Two Common Psychophysical Measures of Surround Suppression Reflect Independent Neuronal Mechanisms Task 1: Motion-direction Discrimination Task 2: Contrast Detection Suppression Index (si)

Psychophysical surround suppression is believed to reflect inhibitory neuronal mechanisms in visual cortex. In recent years, two psychophysical measures of surround suppression have been much studied: (i) duration thresholds on a motion-discrimination task (which are worse for larger than for smaller stimuli) and (ii) contrast thresholds on a contrast-detection task (which are worse when grating stimuli are surrounded by a stimulus of the same orientation than when they are presented in isolation or surrounded by a stimulus of orthogonal orientation). Changes in both metrics have been linked to several different human conditions, including aging, differences in intelligence, and clinical disorders such as schizophrenia, depression, and autism. However, the exact nature of the neuronal correlate underlying these phenomena remains unclear. Here, we use an individual-differences approach to test the hypothesis that both measures reflect the same property of the visual system, e.g., the strength of GABA-ergic inhibition across visual cortex. Under this hypothesis we would expect the two measures to be significantly positively correlated across individuals. In fact, they are not significantly correlated. In addition, we replicate the previously reported correlation between age and motion-discrimination surround suppression, but find no correlation between age and contrast-detection surround suppression. We conclude that the two forms of psychophysical surround suppression arise independently from different cortical mechanisms.

[1]  P. Lennie,et al.  Early and Late Mechanisms of Surround Suppression in Striate Cortex of Macaque , 2005, The Journal of Neuroscience.

[2]  Randolph Blake,et al.  Visual Context Processing in Schizophrenia , 2013, Clinical psychological science : a journal of the Association for Psychological Science.

[3]  I. Serrano-Pedraza,et al.  Reduced visual surround suppression in schizophrenia shown by measuring contrast detection thresholds , 2014, Front. Psychol..

[4]  A. Leventhal,et al.  GABA and Its Agonists Improved Visual Cortical Function in Senescent Monkeys , 2003, Science.

[5]  Xin Huang,et al.  Stimulus Dependency and Mechanisms of Surround Modulation in Cortical Area MT , 2008, The Journal of Neuroscience.

[6]  A. Angelucci,et al.  Contribution of feedforward, lateral and feedback connections to the classical receptive field center and extra-classical receptive field surround of primate V1 neurons. , 2006, Progress in brain research.

[7]  H. Bouma,et al.  Eccentric vision: Adverse interactions between line segments , 1976, Vision Research.

[8]  Allison M. McKendrick,et al.  Aging alters surround modulation of perceived contrast. , 2009, Journal of vision.

[9]  J. M. Hupé,et al.  Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons , 1998, Nature.

[10]  H. Jones,et al.  Surround suppression in primate V1. , 2001, Journal of neurophysiology.

[11]  Allison M. McKendrick,et al.  Migraine Increases Centre-Surround Suppression for Drifting Visual Stimuli , 2011, PloS one.

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

[13]  I. Serrano-Pedraza,et al.  Spatial frequency bandwidth of surround suppression tuning curves. , 2012, Journal of vision.

[14]  O. Creutzfeldt,et al.  Significance of intracortical inhibition in the visual cortex. , 1972, Nature: New biology.

[15]  R. Shapley,et al.  Contrast's effect on spatial summation by macaque V1 neurons , 1999, Nature Neuroscience.

[16]  R. Snowden,et al.  The effects of surround contrast on contrast thresholds, perceived contrast and contrast discrimination , 1998, Vision Research.

[17]  Yoshimichi Ejima,et al.  Apparent contrast of a sinusoidal grating in the simultaneous presence of peripheral gratings , 1985, Vision Research.

[18]  David G. Jones,et al.  Frontiers in Cellular Neuroscience Cellular Neuroscience , 2022 .

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

[20]  W. Hays.  Applied Regression Analysis. 2nd ed. , 1981 .

[21]  Ignacio Serrano-Pedraza,et al.  Moderate acute alcohol intoxication has minimal effect on surround suppression measured with a motion direction discrimination task. , 2015, Journal of vision.

[22]  Christopher Patrick Taylor,et al.  Aging Reduces Center-Surround Antagonism in Visual Motion Processing , 2005, Neuron.

[23]  C. Owsley.  Aging and vision , 2011, Vision Research.

[24]  Yuanye Ma,et al.  Functional degradation of the primary visual cortex during early senescence in rhesus monkeys. , 2013, Cerebral cortex.

[25]  L. Maffei,et al.  The unresponsive regions of visual cortical receptive fields , 1976, Vision Research.

