Parallel motion signals to the medial and lateral motion areas V6 and MT+

MT+ and V6 are key motion areas of the dorsal visual stream in both macaque and human brains. In the present study, we combined electrophysiological and neuroimaging methods (including retinotopic brain mapping) to find the electrophysiological correlates of V6 and to define its temporal relationship with the activity observed in MT+. We also determined the spatio-temporal profile of the motion coherency effect on visual evoked potentials (VEPs), and localized its neural generators. We found that area V6 participates in the very early phase of the coherent motion processing and that its electroencephalographic activity is almost simultaneous with that of MT+. We also found a late second activity in V6 that we interpret as a re-entrant feedback from extrastriate visual areas (e.g. area V3A). Three main cortical sources were differently modulated by the motion coherence: while V6 and MT+ showed a preference for the coherent motion, area V3A preferred the random condition. The response timing of these cortical sources indicates that motion signals flow in parallel from the occipital pole to the medial and lateral motion areas V6 and MT+, suggesting the view of a differential functional role.

[1]  A. Ioannides,et al.  Early (N70m) Neuromagnetic Signal Topography and Striate and Extrastriate Generators Following Pattern Onset Quadrant Stimulation , 2001, NeuroImage.

[2]  Lauri Parkkonen,et al.  Motion sensitivity of human V6: A magnetoencephalography study , 2009, NeuroImage.

[3]  Arthur W. Toga,et al.  A Probabilistic Atlas of the Human Brain: Theory and Rationale for Its Development The International Consortium for Brain Mapping (ICBM) , 1995, NeuroImage.

[4]  Michael Bach,et al.  The distinction between eye and object motion is reflected by the motion-onset visual evoked potential , 2002, Experimental Brain Research.

[5]  G. Orban,et al.  The Retinotopic Organization of the Human Middle Temporal Area MT/V5 and Its Cortical Neighbors , 2010, The Journal of Neuroscience.

[6]  C. Colby,et al.  Heterogeneity of extrastriate visual areas and multiple parietal areas in the Macaque monkey , 1991, Neuropsychologia.

[7]  Mark W Greenlee,et al.  Neural correlates of visually induced self-motion illusion in depth. , 2008, Cerebral cortex.

[8]  K. Zilles,et al.  Polymodal Motion Processing in Posterior Parietal and Premotor Cortex A Human fMRI Study Strongly Implies Equivalencies between Humans and Monkeys , 2001, Neuron.

[9]  K. Thilo,et al.  Vestibular inputs to human motion-sensitive visual cortex. , 2012, Cerebral cortex.

[10]  David C. Van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex , 2005, NeuroImage.

[11]  Leslie G. Ungerleider,et al.  Pathways for motion analysis: Cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque , 1990, The Journal of comparative neurology.

[12]  D. Heeger,et al.  Two Retinotopic Visual Areas in Human Lateral Occipital Cortex , 2006, The Journal of Neuroscience.

[13]  C. Galletti,et al.  Role of the medial parieto-occipital cortex in the control of reaching and grasping movements , 2003, Experimental Brain Research.

[14]  R. Wurtz,et al.  Response of monkey MST neurons to optic flow stimuli with shifted centers of motion , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  W Lang,et al.  Cortical responses to object-motion and visually-induced self-motion perception. , 2001, Brain research. Cognitive brain research.

[16]  Sabine Kastner,et al.  Representation of Eye Movements and Stimulus Motion in Topographically Organized Areas of Human Posterior Parietal Cortex , 2008, The Journal of Neuroscience.

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

[18]  C. Galletti,et al.  The cortical connections of area V6: an occipito‐parietal network processing visual information , 2001, The European journal of neuroscience.

[19]  J W Belliveau,et al.  Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. , 1995, Science.

[20]  Giuseppe Vallar,et al.  The Cognitive and Neural Bases of Spatial Neglect , 2002 .

[21]  D. Heeger,et al.  Retinotopy and Functional Subdivision of Human Areas MT and MST , 2002, The Journal of Neuroscience.

[22]  M. Kuba,et al.  Motion-onset VEPs: Characteristics, methods, and diagnostic use , 2007, Vision Research.

[23]  Tim S Meese,et al.  Neuromagnetic evoked responses to complex motions are greatest for expansion. , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[24]  C. Galletti,et al.  Wide-Field Retinotopy Defines Human Cortical Visual Area V6 , 2006, The Journal of Neuroscience.

[25]  M. M. C. Berg-Lenssen,et al.  A spatiotemporal dipole model of the stimulus preceding negativity (spn) prior to feedback stimuli , 2005, Brain Topography.

