Pattern-motion selective responses in MT, MST and the pulvinar of humans

European Journal of Neuroscience

Volumn 36, Issue 6, 2012, Pages 2849-2858

  Villeneuve, M Y ^a   Thompson, B ^b   Hess, R F ^c   Casanova, C ^d  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c ROYAL VICTORIA HOSPITAL   (Canada)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Dorsal pathway; FMRI; HMT+; Integration; Plaid; V5

Indexed keywords

ADULT; ARTICLE; BOLD SIGNAL; BRAIN MAPPING; EYE MOVEMENT; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; LUMINANCE; MALE; MIDDLE TEMPORAL GYRUS; NEUROIMAGING; NORMAL HUMAN; PATTERN RECOGNITION; PRIORITY JOURNAL; PULVINAR; SENSORIMOTOR INTEGRATION; SUPERIOR TEMPORAL GYRUS; VISUAL CORTEX; VISUAL FIELD; VISUAL STIMULATION; VISUAL SYSTEM;

ADULT; BRAIN MAPPING; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MOTION PERCEPTION; PATTERN RECOGNITION, VISUAL; PULVINAR; VISUAL CORTEX;

EID: 84866372658     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2012.08205.x     Document Type: Article

References (79)

1. Abramson, B.P. & Chalupa, L.M. (1985) The laminar distribution of cortical connections with the tecto- and cortico-recipient zones in the cat's lateral posterior nucleus. Neuroscience, 15, 81-95.
2. Adams, M.M., Hof, P.R., Gattass, R., Webster, M.J. & Ungerleider, L.G. (2000) Visual cortical projections and chemoarchitecture of macaque monkey pulvinar. J. Comp. Neurol., 419, 377-393.
3. Adelson, E.H. & Movshon, J.A. (1982) Phenomenal coherence of moving visual patterns. Nature, 300, 523-525.
4. Albright, T.D. (1984) Direction and orientation selectivity of neurons in visual area MT of the macaque. J. Neurophysiol., 52, 1106-1130.
5. Barnes, G.R., Li, X., Thompson, B., Singh, K.D., Dumoulin, S.O. & Hess, R.F. (2010) Decreased gray matter concentration in the lateral geniculate nuclei in human amblyopes. Invest. Ophthalmol. Vis. Sci., 51, 1432-1438.
6. Benjamini, Y. & Hockberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B Methodol. 57, 289-300.
7. Born, R.T. & Bradley, D.C. (2005) Structure and function of visual area MT. Annu. Rev. Neurosci., 28, 157-189.
8. Bowns, L. (2002) Can spatio-temporal energy models of motion predict feature motion?Vision. Res., 42, 1671-1681.
9. Bruce, C., Desimone, R. & Gross, C.G. (1981) Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. J. Neurophysiol., 46, 369-384.
10. Casanova, C. (2004) The visual function of the pulvinar. In Chalupa, L.M. & Werner, J.S. (Eds), The Visual Neurosciences. MIT Press, Cambridge, MA, pp. 592-608.
11. Castelo-Branco, M., Formisano, E., Backes, W., Zanella, F., Neuenschwander, S., Singer, W. & Goebel, R. (2002) Activity patterns in human motion-sensitive areas depend on the interpretation of global motion. Proc. Natl Acad. Sci. USA, 99, 13914-13919.
12. Champion, R.A., Hammett, S.T. & Thompson, P.G. (2007) Perceived direction of plaid motion is not predicted by component speeds. Vision. Res., 47, 375-83.
13. Clifford, C. & Vaina, L.M. (1999) Anomalous perception of coherence and transparency in moving plaid patterns. Brain Res. Cogn. Brain. Res., 8, 345-353.
14. Cotton, P.L. & Smith, A.T. (2007) Contralateral visual hemifield representations in the human pulvinar nucleus. J. Neurophysiol., 98, 1600-1609.
15. Desimone, R. & Ungerleider, L.G. (1986) Multiple visual areas in the caudal superior temporal sulcus of the macaque. J. Comp. Neurol., 248, 164-189.
16. Duffy, C.J. & Wurtz, R.H. (1991) Sensitivity of MST neurons to optic flow stimuli. I. A continuum of response selectivity to large-field stimuli. J. Neurophysiol., 65, 1329-1345.
