fMR-adaptation reveals invariant coding of biological motion on the human STS

Frontiers in Human Neuroscience

Volumn 4, Issue , 2010, Pages

  Grossman, Emily D ^a   Jardine, Nicole L ^b   Pyles, John A ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VANDERBILT UNIVERSITY   (United States)

^c CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

Biological motion; fMRI; Superior temporal sulcus; Vision; Visual recognition

Indexed keywords

ARTICLE; BRAIN FUNCTION; BRAIN MAPPING; BRAIN NERVE CELL; BRAIN REGION; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEMODYNAMICS; HUMAN; HUMAN EXPERIMENT; HUMAN VERSUS NONHUMAN DATA; IMAGE ANALYSIS; MALE; MOTION; MOVEMENT PERCEPTION; NUCLEAR MAGNETIC RESONANCE SCANNER; PERCEPTIVE DISCRIMINATION; PHYSICAL ACTIVITY; SUPERIOR TEMPORAL SULCUS;

EID: 78951474403     PISSN: 16625161     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/neuro.09.015.2010     Document Type: Article

References (113)

1. Adolphs, R. (2009). The social brain: neural basis of social knowledge. Annu. Rev. Psychol. 60, 693-716.
2. Allison, T., Puce, A., and McCarthy, G. (2000). Social perception from visual cues: role of the STS region. Trends Cogn. Sci. 4, 267-278.
3. Andresen, D. R., Vinberg, J., and Grill-Spector, K. (2009). The representation of object viewpoint in human visual cortex. Neuroimage 45, 522-536.
4. Andrews, T. J., and Ewbank, M. P. (2004). Distinct representations for facial identity and changeable aspects of faces in the human temporal lobe. Neuroimage 23, 905-913.
5. Ashbridge, E., Perrett, D. I., Oram, M. W., and Jellema, T. (2000). Effect of image orientation and size on object recognition: responses of single units in the macaque monkey temporal cortex. Cogn. Neuropsychol. 17, 13-34.
6. Barraclough, N. E., Xiao, D., Oram, M. W., and Perrett, D. I. (2006). The sensitivity of primate STS neurons to walking sequences and to the degree of articulation in static images. Prog. Brain Res. 154, 135-148.
7. Battelli, L., Cavanagh, P., and Thornton, I. M. (2003). Perception of biological motion in parietal patients. Neuropsychologia 41, 1808-1816.
8. Baylis, G. C., and Rolls, E. T. (1987). Responses of neurons in the inferior temporal cortex in short term and serial recognition memory tasks. Exp. Brain Res. 65, 614-622.
9. Beauchamp, M. S., Lee, K. E., Haxby, J. V., and Martin, A. (2003). FMRI responses to video and point-light displays of moving humans and manipulable objects. J. Cogn. Neurosci. 15, 991-1001.
10. Bedny, M., Caramazza, A., Grossman, E., Pascual-Leone, A., and Saxe, R. (2008). Concepts are more than percepts: the case of action verbs. J. Neurosci. 28, 11347-11353.
11. Blake, R., and Shiffrar, M. (2007). Perception of human motion. Annu. Rev. Psychol. 58, 47-73.
12. Bonda, E., Petrides, M., Ostry, D., and Evans, A. (1996). Specific involvement of human parietal systems and the amygdala in the perception of biological motion. J. Neurosci. 16, 3737-3744.
13. Boynton, G. M., Demb, J. B., Glover, G. H., and Heeger, D. J. (1999). Neuronal basis of contrast discrimination. Vision Res. 39, 257-269.
14. Boynton, G. M., Engel, S. A., Glover, G. H., and Heeger, D. J. (1996). Linear systems analysis of functional magnetic resonance imaging in human V1. J. Neurosci. 16, 4207-4221.
15. Brainard, D. H. (1997). The Psychophyics Toolbox. Spatial Vis, 10, 437-442.
16. Brothers, L. (2002). The social brain: a project for integrating primate behavior and neurophysiology in a new domain. In Foundations in Social Neuroscience, J. T. Cacioppo, G. G. Berntson, S. E. Taylor and D. L. Schacter, eds (Cambridge, MIT Press), 1357 p.
17. Bruce, C., Desimone, R., and Gross, C. G. (1981). Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. J. Neurophysiol. 46, 369-384.
18. Buckner, R. L., Goodman, J., Burock, M., Rotte, M., Koutstaal, W., Schacter, D., Rosen, B., and Dale, A. M. (1998). Functional-anatomic correlates of object priming in humans revealed by rapid presentation event-related fMRI. Neuron 20, 285-296.
19. Campbell, R., MacSweeney, M., Surguladze, S., Calvert, G., McGuire, P., Suckling, J., Brammer, M. J., and David, A. S. (2001). Cortical substrates for the perception of face actions: an fMRI study of the specifi city of activation for seen speech and for meaningless lower-face acts (gurning). Brain Res. Cogn. Brain Res. 12, 233-243.
20. Casile, A., and Giese, M. A. (2005). Critical features for the recognition of biological motion. J Vis 5, 348-360.
21. Cavanagh, P. (1992). Attention-based motion perception. Science 257, 1563-1565.
22. Cusick, C. G. (1996). The superior temporal polysensory region in monkeys. In Extrastriate Cortex in Primates, Vol. 14, K. S. Rockland, J. H. Kaas and A. Peters, eds (New York, Plenum Press), pp. 435-468.
23. Cusick, C. G., Seltzer, B., Cola, M., and Griggs, E. (1995). Chemoarchitectonics and corticocortical terminations within the superior temporal sulcus of the rhesus monkey: evidence for subdivisions of superior temporal polysensory cortex. J. Comp. Neurol. 360, 513-535.
