Stochastic resonance enhances the rate of evidence accumulation during combined brain stimulation and perceptual decision-making

Perceptual decision-making relies on the gradual accumulation of noisy sensory evidence. It is often assumed that such decisions are degraded by adding noise to a stimulus, or to the neural systems involved in the decision making process itself. But it has been suggested that adding an optimal amount of noise can, under appropriate conditions, enhance the quality of subthreshold signals in nonlinear systems, a phenomenon known as stochastic resonance. Here we asked whether perceptual decisions made by human observers obey these stochastic resonance principles, by adding noise directly to the visual cortex using transcranial random noise stimulation (tRNS) while participants judged the direction of coherent motion in random-dot kinematograms presented at the fovea. We found that adding tRNS bilaterally to visual cortex enhanced decision-making when stimuli were just below perceptual threshold, but not when they were well below or above threshold. We modelled the data under a drift diffusion framework, and showed that bilateral tRNS selectively increased the drift rate parameter, which indexes the rate of evidence accumulation. Our study is the first to provide causal evidence that perceptual decision-making is susceptible to a stochastic resonance effect induced by tRNS, and to show that this effect arises from selective enhancement of the rate of evidence accumulation for sub-threshold sensory events.

[1]  A. Cowey,et al.  Task–specific impairments and enhancements induced by magnetic stimulation of human visual area V5 , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[2]  Nicole Wenderoth,et al.  Transcranial Random Noise Stimulation of Visual Cortex: Stochastic Resonance Enhances Central Mechanisms of Perception , 2016, The Journal of Neuroscience.

[3]  Frank Huethe,et al.  Improved Sensorimotor Performance via Stochastic Resonance , 2012, The Journal of Neuroscience.

[4]  Philip L. Smith,et al.  A comparison of sequential sampling models for two-choice reaction time. , 2004, Psychological review.

[5]  L. Pinneo On noise in the nervous system. , 1966, Psychological review.

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

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

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

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

[10]  L. Parra,et al.  Low-Intensity Electrical Stimulation Affects Network Dynamics by Modulating Population Rate and Spike Timing , 2010, The Journal of Neuroscience.

[11]  Ranier Gutierrez,et al.  Brownian Optogenetic-Noise-Photostimulation on the Brain Amplifies Somatosensory-Evoked Field Potentials , 2017, Front. Neurosci..

[12]  Duje Tadin,et al.  Temporal evolution of motion direction judgments. , 2015, Journal of vision.

[13]  Axel Thielscher,et al.  Field modeling for transcranial magnetic stimulation: A useful tool to understand the physiological effects of TMS? , 2015, 2015 37th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[14]  A. Antal,et al.  Transcranial Alternating Current and Random Noise Stimulation: Possible Mechanisms , 2016, Neural plasticity.

[15]  Derek Abbott,et al.  What Is Stochastic Resonance? Definitions, Misconceptions, Debates, and Its Relevance to Biology , 2009, PLoS Comput. Biol..

[16]  W. Newsome,et al.  Neural basis of a perceptual decision in the parietal cortex (area LIP) of the rhesus monkey. , 2001, Journal of neurophysiology.

[17]  Peter Hänggi,et al.  Stochastic resonance in biology. How noise can enhance detection of weak signals and help improve biological information processing. , 2002, Chemphyschem : a European journal of chemical physics and physical chemistry.

[18]  Thomas V. Wiecki,et al.  HDDM: Hierarchical Bayesian estimation of the Drift-Diffusion Model in Python , 2013, Front. Neuroinform..

[19]  Takeo Watanabe,et al.  Accounting for speed–accuracy tradeoff in perceptual learning , 2012, Vision Research.

[20]  Leslie G. Ungerleider,et al.  A general mechanism for perceptual decision-making in the human brain , 2004, Nature.

[21]  J. Jefferys,et al.  Effects of uniform extracellular DC electric fields on excitability in rat hippocampal slices in vitro , 2004, The Journal of physiology.

[22]  R. Sekuler,et al.  The effects of aging on motion detection and direction identification , 2007, Vision Research.

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

[24]  Gyula Kovács,et al.  Direct current stimulation over MT+/V5 modulates motion aftereffect in humans , 2004, Neuroreport.

[25]  A. Dale,et al.  The representation of the ipsilateral visual field in human cerebral cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Rafal Bogacz,et al.  Neural Correlates of Decision Thresholds in the Human Subthalamic Nucleus , 2016, Current Biology.

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

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

[29]  Roger Ratcliff,et al.  Individual Differences and Fitting Methods for the Two-Choice Diffusion Model of Decision Making. , 2015, Decision.

[30]  R. Campbell,et al.  High motion coherence thresholds in children with autism. , 2002, Journal of child psychology and psychiatry, and allied disciplines.

[31]  B. Krekelberg,et al.  Transcranial Alternating Current Stimulation Attenuates Visual Motion Adaptation , 2014, The Journal of Neuroscience.

[32]  Mark W Greenlee,et al.  Cathodal stimulation of human MT+ leads to elevated fMRI signal: a tDCS-fMRI study. , 2012, Restorative neurology and neuroscience.

[33]  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.

[34]  W. Curran,et al.  Monkey and humans exhibit similar motion-processing mechanisms , 2010 .

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

[36]  K. Hoffmann,et al.  Direct Current Stimulation over V5 Enhances Visuomotor Coordination by Improving Motion Perception in Humans , 2004, Journal of Cognitive Neuroscience.

