Evidence for fast signals and later processing in human V1/V2 and V5/MT+: A TMS study of motion perception.

Evidence from human and primate studies suggests that fast visual processing may utilize signals projecting from primary visual cortex (V1) through the dorsal stream, to area V5/MT+ or beyond and subsequently back into V1. This coincides with the arrival of parvocellular signals en route to the ventral pathway and infero-temporal cortex. Such evidence suggests that the dorsal stream region V5/MT+ is activated rapidly through the traditional hierarchical pathway and also via a less-well-established direct signal to V5/MT+ bypassing V1. To test this, 16 healthy humans underwent transcranial magnetic stimulation (TMS) of V1/V2 and V5/MT+ while performing a motion-direction detection task. A three-alternate forced-choice design (left/right motion, stationary) allowed analysis of the quality of errors made, in addition to the more usual performance measures. Transient disruption of V1/V2 and V5/MT+ significantly reduced accuracy when TMS was applied at or near motion onset. Most participants also showed disrupted performance with TMS application over V1/V2 approximately 125 ms post motion onset, and significantly reduced accuracy at 158 ms with V5/MT+ stimulation. The two periods of disruption with V1/V2 TMS are suggestive of feedforward/feedback models, although the earlier period of disruption has not been reported in previous TMS studies. Very early activation of V5/MT+, evidenced by diminished accuracy and reduced perception of motion after TMS may be indicative of a thalamic-extrastriate pathway in addition to the traditionally expected later period of processing. A profound disruption of performance prestimulus onset is more likely to reflect disruption of top-down expectancy than disruption of visual processing.

[1]  J. Driver,et al.  Preparatory states in crossmodal spatial attention: spatial specificity and possible control mechanisms , 2003, Experimental Brain Research.

[2]  A. Leventhal,et al.  Signal timing across the macaque visual system. , 1998, Journal of neurophysiology.

[3]  Anna C Nobre,et al.  FEF TMS affects visual cortical activity. , 2006, Cerebral cortex.

[4]  S. Swinnen,et al.  Directional invariance during loading-related modulations of muscle activity: evidence for motor equivalence , 2002, Experimental Brain Research.

[5]  C. Schroeder,et al.  A spatiotemporal profile of visual system activation revealed by current source density analysis in the awake macaque. , 1998, Cerebral cortex.

[6]  Marjan Jahanshahi,et al.  Transcranial magnetic stimulation studies of cognition: an emerging field , 2000, Experimental Brain Research.

[7]  S. Yamane,et al.  Neural activity in cortical area MST of alert monkey during ocular following responses. , 1994, Journal of neurophysiology.

[8]  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 .

[9]  D. Heeger,et al.  Activity in primary visual cortex predicts performance in a visual detection task , 2000, Nature Neuroscience.

[10]  A. Cowey,et al.  The role of the parietal cortex in visual attention—hemispheric asymmetries and the effects of learning: a magnetic stimulation study , 1998, Neuropsychologia.

[11]  G. Orban,et al.  Response latencies of visual cells in macaque areas V1, V2 and V5 , 1989, Brain Research.

[12]  Salil H. Patel,et al.  Characterization of N200 and P300: Selected Studies of the Event-Related Potential , 2005, International journal of medical sciences.

[13]  W. Paulus,et al.  Identification of the visual motion area (area V5) in the human brain by dipole source analysis , 2004, Experimental Brain Research.

[14]  R. Sparing,et al.  Investigation of the primary visual cortex using short-interval paired-pulse transcranial magnetic stimulation (TMS) , 2005, Neuroscience Letters.

[15]  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.

[16]  David C. Van Essen,et al.  Multiple processing streams in occipitotemporal visual cortex , 1994, Nature.

[17]  J. M. Hupé,et al.  Conduction Velocities V 1 and V 2 of the Monkey Have Similar Rapid Feedforward and Feedback Connections Between Areas , .

[18]  Bernard Renault,et al.  Latencies of event related potentials as a tool for studying motor processing organization , 1988, Biological Psychology.