17. Dukelow, S.P., DeSouza, J.F., Culham, J.C., van den Berg, A.V., Menon, R.S. & Vilis, T. (2001) Distinguishing subregions of the human MT+ complex using visual fields and pursuit eye movements. J. Neurophysiol., 86, 1991-2000.
18. Dumoulin, S.O., Bittar, R.G., Kabani, N.J., Baker, C.L. Jr, Le Goualher, G., Bruce Pike, G. & Evans, A.C. (2000) A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning. Cereb. Cortex, 10, 454-463.
19. Dumoulin, S.O., Hoge, R.D., Baker, C.L. Jr, Hess, R.F., Achtman, R.L. & Evans, A.C. (2003) Automatic volumetric segmentation of human visual retinotopic cortex. Neuroimage, 18, 576-587.
20. Dursteler, M.R. & Wurtz, R.H. (1988) Pursuit and optokinetic deficits following chemical lesions of cortical areas MT and MST. J. Neurophysiol., 60, 940-965.
21. Gegenfurtner, K.R., Kiper, D.C. & Levitt, J.B. (1997) Functional properties of neurons in macaque area V3. J. Neurophysiol., 77, 1906-1923.
22. Gutierrez, C., Yaun, A. & Cusick, C.G. (1995) Neurochemical subdivisions of the inferior pulvinar in macaque monkeys. J. Comp. Neurol., 363, 545-562.
23. Heeger, D.J., Boynton, G.M., Demb, J.B., Seidemann, E. & Newsome, W.T. (1999) Motion opponency in visual cortex. J. Neurosci., 19, 7162-7174.
24. Huk, A.C. & Heeger, D.J. (2002) Pattern-motion responses in human visual cortex. Nat. Neurosci., 5, 72-75.
25. Huk, A.C., Dougherty, R.F. & Heeger, D.J. (2002) Retinotopy and functional subdivision of human areas MT and MST. J. Neurosci., 22, 7195-7205.
26. Hupe, J.M. & Rubin, N. (2003) The dynamics of bi-stable alternation in ambiguous motion displays: a fresh look at plaids. Vision Res., 43, 531-548.
27. Kaas, J.H. & Lyon, D.C. (2007) Pulvinar contributions to the dorsal and ventral streams of visual processing in primates. Brain Res. Rev., 55, 285-296.
28. Kastner, S., O'Connor, D.H., Fukui, M.M., Fehd, H.M., Herwig, U. & Pinsk, M.A. (2004) Functional imaging of the human lateral geniculate nucleus and pulvinar. J. Neurophysiol., 91, 438-448.
29. Khawaja, F.A., Tsui, J.M. & Pack, C.C. (2009) Pattern motion selectivity of spiking outputs and local field potentials in macaque visual cortex. J. Neurosci., 29, 13702-13709.
30. Komatsu, H. & Wurtz, R.H. (1988) Relation of cortical areas MT and MST to pursuit eye movements. I. Localization and visual properties of neurons. J. Neurophysiol., 60, 580-603.
31. Lemaire, J.J., Sakka, L., Ouchchane, L., Caire, F., Gabrillargues, J. & Bonny, J.M. (2010) Anatomy of the human thalamus based on spontaneous contrast and microscopic voxels in high-field magnetic resonance imaging. Neurosurgery, 66, 161-172.
32. Li, X., Dumoulin, S.O., Mansouri, B. & Hess, R.F. (2007) The fidelity of the cortical retinotopic map in human amblyopia. Eur. J. Neurosci., 25, 1265-1277.
33. Logothetis, N.K., Pauls, J., Augath, M., Trinath, T. & Oeltermann, A. (2001) Neurophysiological investigation of the basis of the fMRI signal. Nature, 412, 150-157.
34. Malonek, D., Tootell, R.B. & Grinvald, A. (1994) Optical imaging reveals the functional architecture of neurons processing shape and motion in owl monkey area MT. Proc. Biol. Sci., 258, 109-119.
35. Merabet, L., Desautels, A., Minville, K. & Casanova, C. (1998) Motion integration in a thalamic visual nucleus. Nature, 396, 265-268.
36. Morel, A., Magnin, M. & Jeanmonod, D. (1997) Multiarchitectonic and stereotactic atlas of the human thalamus. J. Comp. Neurol., 387, 588-630.
37. Movshon, J.A. & Newsome, W.T. (1996) Visual response properties of striate cortical neuronsprojecting to area MT in macaque monkeys. J. Neurosci., 16, 7733-7741.