[26]  P Fattori,et al.  Sensitivity to optic flow components in human cortical area V6 and other cortical motion areas , 2009, NeuroImage.

[27]  D. Burr,et al.  A cortical area that responds specifically to optic flow, revealed by fMRI , 2000, Nature Neuroscience.

[28]  A. Dale,et al.  Functional Analysis of V3A and Related Areas in Human Visual Cortex , 1997, The Journal of Neuroscience.

[29]  Zhaoping Li,et al.  Neural Activities in V1 Create a Bottom-Up Saliency Map , 2012, Neuron.

[30]  R. Tootell,et al.  Where is 'dorsal V4' in human visual cortex? Retinotopic, topographic and functional evidence. , 2001, Cerebral cortex.

[31]  Patrizia Fattori,et al.  Posterior parietal networks encoding visual space , 2002 .

[32]  C. Blakemore,et al.  Functional imaging of brain areas involved in the processing of coherent and incoherent wide field-of-view visual motion , 2000, Experimental Brain Research.

[33]  A. Cowey,et al.  Can spatial and temporal motion integration compensate for deficits in local motion mechanisms? , 2003, Neuropsychologia.

[34]  M. Kuba,et al.  Effect of stimulus localisation on motion-onset VEP , 2004, Vision Research.

[35]  D. Jeffreys,et al.  Source locations of pattern-specific components of human visual evoked potentials. I. Component of striate cortical origin , 2004, Experimental Brain Research.

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

[37]  O. Blanke,et al.  Multisensory Mechanisms in Temporo-Parietal Cortex Support Self-Location and First-Person Perspective , 2011, Neuron.

[38]  Antigona Martínez,et al.  Source analysis of event-related cortical activity during visuo-spatial attention. , 2003, Cerebral cortex.

[39]  G. Orban,et al.  Extracting 3D from Motion: Differences in Human and Monkey Intraparietal Cortex , 2002, Science.

[40]  Michael A. Pitts,et al.  When and Where Is Binocular Rivalry Resolved in the Visual Cortex? Design and Procedure Eeg/erp Methods Source Analyses , 2022 .

[41]  J. Hennig,et al.  The Processing of First- and Second-Order Motion in Human Visual Cortex Assessed by Functional Magnetic Resonance Imaging (fMRI) , 1998, The Journal of Neuroscience.

[42]  C. Galletti,et al.  ‘Real-motion’ cells in area V3A of macaque visual cortex , 2004, Experimental Brain Research.

[43]  Gaspare Galati,et al.  Intentional signals during saccadic and reaching delays in the human posterior parietal cortex , 2011, The European journal of neuroscience.

[44]  Koji Inui,et al.  Effects of stimulus field size and coherence of visual motion on cortical responses in humans: An MEG study , 2011, Neuroscience Letters.

[45]  Leslie G. Ungerleider,et al.  Multiple visual areas in the caudal superior temporal sulcus of the macaque , 1986, The Journal of comparative neurology.

[46]  Richard S. Frackowiak,et al.  The appreciation of wine by sommeliers: a functional magnetic resonance study of sensory integration , 2005, NeuroImage.

[47]  Velia Cardin,et al.  Sensitivity of human visual and vestibular cortical regions to egomotion-compatible visual stimulation. , 2010, Cerebral cortex.

[48]  S. Hillyard,et al.  Identification of early visual evoked potential generators by retinotopic and topographic analyses , 1994 .

[49]  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.

[50]  D. Spinelli,et al.  Spatiotemporal analysis of the cortical sources of the steady‐state visual evoked potential , 2007, Human brain mapping.

[51]  M. Sereno,et al.  A human parietal face area contains aligned head-centered visual and tactile maps , 2006, Nature Neuroscience.

[52]  Guy Marchal,et al.  Human Cortical Regions Involved in Extracting Depth from Motion , 1999, Neuron.

[53]  S. Zeki,et al.  The Organization of Connections between Areas V5 and V1 in Macaque Monkey Visual Cortex , 1989, The European journal of neuroscience.

[54]  C. Galletti,et al.  Neuronal mechanisms for detection of motion in the field of view , 2003, Neuropsychologia.

[55]  R. Turner,et al.  Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[56]  Gaspare Galati,et al.  A selective representation of the meaning of actions in the auditory mirror system , 2008, NeuroImage.

[57]  Angelika Lingnau,et al.  Selective visual responses to expansion and rotation in the human MT complex revealed by functional magnetic resonance imaging adaptation , 2008, The European journal of neuroscience.

[58]  R. Wurtz,et al.  Sensitivity of MST neurons to optic flow stimuli. I. A continuum of response selectivity to large-field stimuli. , 1991, Journal of neurophysiology.