[19]  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.

[20]  Stephen J. Anderson,et al.  Magnetoencephalographic evidence for non-geniculostriate visual input to human cortical area V5 , 1997, Neuropsychologia.

[21]  Ankoor S. Shah,et al.  Functional anatomy and interaction of fast and slow visual pathways in macaque monkeys. , 2007, Cerebral cortex.

[22]  John H. R. Maunsell,et al.  Visual response latencies of magnocellular and parvocellular LGN neurons in macaque monkeys , 1999, Visual Neuroscience.

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

[24]  G. V. Simpson,et al.  Flow of activation from V1 to frontal cortex in humans , 2001, Experimental Brain Research.

[25]  D. V. van Essen,et al.  Scene segmentation and attention in primate cortical areas V1 and V2. , 2002, Journal of neurophysiology.

[26]  Walter Paulus,et al.  Modulation of moving phosphene thresholds by transcranial direct current stimulation of V1 in human , 2003, Neuropsychologia.

[27]  R. Hari,et al.  Coinciding early activation of the human primary visual cortex and anteromedial cuneus , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Juha Silvanto,et al.  Double dissociation of V1 and V5/MT activity in visual awareness. , 2005, Cerebral cortex.

[29]  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.

[30]  M Hallett,et al.  A theoretical calculation of the electric field induced in the cortex during magnetic stimulation. , 1991, Electroencephalography and clinical neurophysiology.

[31]  John R. Hotson,et al.  Tracing the timing of human analysis of motion and chromatic signals from occipital to temporo-parieto-occipital cortex: A transcranial magnetic stimulation study , 1998, Vision Research.

[32]  A. Cowey,et al.  Magnetically induced phosphenes in sighted, blind and blindsighted observers , 2000, Neuroreport.

[33]  Lawrence C. Sincich,et al.  Bypassing V1: a direct geniculate input to area MT , 2004, Nature Neuroscience.

[34]  M. Aramideh,et al.  Eyelid movements: behavioral studies of blinking in humans under different stimulus conditions. , 2003, Journal of neurophysiology.

[35]  T. Kammer,et al.  Transcranial magnetic stimulation in the visual system. I. The psychophysics of visual suppression , 2004, Experimental Brain Research.

[36]  G. Mangun,et al.  The neural mechanisms of top-down attentional control , 2000, Nature Neuroscience.

[37]  P A Salin,et al.  Response selectivity of neurons in area MT of the macaque monkey during reversible inactivation of area V1. , 1992, Journal of neurophysiology.

[38]  T Landis,et al.  Electrophysiological evidence for fast visual processing through the human koniocellular pathway when stimuli move. , 2000, Cerebral cortex.

[39]  P. Kiely,et al.  Parietal function in good and poor readers , 2006, Behavioral and Brain Functions.

[40]  Mark Hallett,et al.  Interference with vision by TMS over the occipital pole: a fourth period , 2003, Neuroreport.

[41]  V. Lamme,et al.  The distinct modes of vision offered by feedforward and recurrent processing , 2000, Trends in Neurosciences.

[42]  John H. R. Maunsell,et al.  The projections from striate cortex (V1) to areas V2 and V3 in the macaque monkey: Asymmetries, areal boundaries, and patchy connections , 1986, The Journal of comparative neurology.

[43]  S. Hillyard,et al.  Cortical sources of the early components of the visual evoked potential , 2002, Human brain mapping.

[44]  C. Gross,et al.  Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  A. Milner,et al.  The role of V5/MT+ in the control of catching movements: an rTMS study , 2005, Neuropsychologia.

[46]  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.

[47]  Jared Rutter,et al.  Regulation of Clock and NPAS2 DNA Binding by the Redox State of NAD Cofactors , 2001, Science.

[48]  W. Eric L. Grimson,et al.  Experimentation with a transcranial magnetic stimulation system for functional brain mapping , 1998, Medical Image Anal..

[49]  Koji Inui,et al.  Temporal analysis of the flow from V1 to the extrastriate cortex in humans. , 2006, Journal of neurophysiology.

