Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging

Using noninvasive functional magnetic resonance imaging (fMRI) technique, we analyzed the responses in human area MT with regard to visual motion, color, and luminance contrast sensitivity, and retinotopy. As in previous PET studies, we found that area MT responded selectively to moving (compared to stationary) stimuli. The location of human MT in the present fMRI results is consistent with that of MT in earlier PET and anatomical studies. In addition we found that area MT has a much higher contrast sensitivity than that in several other areas, including primary visual cortex (V1). Functional MRI half- amplitudes in V1 and MT occurred at approximately 15% and 1% luminance contrast, respectively. High sensitivity to contrast and motion in MT have been closely associated with magnocellular stream specialization in nonhuman primates. Human psychophysics indicates that visual motion appears to diminish when moving color-varying stimuli are equated in luminance. Electrophysiological results from macaque MT suggest that the human percept could be due to decreases in firing of area MT cells at equiluminance. We show here that fMRI activity in human MT does in fact decrease at and near individually measured equiluminance. Tests with visuotopically restricted stimuli in each hemifield produced spatial variations in fMRI activity consistent with retinotopy in human homologs of macaque areas V1, V2, V3, and VP. Such activity in area MT appeared much less retinotopic, as in macaque. However, it was possible to measure the interhemispheric spread of fMRI activity in human MT (half amplitude activation across the vertical meridian = approximately 15 degrees).

[1]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[2]  S. M. Axstis PHI MOVEMENT AS A SUBTRACTION PROCESS , 1970 .

[3]  S. Zeki,et al.  Response properties and receptive fields of cells in an anatomically defined region of the superior temporal sulcus in the monkey. , 1971, Brain research.

[4]  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.

[5]  J M Allman,et al.  The middle temporal visual area(MT)in the bushbaby, Galago senegalensis. , 1973, Brain research.

[6]  R. L. Valois,et al.  Psychophysical studies of monkey vision. I. Macaque luminosity and color vision tests. , 1974, Vision research.

[7]  R. L. de Valois,et al.  Psychophysical studies of monkey vision. 3. Spatial luminance contrast sensitivity tests of macaque and human observers. , 1974, Vision research.

[8]  H. Morgan,et al.  Psychophysical studies of monkey vision. II. Squirrel monkey wavelength and saturation discrimination. , 1974, Vision research.

[9]  J. Lund,et al.  Interlaminar connections and pyramidal neuron organisation in the visual cortex, area 17, of the Macaque monkey , 1975 .

[10]  J. Lund,et al.  The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase , 1975, The Journal of comparative neurology.

[11]  J. Kaas,et al.  Representation of the visual field on the medial wall of occipital-parietal cortex in the owl monkey. , 1976, Science.

[12]  G. H. Jacobs Visual capacities of the owl monkey (Aotus trivirgatus)—I. Spectral sensitivity and color vision , 1977, Vision Research.

[13]  G. H. Jacobs Visual capacities of the owl monkey (Aotus trivirgatus)—II. Spatial contrast sensitivity , 1977, Vision Research.

[14]  V. S. RAMACHANDRAN,et al.  Does colour provide an input to human motion perception? , 1978, Nature.

[15]  W H Dobelle,et al.  Mapping the representation of the visual field by electrical stimulation of human visual cortex. , 1979, American journal of ophthalmology.

[16]  Eric L. Schwartz,et al.  Computational anatomy and functional architecture of striate cortex: A spatial mapping approach to perceptual coding , 1980, Vision Research.

[17]  S. Zeki The response properties of cells in the middle temporal area (area MT) of owl monkey visual cortex , 1980, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[18]  M. Novacek,et al.  Evolutionary Biology of the New World Monkeys and Continental Drift , 1980, Advances in Primatology.

[19]  Juhani Hyva¨rinen Regional distribution of functions in parietal association area 7 of the monkey , 1981, Brain Research.

[20]  B. C. Motter,et al.  The functional properties of the light-sensitive neurons of the posterior parietal cortex studied in waking monkeys: foveal sparing and opponent vector organization , 1981, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[21]  John H. R. Maunsell,et al.  The middle temporal visual area in the macaque: Myeloarchitecture, connections, functional properties and topographic organization , 1981, The Journal of comparative neurology.

[22]  C. Gross,et al.  Visual topography of striate projection zone (MT) in posterior superior temporal sulcus of the macaque. , 1981, Journal of neurophysiology.

[23]  J Hyvärinen,et al.  Regional distribution of functions in parietal association area 7 of the monkey. , 1981, Brain research.