38. Movshon, J.A., Adelson, E.H., Gizzi, M.S. & Newsome, W.T. (1985) The analysis of moving visual patterns. In Pattern Recognition Mechanisms. C. Chagas, R. Gattass and C. Gross (Eds), Springer-Verlag, NY. pp. 117-151.
39. Mumford, D. (1991) On the computational architecture of the neocortex I. The role of the thalamo-cortical loop. Biol. Cybern., 65, 135-145.
40. Nelissen, K., Vanduffel, W. & Orban, G.A. (2006) Charting the lower superior temporal region, a new motion-sensitive region in monkey superior temporal sulcus. J. Neurosci., 26, 5929-5947.
41. Newsome, W.T. & Pare, E.B. (1988) A selective impairment of motion perception following lesions of the middle temporal visual area (MT). J. Neurosci., 8, 2201-2211.
42. Orban, G.A. (2008) Higher order visual processing in macaque extrastriate cortex. Physiol. Rev., 88, 59-89.
43. Orban, G.A., Saunders, R.C. & Vandenbussche, E. (1995) Lesions of the superior temporal cortical motion areas impair speed discrimination in the macaque monkey. Eur. J. Neurosci., 7, 2261-2276.
44. Orban, G.A., Van Essen, D. & Vanduffel, W. (2004) Comparative mapping of higher visual areas in monkeys and humans. Trends Cogn. Sci., 8, 315-324.
45. Pack, C.C., Berezovskii, V.K. & Born, R.T. (2001) Dynamic properties of neurons in cortical area MT in alert and anaesthetized macaque monkeys. Nature, 414, 905-908.
46. Perrone, J.A. & Krauzlis, R.J. (2008) Spatial integration by MT pattern neurons: a closer look at pattern-to-component effects and the role of speed tuning. J. Vis., 8, 1-14.
47. Ptito, M., Johannsen, P., Faubert, J. & Gjedde, A. (1999) Activation of human extrageniculostriate pathways after damage to area V1. Neuroimage, 9, 97-107.
48. Ptito, M., Faubert, J., Gjedde, A. & Kupers, R. (2003) Separate neural pathways for contour and biological-motion cues in motion-defined animal shapes. Neuroimage, 19, 246-252.
49. Raiguel, S., Van Hulle, M.M., Xiao, D.K., Marcar, V.L., Lagae, L. & Orban, G.A. (1997) Size and shape of receptive fields in the medial superior temporal area (MST) of the macaque. Neuroreport, 8, 2803-2808.
50. Rodman, H.R. & Albright, T.D. (1989) Single-unit analysis of pattern-motion selective properties in the middle temporal visual area (MT). Exp. Brain Res., 75, 53-64.
51. Rust, N.C., Mante, V., Simoncelli, E.P. & Movshon, J.A. (2006) How MT cells analyze the motion of visual patterns. Nat. Neurosci., 9, 1421-1431.
52. Saalmann, Y.B. & Kastner, S. (2009) Gain control in the visual thalamus during perception and cognition. Curr. Opin. Neurobiol., 19, 408-414.
53. Salzman, C.D., Murasugi, C.M., Britten, K.H. & Newsome, W.T. (1992) Microstimulation in visual area MT: effects on direction discrimination performance. J. Neurosci., 12, 2331-2355.
54. Sherman, S.M. & Guillery, R.W. (2002) The role of the thalamus in the flow of information to the cortex. Philos. Trans. R. Soc. Lond. B Biol. Sci., 357, 1695-1708.
55. Shipp, S. (2001) Corticopulvinar connections of areas V5, V4, and V3 in the macaque monkey: a dual model of retinal and cortical topographies. J. Comp. Neurol., 439, 469-490.
56. Shipp, S. (2003) The functional logic of cortico-pulvinar connections. Philos. Trans. R. Soc. Lond. B Biol. Sci., 358, 1605-1624.
57. Smith, A.T., Wall, M.B., Williams, A.L. & Singh, K.D. (2006) Sensitivity to optic flow in human cortical areas MT and MST. Eur. J. Neurosci., 23, 561-569.
58. Smith, A.T., Cotton, P.L., Bruno, A. & Moutsiana, C. (2009) Dissociating vision and visual attention in the human pulvinar. J. Neurophysiol., 101, 917-925.
59. Stepniewska, I. & Kaas, J.H. (1997) Architectonic subdivisions of the inferior pulvinar in New World and Old World monkeys. Vis. Neurosci., 14, 1043-1060.