[50]  C. N. Guy,et al.  The parallel visual motion inputs into areas V1 and V5 of human cerebral cortex. , 1995, Brain : a journal of neurology.

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

[52]  J. Bullier,et al.  Functional interactions between areas V1 and V2 in the monkey , 1996, Journal of Physiology-Paris.

[53]  A. Klistorner,et al.  Separate magnocellular and parvocellular contributions from temporal analysis of the multifocal VEP , 1997, Vision Research.

[54]  T Mergner,et al.  Visual short-term memory of stimulus velocity in patients with unilateral posterior brain damage , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[55]  Leslie G. Ungerleider,et al.  Increased Activity in Human Visual Cortex during Directed Attention in the Absence of Visual Stimulation , 1999, Neuron.

[56]  Stewart Denslow,et al.  An Increased Precision Comparison of TMS-Induced Motor Cortex BOLD fMRI Response for Image-Guided Versus Function-Guided Coil Placement , 2005, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[57]  S. Zeki,et al.  The consequences of inactivating areas V1 and V5 on visual motion perception. , 1995, Brain : a journal of neurology.

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

[59]  D. J. Felleman,et al.  Cortical connections of areas V3 and VP of macaque monkey extrastriate visual cortex , 1997, The Journal of comparative neurology.

[60]  G Schlaug,et al.  Multimodal output mapping of human central motor representation on different spatial scales , 1998, The Journal of physiology.

[61]  J. Bullier Integrated model of visual processing , 2001, Brain Research Reviews.

[62]  Richard S. J. Frackowiak,et al.  Where in the brain does visual attention select the forest and the trees? , 1996, Nature.

[63]  Juha Silvanto,et al.  Stimulation of the human frontal eye fields modulates sensitivity of extrastriate visual cortex. , 2006, Journal of neurophysiology.

[64]  A. Cowey,et al.  Striate cortex (V1) activity gates awareness of motion , 2005, Nature Neuroscience.

[65]  Chantal Delon-Martin,et al.  Sequence of pattern onset responses in the human visual areas: an fMRI constrained VEP source analysis , 2004, NeuroImage.

[66]  L. Benevento,et al.  The organization of connections between the pulvinar and visual area MT in the macaque monkey , 1983, Brain Research.

[67]  Jacob Jolij,et al.  Figure–ground segregation requires two distinct periods of activity in V1: a transcranial magnetic stimulation study , 2005, Neuroreport.

[68]  Frank Tong,et al.  Cognitive neuroscience: Primary visual cortex and visual awareness , 2003, Nature Reviews Neuroscience.

[69]  Mark Hallett,et al.  Two periods of processing in the (circum)striate visual cortex as revealed by transcranial magnetic stimulation , 1998, Neuropsychologia.

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

[71]  Moshe Bar,et al.  Top-Down Facilitation of Visual Object Recognition , 2005 .

[72]  E H de Haan,et al.  Spatial and temporal characteristics of visual motion perception involving V5 visual cortex , 2002, Neurological research.

[73]  M Wagner,et al.  Fast visual evoked potential input into human area V5 , 1997, Neuroreport.

[74]  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.

[75]  Á. Pascual-Leone,et al.  Fast Backprojections from the Motion to the Primary Visual Area Necessary for Visual Awareness , 2001, Science.

[76]  Chantal Delon-Martin,et al.  Timing of interactions across the visual field in the human cortex , 2004, NeuroImage.

[77]  John H. R. Maunsell,et al.  Visual response latencies in striate cortex of the macaque monkey. , 1992, Journal of neurophysiology.

[78]  J. Maunsell,et al.  Functional visual streams , 1992, Current Biology.

[79]  R. Deichmann,et al.  Concurrent TMS-fMRI and Psychophysics Reveal Frontal Influences on Human Retinotopic Visual Cortex , 2006, Current Biology.

[80]  Alan Cowey,et al.  Transcranial magnetic stimulation and cognitive neuroscience , 2000, Nature Reviews Neuroscience.