[24]  R. Shapley,et al.  X and Y cells in the lateral geniculate nucleus of macaque monkeys. , 1982, The Journal of physiology.

[25]  D C Van Essen,et al.  Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. , 1983, Journal of neurophysiology.

[26]  Carol L. Colby,et al.  The responses of single cells in the lateral geniculate nucleus of the rhesus monkey to color and luminance contrast , 1983, Vision Research.

[27]  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.

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

[29]  T. Albright Direction and orientation selectivity of neurons in visual area MT of the macaque. , 1984, Journal of neurophysiology.

[30]  P. Lennie,et al.  Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. , 1984, The Journal of physiology.

[31]  G. Blasdel,et al.  Intrinsic connections of macaque striate cortex: afferent and efferent connections of lamina 4C , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  E. DeYoe,et al.  Segregation of efferent connections and receptive field properties in visual area V2 of the macaque , 1985, Nature.

[33]  S. Zeki,et al.  Segregation of pathways leading from area V2 to areas V4 and V5 of macaque monkey visual cortex , 1985, Nature.

[34]  R B Tootell,et al.  Topography of cytochrome oxidase activity in owl monkey cortex , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  William H. Press,et al.  Numerical recipes in C. The art of scientific computing , 1987 .

[36]  R. Shapley,et al.  Cat and monkey retinal ganglion cells and their visual functional roles , 1986, Trends in Neurosciences.

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

[38]  D. J. Felleman,et al.  Anatomical and physiological asymmetries related to visual areas V3 and VP in macaque extrastriate cortex , 1986, Vision Research.

[39]  John H. R. Maunsell,et al.  Visual processing in monkey extrastriate cortex. , 1987, Annual review of neuroscience.

[40]  John H. R. Maunsell,et al.  Physiological Evidence for Two Visual Subsystems , 1987 .

[41]  John H. R. Maunsell,et al.  Topographic organization of the middle temporal visual area in the macaque monkey: Representational biases and the relationship to callosal connections and myeloarchitectonic boundaries , 1987, The Journal of comparative neurology.

[42]  M. Kendall,et al.  Kendall's advanced theory of statistics , 1995 .

[43]  D. C. Van Essen,et al.  Concurrent processing streams in monkey visual cortex , 1988, Trends in Neurosciences.

[44]  E. Switkes,et al.  Functional anatomy of macaque striate cortex. IV. Contrast and magno- parvo streams , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[45]  R. Shapley,et al.  Background light and the contrast gain of primate P and M retinal ganglion cells. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Kevan A. C. Martin,et al.  From enzymes to visual perception: a bridge too far? , 1988, Trends in Neurosciences.

[47]  S. Shipp,et al.  The functional logic of cortical connections , 1988, Nature.

[48]  R B Buxton,et al.  Susceptibility induced MR line broadening: applications to brain iron mapping. , 1988, Journal of computer assisted tomography.

[49]  D. Hubel,et al.  Segregation of form, color, movement, and depth: anatomy, physiology, and perception. , 1988, Science.

[50]  M. Hawken,et al.  Laminar organization and contrast sensitivity of direction-selective cells in the striate cortex of the Old World monkey , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[51]  E. Switkes,et al.  Functional anatomy of macaque striate cortex. II. Retinotopic organization , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  Karl J. Friston,et al.  The colour centre in the cerebral cortex of man , 1989, Nature.

[53]  F. A. Seiler,et al.  Numerical Recipes in C: The Art of Scientific Computing , 1989 .

[54]  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.

[55]  T. Albright Centrifugal directional bias in the middle temporal visual area (MT) of the macaque , 1989, Visual Neuroscience.

[56]  R Gattass,et al.  Visual area MT in the Cebus monkey: Location, visuotopic organization, and variability , 1989, The Journal of comparative neurology.

[57]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[58]  R. Tootell,et al.  Molecular differences among neurons reveal an organization of human visual cortex. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[59]  DH Hubel,et al.  Color and contrast sensitivity in the lateral geniculate body and primary visual cortex of the macaque monkey , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[60]  L A Krubitzer,et al.  Cortical connections of MT in four species of primates: Areal, modular, and retinotopic patterns , 1990, Visual Neuroscience.

[61]  N. Logothetis,et al.  Role of the color-opponent and broad-band channels in vision , 1990, Visual Neuroscience.

[62]  R. M. Siegel,et al.  Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule , 1990, The Journal of comparative neurology.