[26]  Henry J. Alitto,et al.  Function of inhibition in visual cortical processing , 2010, Current Opinion in Neurobiology.

[27]  Uri Polat,et al.  Collinear facilitation and suppression at the periphery , 2011, Vision Research.

[28]  T. Albright,et al.  Adaptive Surround Modulation in Cortical Area MT , 2007, Neuron.

[29]  Lihua He,et al.  Functional degradation of visual cortical cells in old cats , 2006, Neurobiology of Aging.

[30]  Davis M. Glasser,et al.  Low-level mechanisms do not explain paradoxical motion percepts. , 2010, Journal of vision.

[31]  L. Schwabe,et al.  Response facilitation from the "suppressive" receptive field surround of macaque V1 neurons. , 2007, Journal of neurophysiology.

[32]  M. Carandini,et al.  Temporal properties of surround suppression in cat primary visual cortex , 2007, Visual Neuroscience.

[33]  Allison B Sekuler,et al.  Spatial characteristics of center-surround antagonism in younger and older adults. , 2009, Journal of vision.

[34]  C. Distler,et al.  Attention and normalization circuits in macaque V1 , 2015, The European journal of neuroscience.

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

[36]  Allison M McKendrick,et al.  Age related changes to perceptual surround suppression of moving stimuli. , 2012, Seeing and perceiving.

[37]  Matteo Carandini,et al.  Two Distinct Mechanisms of Suppression in Human Vision , 2005, The Journal of Neuroscience.

[38]  S. Murray,et al.  Orientation-specific surround suppression in the primary visual cortex varies as a function of autistic tendency , 2015, Front. Hum. Neurosci..

[39]  Yuanye Ma,et al.  Aging affects the neural representation of speed in Macaque area MT. , 2009, Cerebral cortex.

[40]  Cameron S Carter,et al.  Diminished orientation-specific surround suppression of visual processing in schizophrenia. , 2009, Schizophrenia bulletin.

[41]  I. Ohzawa,et al.  Organization of suppression in receptive fields of neurons in cat visual cortex. , 1992, Journal of neurophysiology.

[42]  Mark W. Cannon,et al.  Spatial interactions in apparent contrast: Inhibitory effects among grating patterns of different spatial frequencies, spatial positions and orientations , 1991, Vision Research.

[43]  D. Wilkin,et al.  Neuron , 2001, Brain Research.

[44]  David Whitney,et al.  The psychophysics of visual motion and global form processing in autism. , 2010, Brain : a journal of neurology.

[45]  A. Angelucci,et al.  Multiple components of surround modulation in primary visual cortex: Multiple neural circuits with multiple functions? , 2014, Vision Research.

[46]  Jie Zhang,et al.  Aging affects the direction selectivity of MT cells in rhesus monkeys , 2010, Neurobiology of Aging.

[47]  Randolph Blake,et al.  Weakened Center-Surround Interactions in Visual Motion Processing in Schizophrenia , 2006, The Journal of Neuroscience.

[48]  J. B. Levitt,et al.  Comparison of Spatial Summation Properties of Neurons in Macaque V1 and V2 , 2009, Journal of neurophysiology.

[49]  David Whitaker,et al.  Neural contribution to spatiotemporal contrast sensitivity decline in healthy ageing eyes , 1990, Vision Research.

[50]  James M. G. Tsui,et al.  Brief motion stimuli preferentially activate surround-suppressed neurons in macaque visual area MT , 2008, Current Biology.

[51]  Xiangrui Li,et al.  Decreased proportion of GABA neurons accompanies age-related degradation of neuronal function in cat striate cortex , 2008, Brain Research Bulletin.

[52]  Marvin M Chun,et al.  Enhanced Visual Motion Perception in Major Depressive Disorder , 2009, The Journal of Neuroscience.

[53]  Randolph Blake,et al.  Perceptual consequences of centre–surround antagonism in visual motion processing , 2003, Nature.

[54]  Randolph Blake,et al.  Contextual modulations of center-surround interactions in motion revealed with the motion aftereffect. , 2008, Journal of vision.

[55]  Allison B. Sekuler,et al.  Spatial characteristics of motion-sensitive mechanisms change with age and stimulus spatial frequency , 2012, Vision Research.

[56]  L. Kochan,et al.  GABA and Schizophrenia: A Review of Basic Science and Clinical Studies , 2003, Journal of clinical psychopharmacology.

[57]  J Allman,et al.  Direction- and Velocity-Specific Responses from beyond the Classical Receptive Field in the Middle Temporal Visual Area (MT) , 1985, Perception.

[58]  D. Ongur,et al.  Altered Center-Surround Motion Inhibition in Schizophrenia , 2008, Biological Psychiatry.

