Transcranial Random Noise Stimulation of Visual Cortex: Stochastic Resonance Enhances Central Mechanisms of Perception

Random noise enhances the detectability of weak signals in nonlinear systems, a phenomenon known as stochastic resonance (SR). Though counterintuitive at first, SR has been demonstrated in a variety of naturally occurring processes, including human perception, where it has been shown that adding noise directly to weak visual, tactile, or auditory stimuli enhances detection performance. These results indicate that random noise can push subthreshold receptor potentials across the transfer threshold, causing action potentials in an otherwise silent afference. Despite the wealth of evidence demonstrating SR for noise added to a stimulus, relatively few studies have explored whether or not noise added directly to cortical networks enhances sensory detection. Here we administered transcranial random noise stimulation (tRNS; 100–640 Hz zero-mean Gaussian white noise) to the occipital region of human participants. For increasing tRNS intensities (ranging from 0 to 1.5 mA), the detection accuracy of a visual stimuli changed according to an inverted-U-shaped function, typical of the SR phenomenon. When the optimal level of noise was added to visual cortex, detection performance improved significantly relative to a zero noise condition (9.7 ± 4.6%) and to a similar extent as optimal noise added to the visual stimuli (11.2 ± 4.7%). Our results demonstrate that adding noise to cortical networks can improve human behavior and that tRNS is an appropriate tool to exploit this mechanism. SIGNIFICANCE STATEMENT Our findings suggest that neural processing at the network level exhibits nonlinear system properties that are sensitive to the stochastic resonance phenomenon and highlight the usefulness of tRNS as a tool to modulate human behavior. Since tRNS can be applied to all cortical areas, exploiting the SR phenomenon is not restricted to the perceptual domain, but can be used for other functions that depend on nonlinear neural dynamics (e.g., decision making, task switching, response inhibition, and many other processes). This will open new avenues for using tRNS to investigate brain function and enhance the behavior of healthy individuals or patients.

[1]  Carlo Miniussi,et al.  What do you feel if I apply transcranial electric stimulation? Safety, sensations and secondary induced effects , 2015, Clinical Neurophysiology.

[2]  M. Carrasco,et al.  Covert attention affects the psychometric function of contrast sensitivity , 2002, Vision Research.

[3]  C. Miniussi,et al.  The Role of Timing in the Induction of Neuromodulation in Perceptual Learning by Transcranial Electric Stimulation , 2013, Brain Stimulation.

[4]  A. Antal,et al.  Transcranial random noise stimulation-induced plasticity is NMDA-receptor independent but sodium-channel blocker and benzodiazepines sensitive , 2015, Front. Neurosci..

[5]  L. M. Ward,et al.  Stochastic resonance and sensory information processing: a tutorial and review of application , 2004, Clinical Neurophysiology.

[6]  M. Bikson,et al.  Role of cortical cell type and morphology in subthreshold and suprathreshold uniform electric field stimulation in vitro , 2009, Brain Stimulation.

[7]  H. Sasaki,et al.  Subthreshold noise facilitates the detection and discrimination of visual signals , 2008, Neuroscience Letters.

[8]  A. Antal,et al.  Increasing Human Brain Excitability by Transcranial High-Frequency Random Noise Stimulation , 2008, The Journal of Neuroscience.

[9]  C. Miniussi,et al.  Random Noise Stimulation Improves Neuroplasticity in Perceptual Learning , 2011, The Journal of Neuroscience.

[10]  B. Bromm,et al.  Die Natrium-Gleichrichtung der unterschwellig erregten Membran in der quantitativen Formulierung der Ionentheorie , 1968, Pflügers Archiv.

[11]  A. Watson,et al.  Quest: A Bayesian adaptive psychometric method , 1983, Perception & psychophysics.

[12]  R. Blake,et al.  Neural bases of binocular rivalry , 2006, Trends in Cognitive Sciences.

[13]  Abhishek Datta,et al.  Clinician Accessible Tools for GUI Computational Models of Transcranial Electrical Stimulation: BONSAI and SPHERES , 2014, Brain Stimulation.

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

[15]  Claudio R. Mirasso,et al.  Effects of auditory noise on the psychophysical detection of visual signals: Cross-modal stochastic resonance , 2007, Neuroscience Letters.

[16]  Massimo Riani,et al.  Visual Perception of Stochastic Resonance , 1997 .

[17]  P. Fromherz,et al.  Extracellular stimulation of mammalian neurons through repetitive activation of Na+ channels by weak capacitive currents on a silicon chip. , 2008, Journal of neurophysiology.

[18]  Geraint Rees,et al.  Stochastic Resonance Effects Reveal the Neural Mechanisms of Transcranial Magnetic Stimulation , 2011, The Journal of Neuroscience.

[19]  F. Moss,et al.  Non-Dynamical Stochastic Resonance: Theory and Experiments with White and Arbitrarily Coloured Noise , 1995 .

[20]  Edgar Erdfelder,et al.  G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences , 2007, Behavior research methods.

[21]  C. Herrmann,et al.  Finite-Element Model Predicts Current Density Distribution for Clinical Applications of tDCS and tACS , 2012, Front. Psychiatry.

[22]  Denis G. Pelli,et al.  ECVP '07 Abstracts , 2007, Perception.

[23]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[24]  Claudio R Mirasso,et al.  Stochastic resonance in the motor system: effects of noise on the monosynaptic reflex pathway of the cat spinal cord. , 2007, Journal of neurophysiology.

[25]  Justin A. Harris,et al.  Neuroscience and Biobehavioral Reviews Modelling Non-invasive Brain Stimulation in Cognitive Neuroscience , 2022 .

[26]  E. Erdfelder,et al.  Statistical power analyses using G*Power 3.1: Tests for correlation and regression analyses , 2009, Behavior research methods.

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

[28]  Carson C. Chow,et al.  Stochastic resonance without tuning , 1995, Nature.

[29]  Bruce C. Hansen,et al.  The Effects of tDCS Across the Spatial Frequencies and Orientations that Comprise the Contrast Sensitivity Function , 2015, Front. Psychol..

[30]  W Paulus,et al.  Both the cutaneous sensation and phosphene perception are modulated in a frequency-specific manner during transcranial alternating current stimulation. , 2013, Restorative neurology and neuroscience.

[31]  Riani,et al.  Stochastic resonance in the perceptual interpretation of ambiguous figures: A neural network model. , 1994, Physical review letters.

[32]  Dennis J. L. G. Schutter,et al.  Retinal origin of phosphenes to transcranial alternating current stimulation , 2010, Clinical Neurophysiology.

[33]  Rafael Doti,et al.  Ubiquitous Crossmodal Stochastic Resonance in Humans: Auditory Noise Facilitates Tactile, Visual and Proprioceptive Sensations , 2008, PloS one.

[34]  Justin A. Harris,et al.  The Functional Effect of Transcranial Magnetic Stimulation: Signal Suppression or Neural Noise Generation? , 2008, Journal of Cognitive Neuroscience.

[35]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[36]  Sabine Kastner,et al.  Neural correlates of binocular rivalry in the human lateral geniculate nucleus , 2005, Nature Neuroscience.

[37]  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.

[38]  B. Bromm [Sodium rectification in the subthreshold excitation as computed from the voltage clamp analysis]. , 1968, Pflugers Archiv : European journal of physiology.

[39]  André Longtin,et al.  Noise in genetic and neural networks. , 2006, Chaos.

[40]  C. Miniussi,et al.  Transcranial Electrical Stimulation , 2016, The Neuroscientist.