[63]  S. Zeki,et al.  A century of cerebral achromatopsia. , 1990, Brain : a journal of neurology.

[64]  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.

[65]  M Corbetta,et al.  Attentional modulation of neural processing of shape, color, and velocity in humans. , 1990, Science.

[66]  A. Damasio,et al.  Face agnosia and the neural substrates of memory. , 1990, Annual review of neuroscience.

[67]  S. Clarke,et al.  Occipital cortex in man: Organization of callosal connections, related myelo‐ and cytoarchitecture, and putative boundaries of functional visual areas , 1990, The Journal of comparative neurology.

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

[69]  Martin I. Sereno,et al.  Cortical visual areas in mammals , 1991 .

[70]  Jon H. Kaas,et al.  Hierarchical, parallel, and serial arrangements of sensory cortical areas: connection patterns and functional aspects , 1991, Current Opinion in Neurobiology.

[71]  B. Rosen,et al.  Functional mapping of the human visual cortex by magnetic resonance imaging. , 1991, Science.

[72]  Stuart Anstis,et al.  The contribution of color to motion in normal and color-deficient observers , 1991, Vision Research.

[73]  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.

[74]  A. Leventhal The neural basis of visual function , 1991 .

[75]  B. Rosen,et al.  MR Contrast Due to Microscopically Heterogeneous Magnetic Susceptibility: Numerical Simulations and Applications to Cerebral Physiology , 1991, Magnetic resonance in medicine.

[76]  S. Zeki,et al.  Cerebral akinetopsia (visual motion blindness). A review. , 1991, Brain : a journal of neurology.

[77]  J. Horton,et al.  Quadrantic visual field defects. A hallmark of lesions in extrastriate (V2/V3) cortex. , 1991, Brain : a journal of neurology.

[78]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[79]  Thomas D. Albright,et al.  Color and the integration of motion signals , 1991, Trends in Neurosciences.

[80]  J. Horton,et al.  The representation of the visual field in human striate cortex. A revision of the classic Holmes map. , 1991, Archives of ophthalmology.

[81]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[82]  Roger B. H. Tootell,et al.  Segregation of global and local motion processing in primate middle temporal visual area , 1992, Nature.

[83]  T. Albright,et al.  Motion coherency rules are form-cue invariant , 1992, Vision Research.

[84]  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.

[85]  J. R. Baker,et al.  Magnetic Resonance Imaging Mapping of Brain Function: Human Visual Cortex , 1992, Investigative radiology.

[86]  R. S. Hinks,et al.  Time course EPI of human brain function during task activation , 1992, Magnetic resonance in medicine.

[87]  T D Albright,et al.  Form-cue invariant motion processing in primate visual cortex. , 1992, Science.

[88]  D C Van Essen,et al.  Information processing in the primate visual system: an integrated systems perspective. , 1992, Science.

[89]  J. Mazziotta,et al.  Rapid Automated Algorithm for Aligning and Reslicing PET Images , 1992, Journal of computer assisted tomography.

[90]  F. Crick,et al.  Backwardness of human neuroanatomy , 1993, Nature.

[91]  John H. R. Maunsell,et al.  How parallel are the primate visual pathways? , 1993, Annual review of neuroscience.

[92]  A. B. Bonds,et al.  Visual resolution and sensitivity of single cells in the primary visual cortex (V1) of a nocturnal primate (bush baby): correlations with cortical layers and cytochrome oxidase patterns. , 1993, Journal of neurophysiology.

[93]  Jon H. Kaas,et al.  The Organization of Visual Cortex in Primates: Problems, Conclusions, and the Use of Comparative Studies in Understanding the Human Brain , 1993 .

[94]  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.

[95]  Jonathan D. Cohen,et al.  Functional topographic mapping of the cortical ribbon in human vision with conventional MRI scanners , 1993, Nature.

[96]  R. Born,et al.  Segregation of global and local motion processing in primate middle temporal visual area , 1993, Nature.

[97]  J. Frahm,et al.  Functional MRI of human brain activation at high spatial resolution , 1993, Magnetic resonance in medicine.

[98]  Patrick Cavanagh,et al.  The perception of form and motion , 1993, Current Opinion in Neurobiology.

[99]  A. W. Kemp,et al.  Kendall's Advanced Theory of Statistics. , 1994 .

[100]  Karl R. Gegenfurtner,et al.  Contrast dependence of colour and luminance motion mechanisms in human vision , 1994, Nature.

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

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

[103]  J. Movshon,et al.  Chromatic properties of neurons in macaque MT , 1994, Visual Neuroscience.