Improved Motion Perception and Impaired Spatial Suppression following Disruption of Cortical Area MT/V5

As stimulus size increases, motion direction of high-contrast patterns becomes increasingly harder to perceive. This counterintuitive behavioral result, termed “spatial suppression,” is hypothesized to reflect center–surround antagonism—a receptive field property ubiquitous in sensory systems. Prior research proposed that spatial suppression of motion signals is a direct correlate of center–surround antagonism within cortical area MT. Here, we investigated whether human MT/V5 is indeed causally involved in spatial suppression of motion signals. The key assumption is that a disruption of neural mechanisms that play a critical role in spatial suppression could allow these normally suppressed motion signals to reach perceptual awareness. Thus, our hypothesis was that a disruption of MT/V5 should weaken spatial suppression and, consequently, improve motion perception of large, moving patterns. To disrupt MT/V5, we used offline 1 Hz transcranial magnetic stimulation (TMS)—a method that temporarily attenuates normal functioning of the targeted cortex. Early visual areas were also targeted as a control site. The results supported our hypotheses and showed that disruption of MT/V5 improved motion discrimination of large, moving stimuli, presumably by weakening surround suppression strength. This effect was specific to MT/V5 stimulation and contralaterally presented stimuli. Evidently, the critical neural constraints limiting motion perception of large, high-contrast stimuli involve MT/V5. Additionally, our findings mimic spatial suppression deficits that are observed in several patient populations and implicate impaired MT/V5 processes as likely neural correlates for the reported perceptual abnormalities in the elderly, patients with schizophrenia and those with a history of depression.

[1]  J. R. Hughes,et al.  Sensory integration in children. Evoked potentials and intersensory functions in pediatrics and psychology: T. Shipley (Thomas, Springfield, Ill., 1980, 154 p., U.S. $ 15.50) , 1981 .

[2]  K. Nakayama,et al.  The characteristics of residual motion perception in the hemifield contralateral to lateral occipital lesions in humans. , 1993, Brain : a journal of neurology.

[3]  G. Orban,et al.  Shape and Spatial Distribution of Receptive Fields and Antagonistic Motion Surrounds in the Middle Temporal Area (V5) of the Macaque , 1995, The European journal of neuroscience.

[4]  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.

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

[6]  U. Ziemann,et al.  Transient visual field defects induced by transcranial magnetic stimulation over human occipital pole , 1998, Experimental Brain Research.

[7]  G. Orban,et al.  Motion-responsive regions of the human brain , 1999, Experimental Brain Research.

[8]  T. Pasternak,et al.  Transient and permanent deficits in motion perception after lesions of cortical areas MT and MST in the macaque monkey. , 1999, Cerebral cortex.

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

[10]  L. Cohen,et al.  Reduction of human visual cortex excitability using 1-Hz transcranial magnetic stimulation , 2000, Neurology.

[11]  J L Gallant,et al.  Sparse coding and decorrelation in primary visual cortex during natural vision. , 2000, Science.

[12]  R. Born,et al.  Segregation of Object and Background Motion in Visual Area MT Effects of Microstimulation on Eye Movements , 2000, Neuron.

[13]  R. Born Center-surround interactions in the middle temporal visual area of the owl monkey. , 2000, Journal of neurophysiology.

[14]  Ron Kikinis,et al.  Transcranial magnetic stimulation coregistered with MRI: a comparison of a guided versus blind stimulation technique and its effect on evoked compound muscle action potentials , 2001, Clinical Neurophysiology.

[15]  Eero P. Simoncelli,et al.  Natural signal statistics and sensory gain control , 2001, Nature Neuroscience.

[16]  Á. Pascual-Leone,et al.  Enhanced visual spatial attention ipsilateral to rTMS-induced 'virtual lesions' of human parietal cortex , 2001, Nature Neuroscience.

[17]  A. Sillito,et al.  Surround suppression in primate V1. , 2001, Journal of neurophysiology.

[18]  M. Martinez,et al.  Mapping of the human visual cortex using image-guided transcranial magnetic stimulation. , 2002, Brain research. Brain research protocols.

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

[20]  Walter Paulus,et al.  Transcranial magnetic and direct current stimulation of the visual cortex. , 2003, Supplements to Clinical neurophysiology.

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

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

[23]  R. Desimone,et al.  Local precision of visuotopic organization in the middle temporal area (MT) of the macaque , 2004, Experimental Brain Research.

[24]  Gregor Thut,et al.  Feeling by Sight or Seeing by Touch? , 2004, Neuron.

[25]  Duje Tadin,et al.  Linking Psychophysics and Physiology of Center-Surround Interactions in Visual Motion Processing , 2005 .

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

[27]  Christopher C. Pack,et al.  Contrast dependence of suppressive influences in cortical area MT of alert macaque. , 2005, Journal of neurophysiology.

[28]  R. Blake,et al.  Motion Perception Getting Better with Age? , 2005, Neuron.

[29]  Duje Tadin,et al.  Optimal size for perceiving motion decreases with contrast , 2005, Vision Research.

[30]  D. Bradley,et al.  Structure and function of visual area MT. , 2005, Annual review of neuroscience.

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

[32]  Rainer Goebel,et al.  The temporal characteristics of motion processing in hMT/V5+: Combining fMRI and neuronavigated TMS , 2006, NeuroImage.

[33]  Brian N. Pasley,et al.  Transcranial Magnetic Stimulation Elicits Coupled Neural and Hemodynamic Consequences , 2007, Science.

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

[35]  Juha Silvanto,et al.  Baseline cortical excitability determines whether TMS disrupts or facilitates behavior. , 2008, Journal of neurophysiology.

[36]  Christopher M. Masciocchi,et al.  Everyone knows what is interesting: salient locations which should be fixated. , 2009, Journal of vision.

[37]  George A. Alvarez,et al.  The Role of the Parietal Lobe in Visual Extinction Studied with Transcranial Magnetic Stimulation , 2009, Journal of Cognitive Neuroscience.

[38]  Ari Koskelainen,et al.  Origin of the fast negative ERG component from isolated aspartate-treated mouse retina. , 2009, Journal of vision.

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

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

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

[42]  S. Rossi,et al.  Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research , 2009, Clinical Neurophysiology.

[43]  Jeffrey B. Nyquist,et al.  Spatial and temporal limits of motion perception across variations in speed, eccentricity, and low vision. , 2009, Journal of vision.

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

[45]  Kazumichi Matsumiya,et al.  Motion mechanisms with different spatiotemporal characteristics identified by an MAE technique with superimposed gratings. , 2009, Journal of vision.

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

[47]  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.