Natural vision reveals regional specialization to local motion and to contrast-invariant, global flow in the human brain.

Visual changes in feature movies, like in real-live, can be partitioned into global flow due to self/camera motion, local/differential flow due to object motion, and residuals, for example, due to illumination changes. We correlated these measures with brain responses of human volunteers viewing movies in an fMRI scanner. Early visual areas responded only to residual changes, thus lacking responses to equally large motion-induced changes, consistent with predictive coding. Motion activated V5+ (MT+), V3A, medial posterior parietal cortex (mPPC) and, weakly, lateral occipital cortex (LOC). V5+ responded to local/differential motion and depended on visual contrast, whereas mPPC responded to global flow spanning the whole visual field and was contrast independent. mPPC thus codes for flow compatible with unbiased heading estimation in natural scenes and for the comparison of visual flow with nonretinal, multimodal motion cues in it or downstream. mPPC was functionally connected to anterior portions of V5+, whereas laterally neighboring putative homologue of lateral intraparietal area (LIP) connected with frontal eye fields. Our results demonstrate a progression of selectivity from local and contrast-dependent motion processing in V5+ toward global and contrast-independent motion processing in mPPC. The function, connectivity, and anatomical neighborhood of mPPC imply several parallels to monkey ventral intraparietal area (VIP).

[1]  J. Gibson The visual perception of objective motion and subjective movement. , 1994, Psychological review.

[2]  J. Pokorny Foundations of Cyclopean Perception , 1972 .

[3]  O. Braddick A short-range process in apparent motion. , 1974, Vision research.

[4]  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.

[5]  D. J. Felleman,et al.  Receptive-field properties of neurons in middle temporal visual area (MT) of owl monkeys. , 1984, Journal of neurophysiology.

[6]  E. Adelson,et al.  The analysis of moving visual patterns , 1985 .

[7]  Charles G. Gross,et al.  Pattern recognition mechanisms , 1985 .

[8]  R. Andersen,et al.  Callosal and prefrontal associational projecting cell populations in area 7A of the macaque monkey: A study using retrogradely transported fluorescent dyes , 1985, The Journal of comparative neurology.

[9]  K. Tanaka,et al.  Analysis of local and wide-field movements in the superior temporal visual areas of the macaque monkey , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[10]  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.

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

[12]  H. Komatsu,et al.  Relation of cortical areas MT and MST to pursuit eye movements. II. Differentiation of retinal from extraretinal inputs. , 1988, Journal of neurophysiology.

[13]  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.

[14]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[15]  T. Poggio,et al.  A parallel algorithm for real-time computation of optical flow , 1989, Nature.

[16]  John H. R. Maunsell,et al.  Coding of image contrast in central visual pathways of the macaque monkey , 1990, Vision Research.

[17]  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.

[18]  Thomas D. Albright,et al.  Neural correlates of perceptual motion coherence , 1992, Nature.

[19]  J R Duhamel,et al.  The updating of the representation of visual space in parietal cortex by intended eye movements. , 1992, Science.

[20]  M. Goldberg,et al.  Ventral intraparietal area of the macaque: anatomic location and visual response properties. , 1993, Journal of neurophysiology.

[21]  M. Graziano,et al.  Tuning of MST neurons to spiral motions , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  T D Albright,et al.  What happens if it changes color when it moves?: the nature of chromatic input to macaque visual area MT , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[23]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[24]  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.

[25]  R. Andersen,et al.  Mechanisms of Heading Perception in Primate Visual Cortex , 1996, Science.

[26]  R. S. J. Frackowiak,et al.  Activity in human areas V1/V2, V3 and V5 during the perception of coherent and incoherent motion , 1996, NeuroImage.

[27]  J Duysens,et al.  Neurons in the ventral intraparietal area of awake macaque monkey closely resemble neurons in the dorsal part of the medial superior temporal area in their responses to optic flow patterns. , 1996, Journal of neurophysiology.

[28]  Peter Thier,et al.  False perception of motion in a patient who cannot compensate for eye movements , 1997, Nature.

[29]  Y. Diao,et al.  Sensitivity of LS neurons to optic flow stimuli , 1997 .

[30]  R. M. Siegel,et al.  Analysis of optic flow in the monkey parietal area 7a. , 1997, Cerebral cortex.

[31]  P. Cavanagh,et al.  Cortical fMRI activation produced by attentive tracking of moving targets. , 1998, Journal of neurophysiology.

[32]  Karl J. Friston,et al.  Characterizing Stimulus–Response Functions Using Nonlinear Regressors in Parametric fMRI Experiments , 1998, NeuroImage.

[33]  W. Heide,et al.  Combined deficits of saccades and visuo-spatial orientation after cortical lesions , 1998, Experimental Brain Research.

[34]  M. Goldberg,et al.  The representation of visual salience in monkey parietal cortex , 1998, Nature.

[35]  M. Corbetta,et al.  A Common Network of Functional Areas for Attention and Eye Movements , 1998, Neuron.

[36]  Peter Thier,et al.  An Electrophysiological Correlate of Visual Motion Awareness in Man , 1998, Journal of Cognitive Neuroscience.

[37]  S. Edelman,et al.  Cue-Invariant Activation in Object-Related Areas of the Human Occipital Lobe , 1998, Neuron.

[38]  M. Goldberg,et al.  Ventral intraparietal area of the macaque: congruent visual and somatic response properties. , 1998, Journal of neurophysiology.

[39]  K. Scheffler,et al.  Effect of eye movements on the magnitude of functional magnetic resonance imaging responses in extrastriate cortex during visual motion perception , 1998, Experimental Brain Research.