[59]  M. A. Smith,et al.  Surround Suppression in the Early Visual System , 2006, The Journal of Neuroscience.

[60]  U. Polat,et al.  Lateral interactions between spatial channels: Suppression and facilitation revealed by lateral masking experiments , 1993, Vision Research.

[61]  Duje Tadin,et al.  A Substantial and Unexpected Enhancement of Motion Perception in Autism , 2013, The Journal of Neuroscience.

[62]  G F Mason,et al.  Reduced cortical gamma-aminobutyric acid levels in depressed patients determined by proton magnetic resonance spectroscopy. , 1999, Archives of general psychiatry.

[63]  Duje Tadin,et al.  A Strong Interactive Link between Sensory Discriminations and Intelligence , 2013, Current Biology.

[64]  S. Shergill,et al.  Reduced Crowding and Poor Contour Detection in Schizophrenia Are Consistent with Weak Surround Inhibition , 2012, PloS one.

[65]  C. Blakemore,et al.  Characteristics of surround inhibition in cat area 17 , 1997, Experimental Brain Research.

[66]  R. Hess,et al.  Low-level mechanisms may contribute to paradoxical motion percepts. , 2009, Journal of vision.

[67]  Fahmeed Hyder,et al.  Reduced Cortical γ-Aminobutyric Acid Levels in Depressed Patients Determined by Proton Magnetic Resonance Spectroscopy , 1999 .

[68]  A. McKendrick,et al.  Increased Surround Modulation of Perceived Contrast in the Elderly , 2011, Optometry and vision science : official publication of the American Academy of Optometry.

[69]  Dennis M. Levi,et al.  Surround modulation in human vision unmasked by masking experiments , 2000, Nature Neuroscience.

[70]  N. Draper,et al.  Applied Regression Analysis , 1966 .

[71]  A. McKendrick,et al.  Contrast and stimulus duration dependence of perceptual surround suppression in older adults , 2015, Vision Research.

[72]  Jonathan W Peirce,et al.  Two expressions of “surround suppression” in V1 that arise independent of cortical mechanisms of suppression , 2007, Visual Neuroscience.

[73]  D. Heeger,et al.  Center-surround interactions in foveal and peripheral vision , 2000, Vision Research.

[74]  D. Burr,et al.  Spatial summation properties of directionally selective mechanisms in human vision. , 1991, Journal of the Optical Society of America. A, Optics and image science.

[75]  S. Shergill,et al.  Visual Surround Suppression in Schizophrenia , 2013, Front. Psychol..

[76]  Davis M. Glasser,et al.  Visual context processing in bipolar disorder: a comparison with schizophrenia , 2013, Front. Psychol..

[77]  Jude F. Mitchell,et al.  Spatial Attention Modulates Center-Surround Interactions in Macaque Visual Area V4 , 2009, Neuron.

[78]  A. Thiele,et al.  Comparison of spatial integration and surround suppression characteristics in spiking activity and the local field potential in macaque V1 , 2008, The European journal of neuroscience.

[79]  Christopher C. Pack,et al.  The role of V1 surround suppression in MT motion integration. , 2010, Journal of neurophysiology.

[80]  Jong H. Yoon,et al.  GABA Concentration Is Reduced in Visual Cortex in Schizophrenia and Correlates with Orientation-Specific Surround Suppression , 2010, The Journal of Neuroscience.

[81]  I. Ohzawa,et al.  Binocular cross-orientation suppression in the cat's striate cortex. , 1998, Journal of neurophysiology.

[82]  Christopher C. Pack,et al.  Contrast sensitivity of MT receptive field centers and surrounds. , 2011, Journal of neurophysiology.

[83]  Wilsaan M. Joiner,et al.  Suppressive Surrounds of Receptive Fields In Monkey Frontal Eye Field , 2012, The Journal of Neuroscience.

[84]  Duje Tadin,et al.  Mechanisms of motion-based object segregation , 2014 .

[85]  C. Blakemore,et al.  Lateral inhibition between orientation detectors in the cat's visual cortex , 2004, Experimental Brain Research.

[86]  David J Heeger,et al.  Response Suppression in V1 Agrees with Psychophysics of Surround Masking , 2003, The Journal of Neuroscience.

[87]  J. Movshon,et al.  Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons. , 2002, Journal of neurophysiology.

[88]  B Suresh Krishna,et al.  Surround Suppression Sharpens the Priority Map in the Lateral Intraparietal Area , 2022 .

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

[90]  Allison M McKendrick,et al.  Center-surround visual motion processing in migraine. , 2010, Investigative ophthalmology & visual science.

[91]  R. Rosenfeld.  Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.