Behavioral stochastic resonance associated with large-scale synchronization of human brain activity

We demonstrate experimentally that enhanced detection of weak visual signals by addition of visual noise is accompanied by an increase in phase synchronization of EEG signals across widely-separated areas of the human brain. In our sensorimotor integration task, observers responded to a weak rectangular gray-level signal presented to their right eyes by pressing and releasing a button whenever they detected an increment followed by a decrement in brightness. Signal detection performance was optimized by presenting randomly-changing-gray-level noise separately to observers' left eyes using a mirror stereoscope. We measured brain electrical activity at the scalp by electroencephalograph (EEG), calculated the instantaneous phase for each EEG signal, and evaluated the degree of large-scale phase synchronization between pairs of EEG signals. Dynamic synchronization-desynchronization patterns were observed and we found evidence of noise-enhanced large-scale synchronization associated with detection of the brightness changes under conditions of noise-enhanced performance. Our results suggest that behavioral stochastic resonance might arise from noise-enhanced synchronization of neural activities across widespread brain regions.

[1]  Fan-Gang Zeng,et al.  Human hearing enhanced by noise 1 1 Published on the World Wide Web on 23 May 2000. , 2000, Brain Research.

[2]  James J. Collins,et al.  Noise-Enhanced Human Sensorimotor Function Using Stochastic Resonance to Enhance Somatosensation and Improve Performance of the Human Balance Control System , 2003 .

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

[4]  Jürgen Kurths,et al.  Detection of n:m Phase Locking from Noisy Data: Application to Magnetoencephalography , 1998 .

[5]  L. M. Ward,et al.  Stochastic resonance enhances the electrosensory information available to paddlefish for prey capture. , 2000, Physical review letters.

[6]  John P. Miller,et al.  Broadband neural encoding in the cricket cereal sensory system enhanced by stochastic resonance , 1996, Nature.

[7]  R Quian Quiroga,et al.  Performance of different synchronization measures in real data: a case study on electroencephalographic signals. , 2002, Physical review. E, Statistical, nonlinear, and soft matter physics.

[8]  Frank Moss,et al.  Use of behavioural stochastic resonance by paddle fish for feeding , 1999, Nature.

[9]  Frank Moss,et al.  Noise enhancement of information transfer in crayfish mechanoreceptors by stochastic resonance , 1993, Nature.

[10]  E. Evans,et al.  Enhancement of vowel coding for cochlear implants by addition of noise , 1996, Nature Medicine.

[11]  W. Stacey,et al.  Stochastic resonance improves signal detection in hippocampal CA1 neurons. , 2000, Journal of neurophysiology.

[12]  Alexander B. Neiman,et al.  Stochastic resonance in psychophysics and in animal behavior , 2002, Biological Cybernetics.

[13]  A. Kleinschmidt,et al.  Electroencephalographic signatures of attentional and cognitive default modes in spontaneous brain activity fluctuations at rest , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Massimo Riani,et al.  Role of noise in image processing by the human perceptive system. , 2000 .

[15]  M. Morillo,et al.  Stochastic resonance in a mean-field model of cooperative behavior. , 1995, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[16]  Bernd Pompe,et al.  Ranking and Entropy Estimation in Nonlinear Time Series Analysis , 1998 .

[17]  S Setoguchi,et al.  Noise-enhanced heart rate and sympathetic nerve responses to oscillatory lower body negative pressure in humans. , 2001, Journal of neurophysiology.

[18]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[19]  Ditto,et al.  Stochastic Resonance in a Neuronal Network from Mammalian Brain. , 1996, Physical review letters.

[20]  Neil A. Macmillan,et al.  Detection Theory: A User's Guide , 1991 .

[21]  W. Stacey,et al.  Synaptic noise improves detection of subthreshold signals in hippocampal CA1 neurons. , 2001, Journal of neurophysiology.

[22]  Jung,et al.  Collective response in globally coupled bistable systems. , 1992, Physical review. A, Atomic, molecular, and optical physics.

[23]  L Schimansky-Geier,et al.  Synchronization of noisy systems by stochastic signals. , 1999, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[24]  Bulsara,et al.  Scaling laws for spatiotemporal synchronization and array enhanced stochastic resonance. , 1996, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[25]  Thomas T. Imhoff,et al.  Using electrical noise to enhance the ability of humans to detect subthreshold mechanical cutaneous stimuli. , 1998, Chaos.

[26]  Jürgen Kurths,et al.  Synchronization - A Universal Concept in Nonlinear Sciences , 2001, Cambridge Nonlinear Science Series.

[27]  R. Srebro,et al.  Stochastic resonance of the visually evoked potential , 1999 .

[28]  W. Klimesch EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis , 1999, Brain Research Reviews.

[29]  L. M. Ward,et al.  Synchronous neural oscillations and cognitive processes , 2003, Trends in Cognitive Sciences.

[30]  Thomas T. Imhoff,et al.  Noise-enhanced tactile sensation , 1996, Nature.

[31]  Lawrence M. Ward,et al.  Behavioral stochastic resonance in the human brain , 2003, SPIE International Symposium on Fluctuations and Noise.

[32]  W. Singer,et al.  Visuomotor integration is associated with zero time-lag synchronization among cortical areas , 1997, Nature.

[33]  Bulsara,et al.  Nonlinear dynamic elements with noisy sinusoidal forcing: Enhancing response via nonlinear coupling. , 1995, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[34]  D Nozaki,et al.  Functional stochastic resonance in the human brain: noise induced sensitization of baroreflex system. , 2000, Physical review letters.

[35]  L M Ward,et al.  Statistical analysis of stochastic resonance in a simple setting. , 1999, Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics.

[36]  Kurt Wiesenfeld,et al.  Stochastic resonance and the benefits of noise: from ice ages to crayfish and SQUIDs , 1995, Nature.

[37]  Dekang Lin,et al.  Automatic Identification of Non-compositional Phrases , 1999, ACL.

[38]  Shoichi Kai,et al.  Noise-induced entrainment and stochastic resonance in human brain waves. , 2002, Physical review letters.

[39]  Thomas T. Imhoff,et al.  Noise-enhanced information transmission in rat SA1 cutaneous mechanoreceptors via aperiodic stochastic resonance. , 1996, Journal of neurophysiology.

[40]  Keiichi Kitajo,et al.  Behavioral stochastic resonance within the human brain. , 2003, Physical review letters.

[41]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.