Dynamic causal modelling of precision and synaptic gain in visual perception — an EEG study

Estimating the precision or uncertainty associated with sensory signals is an important part of perception. Based on a previous computational model, we tested the hypothesis that increasing visual contrast increased the precision encoded in early visual areas by the gain or excitability of superficial pyramidal cells. This hypothesis was investigated using electroencephalography and dynamic causal modelling (DCM); a biologically constrained modelling of the cortical processes underlying EEG activity. Source localisation identified the electromagnetic sources of visually evoked responses and DCM was used to characterise the coupling among these sources. Bayesian model selection was used to select the most likely connectivity pattern and contrast-dependent changes in connectivity. As predicted, the model with the highest evidence entailed increased superficial pyramidal cell gain in higher-contrast trials. As predicted theoretically, contrast-dependent increases were reduced at higher levels of the hierarchy. These results demonstrate that increased signal-to-noise ratio in sensory signals produce (or are represented by) increased superficial pyramidal cell gain, and that synaptic parameters encoding statistical properties like sensory precision can be quantified using EEG and dynamic causal modelling.

[1]  Hakwan Lau,et al.  Prior Expectation Modulates the Interaction between Sensory and Prefrontal Regions in the Human Brain , 2011, The Journal of Neuroscience.

[2]  Gary F. Egan,et al.  Real and Imaginary Rotary Motion Processing: Functional Parcellation of the Human Parietal Lobe Revealed by fMRI , 2005, Journal of Cognitive Neuroscience.

[3]  Jim M. Monti,et al.  Neural repetition suppression reflects fulfilled perceptual expectations , 2008, Nature Neuroscience.

[4]  D J Field,et al.  Local Contrast in Natural Images: Normalisation and Coding Efficiency , 2000, Perception.

[5]  Karl J. Friston,et al.  Free-Energy and Illusions: The Cornsweet Effect , 2011, Front. Psychology.

[6]  D. G. Albrecht,et al.  Spatial contrast adaptation characteristics of neurones recorded in the cat's visual cortex. , 1984, The Journal of physiology.

[7]  Christopher Summerfield,et al.  Dissociable prior influences of signal probability and relevance on visual contrast sensitivity , 2011 .

[8]  E. Boring Helmholtz's treatise on physiological optics. , 1926 .

[9]  Karl J. Friston,et al.  Predictive coding under the free-energy principle , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[10]  Karl J. Friston,et al.  Variational free energy and the Laplace approximation , 2007, NeuroImage.

[11]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[12]  Karl J. Friston,et al.  Electromagnetic source reconstruction for group studies , 2008, NeuroImage.

[13]  A. Anderson,et al.  An fMRI study of stroop word-color interference: evidence for cingulate subregions subserving multiple distributed attentional systems , 1999, Biological Psychiatry.

[14]  C. Frith,et al.  From drugs to deprivation: a Bayesian framework for understanding models of psychosis , 2009, Psychopharmacology.

[15]  Karl J. Friston,et al.  Dynamic Causal Modeling of the Response to Frequency Deviants , 2009, Journal of neurophysiology.

[16]  Kuzma Strelnikov,et al.  Can mismatch negativity be linked to synaptic processes? A glutamatergic approach to deviance detection , 2007, Brain and Cognition.

[17]  Anthony J. Rissling,et al.  Automatic sensory information processing abnormalities across the illness course of schizophrenia , 2011, Psychological Medicine.

[18]  A. Borst Seeing smells: imaging olfactory learning in bees , 1999, Nature Neuroscience.

[19]  Karl J. Friston,et al.  Dynamic causal modeling for EEG and MEG , 2009, Human brain mapping.

[20]  Janneke F. M. Jehee,et al.  Attention Reverses the Effect of Prediction in Silencing Sensory Signals , 2011, Cerebral cortex.

[21]  Karl J. Friston,et al.  The functional anatomy of the MMN: A DCM study of the roving paradigm , 2008, NeuroImage.

[22]  S. Nelson,et al.  Short-Term Depression at Thalamocortical Synapses Contributes to Rapid Adaptation of Cortical Sensory Responses In Vivo , 2002, Neuron.

[23]  A. T. Smith,et al.  Pharmacological separation of mechanisms contributing to human contrast sensitivity , 1993, Visual Neuroscience.

[24]  W. PEDDIE,et al.  Helmholtz's Treatise on Physiological Optics , 1926, Nature.

[25]  M. Hawken,et al.  Gain Modulation by Nicotine in Macaque V1 , 2007, Neuron.

[26]  D. Heeger,et al.  The Normalization Model of Attention , 2009, Neuron.

[27]  Volkmar Glauche,et al.  Functional properties and interaction of the anterior and posterior intraparietal areas in humans , 2003, The European journal of neuroscience.

[28]  John H. R. Maunsell,et al.  The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  I. Ohzawa,et al.  Contrast gain control in the cat visual cortex , 1982, Nature.

[30]  G. Pourtois,et al.  Top-down effects on early visual processing in humans: A predictive coding framework , 2011, Neuroscience & Biobehavioral Reviews.

[31]  B. Skottun,et al.  Contrast sensitivity and magnocellular functioning in schizophrenia , 2007, Vision Research.

[32]  U. Polat,et al.  Neurophysiological Evidence for Contrast Dependent Long-range Facilitation and Suppression in the Human Visual Cortex , 1996, Vision Research.

[33]  T. Wiesel,et al.  Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex , 1979, Nature.

[34]  H. Lau,et al.  Attention induces conservative subjective biases in visual perception , 2011, Nature Neuroscience.

[35]  M. Ernst,et al.  Humans integrate visual and haptic information in a statistically optimal fashion , 2002, Nature.

[36]  S. Grossberg,et al.  Spikes, synchrony, and attentive learning by laminar thalamocortical circuits , 2006, Brain Research.

[37]  A. B. Bonds,et al.  Anticholinesterase agents affect contrast gain of the cat cortical visual evoked potential , 1986, Neuroscience Letters.

[38]  Dale Purves,et al.  Perceiving the intensity of light. , 2004, Psychological review.

[39]  Karl J. Friston,et al.  Attention, Uncertainty, and Free-Energy , 2010, Front. Hum. Neurosci..

[40]  Michael W. Spratling Reconciling Predictive Coding and Biased Competition Models of Cortical Function , 2008, Frontiers Comput. Neurosci..

[41]  D Purves,et al.  An Empirical Explanation of the Cornsweet Effect , 1999, The Journal of Neuroscience.

[42]  M. Carandini,et al.  Summation and division by neurons in primate visual cortex. , 1994, Science.

[43]  Karl J. Friston,et al.  Dynamic causal modeling for EEG and MEG , 2009, Human brain mapping.

[44]  John J. Foxe,et al.  Sensory deficits and distributed hierarchical dysfunction in schizophrenia. , 2010, The American journal of psychiatry.

[45]  B. Rockstroh,et al.  Reduced mismatch negativity and increased variability of brain activity in schizophrenia , 2011, Clinical Neurophysiology.

[46]  W. Slaghuis,et al.  Contrast sensitivity for stationary and drifting spatial frequency gratings in positive- and negative-symptom schizophrenia. , 1998, Journal of abnormal psychology.

[47]  S. Grossberg,et al.  A neural model of surface perception: lightness, anchoring, and filling-in. , 2006, Spatial vision.

[48]  M. Carandini,et al.  A Synaptic Explanation of Suppression in Visual Cortex , 2002, The Journal of Neuroscience.

[49]  H L Evans,et al.  Scopolamine effects on visual discrimination: modifications related to stimulus control. , 1975, The Journal of pharmacology and experimental therapeutics.