[40]  W K Page,et al.  MST neuronal responses to heading direction during pursuit eye movements. , 1999, Journal of neurophysiology.

[41]  D. Burr,et al.  Saccadic suppression precedes visual motion analysis , 1999, Current Biology.

[42]  R A Andersen,et al.  Influence of gaze rotation on the visual response of primate MSTd neurons. , 1999, Journal of neurophysiology.

[43]  Rajesh P. N. Rao,et al.  Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. , 1999 .

[44]  J. Haxby,et al.  Functional anatomy of pursuit eye movements in humans as revealed by fMRI. , 1999, Journal of neurophysiology.

[45]  S. Zeki,et al.  The neurology of saccades and covert shifts in spatial attention: an event-related fMRI study. , 2000, Brain : a journal of neurology.

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

[47]  R. M. Siegel,et al.  Speed selectivity for optic flow in area 7a of the behaving macaque. , 2000, Cerebral cortex.

[48]  S. Zeki,et al.  The architecture of the colour centre in the human visual brain: new results and a review * , 2000, The European journal of neuroscience.

[49]  G. A. Orban,et al.  Human Brain Regions Involved in Heading Estimation , 2001, The Journal of Neuroscience.

[50]  Ravi S. Menon,et al.  Distinguishing subregions of the human MT+ complex using visual fields and pursuit eye movements. , 2001, Journal of neurophysiology.

[51]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

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

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

[54]  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.

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

[56]  David J. Heeger,et al.  Pattern-motion responses in human visual cortex , 2002, Nature Neuroscience.

[57]  K. Hoffmann,et al.  Neural Mechanisms of Saccadic Suppression , 2002, Science.

[58]  Michael Erb,et al.  Object-selective responses in the human motion area MT/MST , 2002, Nature Neuroscience.

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

[60]  Milena Raffi,et al.  Neuronal responses to optic flow in the monkey parietal area PEc. , 2002, Cerebral cortex.

[61]  R. Blake,et al.  Brain Areas Active during Visual Perception of Biological Motion , 2002, Neuron.

[62]  Paul Schrater,et al.  Shape perception reduces activity in human primary visual cortex , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[63]  Ravi S. Menon,et al.  Interaction of Retinal Image and Eye Velocity in Motion Perception , 2003, Neuron.

[64]  Alexandra Battaglia-Mayer,et al.  Functional organization of parietal neuronal responses to optic-flow stimuli. , 2003, Journal of neurophysiology.

[65]  M. Corbetta,et al.  Functional Organization of Human Intraparietal and Frontal Cortex for Attending, Looking, and Pointing , 2003, The Journal of Neuroscience.

[66]  A Pouget,et al.  MSTd neuronal basis functions for the population encoding of heading direction. , 2003, Journal of neurophysiology.

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

[68]  P. Glimcher,et al.  Activity in Posterior Parietal Cortex Is Correlated with the Relative Subjective Desirability of Action , 2004, Neuron.

[69]  Y. Miyashita,et al.  Functional Magnetic Resonance Imaging of Macaque Monkeys Performing Visually Guided Saccade Tasks Comparison of Cortical Eye Fields with Humans , 2004, Neuron.

[70]  Andreas Bartels,et al.  The chronoarchitecture of the human brain—natural viewing conditions reveal a time-based anatomy of the brain , 2004, NeuroImage.

[71]  Hilary W. Heuer,et al.  Parietal Area VIP Neuronal Responses to Heading Stimuli Are Encoded in Head-Centered Coordinates , 2004, Neuron.

[72]  P. Thier,et al.  A neuronal correlate of spatial stability during periods of self-induced visual motion , 2004, Experimental Brain Research.

[73]  S. Zeki,et al.  Functional brain mapping during free viewing of natural scenes , 2004, Human brain mapping.

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

[75]  Alexander Thiele,et al.  Chromatic sensitivity of neurones in area MT of the anaesthetised macaque monkey compared to human motion perception , 2005, Experimental Brain Research.

[76]  D. Heeger,et al.  Topographic organization for delayed saccades in human posterior parietal cortex. , 2005, Journal of neurophysiology.

[77]  Matthew W Self,et al.  The integration of colour and motion by the human visual brain. , 2005, Cerebral cortex.

[78]  S. Sterbing-D’Angelo,et al.  Behavioral/systems/cognitive Multisensory Space Representations in the Macaque Ventral Intraparietal Area , 2022 .

[79]  Andreas Bartels,et al.  Brain dynamics during natural viewing conditions—A new guide for mapping connectivity in vivo , 2005, NeuroImage.

[80]  Jesper Andersson,et al.  Valid conjunction inference with the minimum statistic , 2005, NeuroImage.

[81]  Geraint Rees,et al.  Extraretinal saccadic signals in human LGN and early retinotopic cortex , 2006, NeuroImage.

[82]  D. Heeger,et al.  Sustained Activity in Topographic Areas of Human Posterior Parietal Cortex during Memory-Guided Saccades , 2006, The Journal of Neuroscience.

[83]  Ravi S. Menon,et al.  Representation of Head-Centric Flow in the Human Motion Complex , 2006, The Journal of Neuroscience.

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

[85]  Scott O. Murray,et al.  Contrast Invariance in the Human Lateral Occipital Complex Depends on Attention , 2006, Current Biology.

[86]  Dora E Angelaki,et al.  Visual and Nonvisual Contributions to Three-Dimensional Heading Selectivity in the Medial Superior Temporal Area , 2006, The Journal of Neuroscience.