagnetic beta-band activities , 2008, Neuroscience Research.

[5]  Catherine Tallon-Baudry,et al.  Unconscious Learning versus Visual Perception: Dissociable Roles for Gamma Oscillations Revealed in MEG , 2009, Journal of Cognitive Neuroscience.

[6]  N. Kanwisher,et al.  Recognition alters the spatial pattern of FMRI activation in early retinotopic cortex. , 2010, Journal of neurophysiology.

[7]  W. Singer,et al.  Neuroelectromagnetic Correlates of Perceptual Closure Processes , 2010, The Journal of Neuroscience.

[8]  Bruno Rossion,et al.  Human non-phase-locked gamma oscillations in experience-based perception of visual scenes , 2004, Neuroscience Letters.

[9]  O. Jensen,et al.  Neuromagnetic localization of rhythmic activity in the human brain: a comparison of three methods , 2005, NeuroImage.

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

[11]  Maria Pia Viggiano,et al.  Involvement of the parietal cortex in perceptual learning (Eureka effect): An interference approach using rTMS , 2010, Neuropsychologia.

[12]  Roger D. Traub,et al.  Long-Range Synchronization of γ and β Oscillations and the Plasticity of Excitatory and Inhibitory Synapses: A Network Model , 2002 .

[13]  R N Henson,et al.  Mechanisms of top-down facilitation in perception of visual objects studied by FMRI. , 2007, Cerebral cortex.

[14]  D. Hassabis,et al.  Using Imagination to Understand the Neural Basis of Episodic Memory , 2007, The Journal of Neuroscience.

[15]  C. Tallon-Baudry,et al.  How Ongoing Fluctuations in Human Visual Cortex Predict Perceptual Awareness: Baseline Shift versus Decision Bias , 2009, The Journal of Neuroscience.

[16]  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.

[17]  Mark E Wheeler,et al.  Functional-anatomic correlates of remembering and knowing , 2004, NeuroImage.

[18]  Caspar M. Schwiedrzik,et al.  Expectations Change the Signatures and Timing of Electrophysiological Correlates of Perceptual Awareness , 2011, The Journal of Neuroscience.

[19]  Margot J. Taylor,et al.  Holistic Processing of Faces: Learning Effects with Mooney Faces , 2005, Journal of Cognitive Neuroscience.

[20]  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.

[21]  Aniruddh D. Patel,et al.  Top‐Down Control of Rhythm Perception Modulates Early Auditory Responses , 2009, Annals of the New York Academy of Sciences.

[22]  R. Oostenveld,et al.  Theta and Gamma Oscillations Predict Encoding and Retrieval of Declarative Memory , 2006, The Journal of Neuroscience.

[23]  John J. B. Allen,et al.  EEG phase synchrony differences across visual perception conditions may depend on recording and analysis methods , 2005, Clinical Neurophysiology.

[24]  F. Tong,et al.  The timing of perceptual decisions for ambiguous face stimuli in the human ventral visual cortex. , 2006, Cerebral cortex.

[25]  O. Bertrand,et al.  Oscillatory Synchrony between Human Extrastriate Areas during Visual Short-Term Memory Maintenance , 2001, The Journal of Neuroscience.

[26]  Robert Oostenveld,et al.  Brain symmetry and topographic analysis of lateralized event-related potentials , 2003, Clinical Neurophysiology.

[27]  Matthias M. Müller,et al.  Repetition suppression of induced gamma band responses is eliminated by task switching , 2006, The European journal of neuroscience.

[28]  D. C. Mccarthy,et al.  Hippocampal and neocortical gamma oscillations predict memory formation in humans. , 2006, Cerebral cortex.

[29]  Michael Bach,et al.  Ambiguous Figures and Binding: Eeg Frequency Modulations during Multistable Perception , 2022 .

[30]  D. Eagleman,et al.  Beta oscillations correlate with the probability of perceiving rivalrous visual stimuli. , 2010, Journal of vision.

[31]  Matthias M. Müller,et al.  Oscillatory brain activity dissociates between associative stimulus content in a repetition priming task in the human EEG. , 2004, Cerebral cortex.

[32]  Stephen A. Engel,et al.  Neural Response to Perception of Volume in the Lateral Occipital Complex , 2001, Neuron.

[33]  Leslie G. Ungerleider,et al.  Distributed Neural Systems for the Generation of Visual Images , 2000, Neuron.

[34]  J. Hegdé,et al.  A Link between Visual Disambiguation and Visual Memory , 2010, The Journal of Neuroscience.

[35]  Karl J. Friston,et al.  How the brain learns to see objects and faces in an impoverished context , 1997, Nature.

[36]  Florin Dolcos,et al.  Attention-related activity during episodic memory retrieval: a cross-function fMRI study , 2003, Neuropsychologia.

[37]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[38]  Bruna Velasques,et al.  Minor and Unsystematic Cortical Topographic Changes of Attention Correlates between Modalities , 2010, PloS one.

[39]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[40]  R. Eckhorn,et al.  Perception-related modulations of local field potential power and coherence in primary visual cortex of awake monkey during binocular rivalry. , 2004, Cerebral cortex.

[41]  G. Ermentrout,et al.  Gamma rhythms and beta rhythms have different synchronization properties. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[42]  J. Pernier,et al.  Oscillatory γ-Band (30–70 Hz) Activity Induced by a Visual Search Task in Humans , 1997, The Journal of Neuroscience.

[43]  F. Varela,et al.  Perception's shadow: long-distance synchronization of human brain activity , 1999, Nature.

[44]  Anthony D. Wagner,et al.  Neural Priming in Human Frontal Cortex: Multiple Forms of Learning Reduce Demands on the Prefrontal Executive System , 2009, Journal of Cognitive Neuroscience.

[45]  Denis Schluppeck,et al.  Neural responses to Mooney images reveal a modular representation of faces in human visual cortex , 2004, NeuroImage.

[46]  T. Kjaer,et al.  Precuneus–Prefrontal Activity during Awareness of Visual Verbal Stimuli , 2001, Consciousness and Cognition.

[47]  Markus Butz,et al.  Task-dependent oscillations during unimanual and bimanual movements in the human primary motor cortex and SMA studied with magnetoencephalography , 2005, NeuroImage.

[48]  Mirka Pesonen,et al.  Brain oscillatory 4–30 Hz responses during a visual n-back memory task with varying memory load , 2007, Brain Research.