60. Tailby, C., Majaj, N.J. & Movshon, J.A. (2010) Binocular integration of pattern motion signals by MT neurons and by human observers. J. Neurosci., 30, 7344-7349.
61. Talairach, J. & Tournoux, P. (1988) Co-Planar Stereotactic Atlas of the Human Brain. Thieme Stuttgart, New York.
62. Tanaka, K., Sugita, Y., Moriya, M. & Saito, H. (1993) Analysis of object motion in the ventral part of the medial superior temporal area of the macaque visual cortex. J. Neurophysiol., 69, 128-142.
63. Thompson, B., Aaen-Stockdale, C.R., Mansouri, B. & Hess, R.F. (2008) Plaid perception is only subtly impaired in strabismic amblyopia. Vision Res., 48, 1307-1314.
64. Thompson, B., Aaen-Stockdale, C., Koski, L. & Hess, R.F. (2009) A double dissociation between striate and extrastriate visual cortex for pattern motion perception revealed using rTMS. Hum. Brain Mapp., 30, 3115-3126.
65. Thompson, B., Villeneuve, M.Y., Casanova, C. & Hess, R.F. (2012) Abnormal cortical processing of pattern motion in amblyopia: evidence from fMRI. Neuroimage, 60, 1307-1315.
66. Tinsley, C.J., Webb, B.S., Barraclough, N.E., Vincent, C.J., Parker, A. & Derrington, A.M. (2003) The nature of V1 neural responses to 2D moving patterns depends on receptive-field structure in the marmoset monkey. J. Neurophysiol., 2, 930-937.
67. Tolias, A.S., Smirnakis, S.M., Augath, M.A., Trinath, T. & Logothetis, N.K. (2001) Motion processing in the macaque: revisited with functional magnetic resonance imaging. J. Neurosci., 21, 8594-8601.
68. Tootell, R.B. & Taylor, J.B. (1995) Anatomical evidence for MT and additional cortical visual areas in humans. Cereb. Cortex, 5, 39-55.
69. Tootell, R.B., Reppas, J.B., Dale, A.M., Look, R.B., Sereno, M.I., Malach, R., Brady, T.J. & Rosen, B.R. (1995a) Visual motion aftereffect in human cortical area MT revealed by functional magnetic resonance imaging. Nature, 375, 139-141.
70. Tootell, R.B., Reppas, J.B., Kwong, K.K., Malach, R., Born, R.T., Brady, T.J., Rosen, B.R. & Belliveau, J.W. (1995b) Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. J. Neurosci., 15, 3215-3230.
71. Tsui, J.M., Hunter, J.N., Born, R.T. & Pack, C.C. (2010) The role of V1 surround suppression in MT motion integration. J. Neurophysiol., 6, 3123-3138.
72. Vaina, L.M., Cowey, A., Jakab, M. & Kikinis, R. (2005) Deficits of motion integration and segregation in patients with unilateral extrastriate lesions. Brain, 128, 2134-2145.
73. Van Essen, D.C., Maunsell, J.H. & Bixby, J.L. (1981) The middle temporal visual area in the macaque: myeloarchitecture, connections, functional properties and topographic organization. J. Comp. Neurol., 199, 293-326.
74. Villeneuve, M.Y., Kupers, R., Gjedde, A., Ptito, M. & Casanova, C. (2005) Pattern-motion selectivity in the human pulvinar. Neuroimage, 28, 474-480.
75. Wenderoth, P., Watson, J.D., Egan, G.F., Tochon-Danguy, H.J. & O'Keefe G, J. (1999) Second order components of moving plaids activate extrastriate cortex: a positron emission tomography study. Neuroimage, 9, 227-234.
76. Wilson, H.R., Ferrera, V.P. & Yo, C. (1992) A psychophysically motivated model for two-dimensional motion perception. Vis. Neurosci., 9, 79-97.
77. Xu, X., Collins, C.E., Khaytin, I., Kaas, J.H. & Casagrande, V.A. (2006) Unequal representation of cardinal vs. oblique orientations in the middle temporal visual area. Proc. Natl Acad. Sci. USA, 103, 17490-17495.
78. Zeki, S.M. (1974) Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. J. Physiol., 236, 549-573.
79. Zeki, S., Watson, J.D., Lueck, C.J., Friston, K.J., Kennard, C. & Frackowiak, R.S. (1991) A direct demonstration of functional specialization in human visual cortex. J. Neurosci., 11, 641-649.