[59]  R. Turner,et al.  Form and motion coherence activate independent, but not dorsal/ventral segregated, networks in the human brain , 2000, Current Biology.

[60]  Lotfi B Merabet,et al.  Visual Topography of Human Intraparietal Sulcus , 2007, The Journal of Neuroscience.

[61]  C. Galletti,et al.  The cortical visual area V6: brain location and visual topography , 1999, The European journal of neuroscience.

[62]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[63]  M. Sereno,et al.  Mapping of Contralateral Space in Retinotopic Coordinates by a Parietal Cortical Area in Humans , 2001, Science.

[64]  A. T. Smith,et al.  Sensitivity to optic flow in human cortical areas MT and MST , 2006, The European journal of neuroscience.

[65]  Andreas Bartels,et al.  Visual Motion Responses in the Posterior Cingulate Sulcus: A Comparison to V5/MT and MST , 2011, Cerebral cortex.

[66]  Michael Erb,et al.  Differential dependency on motion coherence in subregions of the human MT+ complex , 2008, The European journal of neuroscience.

[67]  Georgios A. Keliris,et al.  A binocular rivalry study of motion perception in the human brain , 2005, Vision Research.

[68]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[70]  H. Komatsu,et al.  Relation of cortical areas MT and MST to pursuit eye movements. III. Interaction with full-field visual stimulation. , 1988, Journal of neurophysiology.

[71]  C. Duffy MST neurons respond to optic flow and translational movement. , 1998, Journal of neurophysiology.

[72]  Sabrina Pitzalis,et al.  Spatio-Temporal Brain Mapping of Motion-Onset VEPs Combined with fMRI and Retinotopic Maps , 2012, PloS one.

[73]  O. Blanke,et al.  Motion direction tuning in human visual cortex , 2009, The European journal of neuroscience.

[74]  Guy A. Orban,et al.  Similarities and differences in motion processing between the human and macaque brain: evidence from fMRI , 2003, Neuropsychologia.

[75]  R. Wurtz,et al.  Sensitivity of MST neurons to optic flow stimuli. II. Mechanisms of response selectivity revealed by small-field stimuli. , 1991, Journal of neurophysiology.

[76]  Jürgen Kompenhans,et al.  Experimental methods for multi-diagnostics of flow fields in wind tunnels , 2007, J. Vis..

[77]  Andrew T. Smith,et al.  The Representation of Egomotion in the Human Brain , 2008, Current Biology.

[78]  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.

[79]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[80]  Thomas Haarmeier,et al.  Processing of Coherent Visual Motion in Topographically Organized Visual Areas in Human Cerebral Cortex , 2012, Brain Topography.

[81]  Christopher C. Pack,et al.  temporal neurons Speed and direction selectivity of macaque middle , 2002 .

[82]  Keiji Tanaka,et al.  Integration of direction signals of image motion in the superior temporal sulcus of the macaque monkey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[83]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[84]  C. Galletti,et al.  Human V6: The Medial Motion Area , 2009, Cerebral cortex.

[85]  G. Orban,et al.  The kinetic occipital (KO) region in man: an fMRI study. , 1997, Cerebral cortex.

[86]  Werner Lutzenberger,et al.  Neuromagnetic activity in medial parietooccipital cortex reflects the perception of visual motion during eye movements , 2004, NeuroImage.

[87]  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.

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

[89]  C. Galletti,et al.  Gaze-dependent visual neurons in area V3A of monkey prestriate cortex , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[90]  D. Heeger,et al.  Topographic maps of visual spatial attention in human parietal cortex. , 2005, Journal of neurophysiology.

[91]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[92]  J. Mattingley,et al.  The cognitive and neural bases of spatial neglect , 2004 .

[93]  S. Zeki,et al.  The third visual complex of rhesus monkey prestriate cortex. , 1978, The Journal of physiology.

[94]  Chara Vakrou,et al.  Induced Deficits in Speed Perception by Transcranial Magnetic Stimulation of Human Cortical Areas V5/MT+ and V3A , 2008, The Journal of Neuroscience.

[95]  Donatella Spinelli,et al.  Spatiotemporal brain mapping of spatial attention effects on pattern‐reversal ERPs , 2012, Human brain mapping.

[96]  Steven A. Hillyard,et al.  Identification of the neural sources of the pattern-reversal VEP , 2005, NeuroImage.

[97]  Martin I. Sereno,et al.  Spatial maps in frontal and prefrontal cortex , 2006, NeuroImage.

[98]  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.

[99]  Velia Cardin,et al.  Sensitivity of human visual cortical area V6 to stereoscopic depth gradients associated with self-motion , 2011, Journal of neurophysiology.