[37]  W. Newsome,et al.  A selective impairment of motion perception following lesions of the middle temporal visual area (MT) , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  A. Cowey,et al.  Functional and anatomical profile of visual motion impairments in stroke patients correlate with fMRI in normal subjects. , 2010, Journal of neuropsychology.

[39]  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.

[40]  Richard S. J. Frackowiak,et al.  Area V5 of the human brain: evidence from a combined study using positron emission tomography and magnetic resonance imaging. , 1993, Cerebral cortex.

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

[42]  Matthew F. Tang,et al.  The broad orientation dependence of the motion streak aftereffect reveals interactions between form and motion neurons. , 2015, Journal of vision.

[43]  Francesca Grassi,et al.  Noise Enhances Action Potential Generation in Mouse Sensory Neurons via Stochastic Resonance , 2016, PloS one.

[44]  Matthew T. Kaufman,et al.  Cognitive neuroscience: Sensory noise drives bad decisions , 2013, Nature.

[45]  J. Deans,et al.  Sensitivity of coherent oscillations in rat hippocampus to AC electric fields , 2007, The Journal of physiology.

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

[47]  E. Manjarrez,et al.  Noise Improves Visual Motion Discrimination via a Stochastic Resonance-Like Phenomenon , 2016, Front. Hum. Neurosci..

[48]  J. Maunsell,et al.  Responses of neurons in the parietal and temporal visual pathways during a motion task , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[50]  L. Parra,et al.  Measurements and models of electric fields in the in vivo human brain during transcranial electric stimulation , 2017, Brain Stimulation.

[51]  Gregoire Nicolis,et al.  Stochastic resonance , 2007, Scholarpedia.

[52]  P. Boulinguez,et al.  Hemispheric asymmetry for trajectory perception. , 2003, Brain research. Cognitive brain research.

[53]  Roger Ratcliff,et al.  The Diffusion Decision Model: Theory and Data for Two-Choice Decision Tasks , 2008, Neural Computation.

[54]  A. Cowey,et al.  Motion perception and perceptual learning studied by magnetic stimulation. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[55]  Wiesenfeld,et al.  Stochastic resonance on a circle. , 1994, Physical review letters.

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

[57]  David R Badcock,et al.  Asymmetries in the Sensitivity to Motion in Depth: A Centripetal Bias , 1993, Perception.

[58]  Karl J. Friston,et al.  A direct demonstration of functional specialization in human visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[60]  A. Antal,et al.  Evaluating Aftereffects of Short-Duration Transcranial Random Noise Stimulation on Cortical Excitability , 2011, Neural plasticity.

[61]  Bingni W. Brunton,et al.  Rats and Humans Can Optimally Accumulate Evidence for Decision-Making , 2013, Science.

[62]  R. Ratcliff,et al.  A retrieval theory of priming in memory. , 1988, Psychological review.

[63]  O. Braddick,et al.  Brain Areas Sensitive to Coherent Visual Motion , 2001, Perception.

[64]  Preston P. Thakral,et al.  Disruption of MT impairs motion processing , 2011, Neuroscience Letters.

[65]  T. Nef,et al.  Cathodal HD-tDCS on the right V5 improves motion perception in humans , 2015, Front. Behav. Neurosci..

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

[67]  Ronald Mac Keith,et al.  JOURNAL OF CHILD PSYCHOLOGY AND PSYCHIATRY AND ALLIED DISCIPLINES , 1968 .

[68]  L. Tsimring Noise in biology , 2014, Reports on progress in physics. Physical Society.

[69]  Ranier Gutierrez,et al.  Optogenetic noise-photostimulation on the brain increases somatosensory spike firing responses , 2018, Neuroscience Letters.

[70]  D. Braun,et al.  Transcranial magnetic stimulation of extrastriate cortex degrades human motion direction discrimination , 1994, Vision Research.

[71]  Geraint Rees,et al.  Motion area V5/MT+ response to global motion in the absence of V1 resembles early visual cortex , 2014, Brain : a journal of neurology.

[72]  D. Bowler Autism: The International Journal of Research and Practice , 2012, Autism : the international journal of research and practice.

[73]  Andrew Gelman,et al.  General methods for monitoring convergence of iterative simulations , 1998 .

[74]  W. Newsome,et al.  Microstimulation in visual area MT: effects on direction discrimination performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[76]  Nicolas J. Kerscher,et al.  Noise‐improved signal detection in cat primary visual cortex via a well‐balanced stochastic resonance‐like procedure , 2007, The European journal of neuroscience.

[77]  R. Andersen,et al.  Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[78]  G. Davis,et al.  Low endogenous neural noise in autism , 2015, Autism : the international journal of research and practice.

[79]  N. Wenderoth,et al.  A technical guide to tDCS, and related non-invasive brain stimulation tools , 2016, Clinical Neurophysiology.

[80]  S. Anand,et al.  The selectivity and timing of motion processing in human temporo–parieto–occipital and occipital cortex: a transcranial magnetic stimulation study , 1998, Neuropsychologia.

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

[82]  V. Hömberg,et al.  Cerebral visual motion blindness: transitory akinetopsia induced by transcranial magnetic stimulation of human area V5 , 1992, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[83]  Kenneth D. Harris,et al.  High-Yield Methods for Accurate Two-Alternative Visual Psychophysics in Head-Fixed Mice , 2016, bioRxiv.

[84]  D. Burr,et al.  Spatiotopic selectivity of BOLD responses to visual motion in human area MT , 2007, Nature Neuroscience.