Selective visual responses to expansion and rotation in the human MT complex revealed by functional magnetic resonance imaging adaptation

Many neurons in the macaque visual area MSTd are sensitive to the global structure of a pattern of moving dots, responding to optic flow components such as expansion and rotation. Direct evidence for neurons with similar properties in humans has been lacking. We have explored sensitivity to optic flow in the human occipital cortex using an event‐related functional magnetic resonance imaging adaptation paradigm. On each trial, two brief random‐dot kinematograms were presented sequentially. Attention was controlled with a demanding task at fixation. In human MST, the compound response was smaller (indicating adaptation) when the two had the same flow structure than when they were different, suggesting the presence of separate neural populations sensitive to rotation and expansion. Surprisingly, the middle‐temporal (MT) gyrus visual area also showed signs of flow specificity, and even V3A showed weak specificity. In V1, which is expected to respond only to local dot motions, no evidence of flow‐specific neurons was found. The same was true in V2, V3, V3B and V4. Control experiments showed that the results cannot be attributed to adaptation to local translation within the flow pattern, or to attentional effects. Our results clearly demonstrate selective responses to specific optic flow structures in MST, and we tentatively suggest that the human MT and even V3A may show similar properties.

[1]  G. Boynton,et al.  Orientation-Specific Adaptation in Human Visual Cortex , 2003, The Journal of Neuroscience.

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

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

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

[5]  Alex R. Wade,et al.  Functional measurements of human ventral occipital cortex: retinotopy and colour. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[6]  D. Kersten,et al.  Orientation-tuned FMRI adaptation in human visual cortex. , 2005, Journal of neurophysiology.

[7]  Tony Ro,et al.  Human MST But Not MT Responds to Tactile Stimulation , 2007, The Journal of Neuroscience.

[8]  C D Frith,et al.  Modulating irrelevant motion perception by varying attentional load in an unrelated task. , 1997, Science.

[9]  K. Grill-Spector,et al.  fMR-adaptation: a tool for studying the functional properties of human cortical neurons. , 2001, Acta psychologica.

[10]  Takeo Watanabe,et al.  Separate Processing of Different Global-Motion Structures in Visual Cortex Is Revealed by fMRI , 2005, Current Biology.

[11]  Alexander M. Harner,et al.  Task-dependent influences of attention on the activation of human primary visual cortex. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[12]  C. Schroeder,et al.  Intermodal selective attention in monkeys. I: distribution and timing of effects across visual areas. , 2000, Cerebral cortex.

[13]  Stephen A Engel,et al.  Adaptation of Oriented and Unoriented Color-Selective Neurons in Human Visual Areas , 2005, Neuron.

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

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

[17]  Z Kourtzi,et al.  Representation of Perceived Object Shape by the Human Lateral Occipital Complex , 2001, Science.

[18]  Alex R. Wade,et al.  Extended Concepts of Occipital Retinotopy , 2005 .

[19]  J. Kaas,et al.  A representation of the visual field in the caudal third of the middle tempral gyrus of the owl monkey (Aotus trivirgatus). , 1971, Brain research.

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

[21]  Karl J. Friston,et al.  Speed-Dependent Motion-Sensitive Responses in V5: An fMRI Study , 1998, NeuroImage.

[22]  G. Orban,et al.  Selectivity of Neuronal Adaptation Does Not Match Response Selectivity: A Single-Cell Study of the fMRI Adaptation Paradigm , 2006, Neuron.

[23]  D. B. Bender,et al.  Effect of attentive fixation in macaque thalamus and cortex. , 2001, Journal of neurophysiology.

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

[25]  G. Boynton,et al.  Adaptation: from single cells to BOLD signals , 2006, Trends in Neurosciences.

[26]  K. Tanaka,et al.  Analysis of motion of the visual field by direction, expansion/contraction, and rotation cells clustered in the dorsal part of the medial superior temporal area of the macaque monkey. , 1989, Journal of neurophysiology.

[27]  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.

[28]  D. Heeger,et al.  Spatial attention affects brain activity in human primary visual cortex. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[29]  K. Amunts,et al.  Human V5/MT+: comparison of functional and cytoarchitectonic data , 2005, Anatomy and Embryology.

[30]  S. Zeki Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey , 1974, The Journal of physiology.

[31]  Alex R. Wade,et al.  Visual areas and spatial summation in human visual cortex , 2001, Vision Research.

[32]  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.

[33]  J. Maunsell,et al.  Effects of Attention on the Processing of Motion in Macaque Middle Temporal and Medial Superior Temporal Visual Cortical Areas , 1999, The Journal of Neuroscience.

[34]  H. Bülthoff,et al.  Representation of the perceived 3-D object shape in the human lateral occipital complex. , 2003, Cerebral cortex.

[35]  Neurosciences,et al.  Organization of Visual Areas in Macaque and Human Cerebral Cortex , 2002 .

[36]  R. Desimone,et al.  Competitive Mechanisms Subserve Attention in Macaque Areas V2 and V4 , 1999, The Journal of Neuroscience.

[37]  G H Recanzone,et al.  Effects of attention on MT and MST neuronal activity during pursuit initiation. , 2000, Journal of neurophysiology.

[38]  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.

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

[40]  Rainer Goebel,et al.  Receptive field size-dependent attention effects in simultaneously presented stimulus displays , 2006, NeuroImage.

[41]  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.

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

[43]  G. Orban,et al.  Responses of macaque STS neurons to optic flow components: a comparison of areas MT and MST. , 1994, Journal of neurophysiology.

[44]  M. Landy,et al.  Orientation-selective adaptation to first- and second-order patterns in human visual cortex. , 2006, Journal of neurophysiology.

[45]  Svetlana S. Georgieva,et al.  Using Functional Magnetic Resonance Imaging to Assess Adaptation and Size Invariance of Shape Processing by Humans and Monkeys , 2005, The Journal of Neuroscience.

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

[47]  H. Ashida,et al.  FMRI adaptation reveals separate mechanisms for first-order and second-order motion. , 2007, Journal of neurophysiology.

[48]  Karl J. Friston,et al.  Speed-dependent motion sensitive responses in V5: an fMRI study , 1998, NeuroImage.

[49]  A. Dale,et al.  Selective averaging of rapidly presented individual trials using fMRI , 1997, Human brain mapping.

[50]  Stefan Treue,et al.  Feature-based attention influences motion processing gain in macaque visual cortex , 1999, Nature.

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

[52]  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.

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

[54]  Guillaume P. Dehaene,et al.  Functional segregation of cortical language areas by sentence repetition , 2006, Human brain mapping.