24. Dale, A. M. (1999). Optimal experimental design for event-related fMRI. Hum. Brain Mapp. 8, 109-114.
25. Dale, A. M., and Buckner, R. L. (1997). Selective averaging of rapidly presented individual trials using fMRI. Hum. Brain Mapp. 5, 329-340.
26. Davies, T. N., and Hoffman, D. D. (2003). Facial attention and spacetime fragments. Axiomathes 13, 303-327.
27. de Lussanet, M. H., Fadiga, L., Michels, L., Seitz, R. J., Kleiser, R., and Lappe, M. (2008). Interaction of visual hemifi eld and body view in biological motion perception. Eur. J. Neurosci. 27, 514-522.
28. DiCarlo, J. J., and Cox, D. D. (2007). Untangling invariant object recognition. Trends Cogn. Sci. 11, 333-341.
29. Fahy, F. L., Riches, I. P., and Brown, M. W. (1993). Neuronal activity related to visual recognition memory: long-term memory and the encoding of recency and familiarity information in the primate anterior and medial inferior temporal and rhinal cortex. Exp. Brain Res. 96, 457-472.
30. Fang, F., Murray, S. O., and He, S. (2007). Duration-dependent fMRI adaptation and distributed viewer-centered face representation in human visual cortex. Cereb. Cortex 17, 1402-1411.
31. Ganel, T., Gonzalez, C. L., Valyear, K. F., Culham, J. C., Goodale, M. A., and Kohler, S. (2006). The relationship between fMRI adaptation and repetition priming. Neuroimage 32, 1432-1440.
32. Garcia, J. O., and Grossman, E. D. (2008). Necessary but not suffi cient: motion perception is required for perceiving biological motion. Vision Res. 48, 1144-1149.
33. Genovese, C. R., Lazar, N. A., and Nichols, T. (2002). Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15, 870-878.
34. Gibson, L. A., Sadr, J., Troje, N. F., and Nakayama, K. (2005). Perception of biological motion at varying eccentricity. J Vis 5, 16a.
35. Giese, M. A., and Poggio, T. (2003). Neural mechanisms for the recognition of biological movements. Nat. Rev. Neurosci. 4, 179-192.
36. Gobbini, M. I., Koralek, A. C., Bryan, R. E., Montgomery, K. J., and Haxby, J. V. (2007). Two takes on the social brain: acomparison of theory of mind tasks. J. Cogn. Neurosci. 19, 1803-1814.
37. Grill-Spector, K. (2006). Selectivity of adaptation in single units: implications for fMRI experiments. Neuron 49, 170-171.
38. Grill-Spector, K., Henson, R., and Martin, A. (2006). Repetition and the brain: neural models of stimulus-specific effects. Trends Cogn. Sci. 10, 14-23.
39. Grill-Spector, K., and Malach, R. (2001). FMR-adaptation: a tool for studying the functional properties of human cortical neurons. Acta Psychol. (Amst) 107, 293-321.
40. Grossman, E., Battelli, L., and Pascual-Leone, A. (2005). TMS over STSp disrupts perception of biological motion. Vision Res. 45, 2847-2853.
41. Grossman, E., and Blake, R. (2002). Brain areas active during visual perception of biological motion. Neuron 35, 1157-1165.
42. Grossman, E., Donnelly, M., Price, R., Pickens, D., Morgan, V., Neighbor, G., and Blake, R. (2000). Brain areas involved in perception of biological motion. J. Cogn. Neurosci. 12, 711-720.
43. Grossman, E. D., and Blake, R. (2001). Brain activity evoked by inverted and imagined biological motion. Vision Res. 41, 1475-1482.
44. Grossman, E. D., Kim, C. Y., and Blake, R. (2004). Learning to see biological motion: Brain activity parallels behavior. J. Cogn. Neurosci. 16, 1-11.
45. Haxby, J. V., Hoffman, E. A., and Gobbini, M. I. (2000). The distributed human neural system for face perception. Trends Cogn. Sci. 4, 223-233.
46. Hein, G., and Knight, R. T. (2008). Superior temporal sulcus - it's my area: or is it? J. Cogn. Neurosci. 20, 2125-2136.
47. Henson, R. N., Cansino, S., Herron, J. E., Robb, W. G., and Rugg, M. D. (2003). A familiarity signal in human anterior medial temporal cortex? Hippocampus 13, 301-304.
48. Hickok, G. (2009). Eight problems for the mirror neuron theory of action understanding in monkeys and humans. J. Cogn. Neurosci. 21, 1229-1243.
49. Hickok, G., and Poeppel, D. (2000). Towards a functional neuroanatomy of speech perception. Trends Cogn. Sci. 4, 131-138.
50. Hickok, G., and Saberi, K. (in press). Redefining the functional organization of the planum temporale region: space, objects and sensory-motor integration. In Springer Handbook on Auditory Research: Human Auditory Cortex, D. Poeppel, T. Overath, A. N. Popper and R. R. Fay, eds (Springer).
51. Huk, A. C., Dougherty, R. F., and Heeger, D. J. (2002). Retinotopy and functional subdivision of human areas MT and MST. J. Neurosci. 22, 7195-7205.
52. Huk, A. C., Ress, D., and Heeger, D. J. (2001). Neuronal basis of the motion aftereffect reconsidered. Neuron 32, 161-172.
53. Ikeda, H., Blake, R., and Watanabe, K. (2005). Eccentric perception of biological motion is unscalably poor. Vision Res. 45, 1935-1943.
54. Jellema, T., Baker, C. I., Wicker, B., and Perrett, D. I. (2000). Neural representation for the perception of the intentionality of actions. Brain Cogn. 44, 280-302.
55. Jellema, T., Maassen, G., and Perrett, D. I. (2004). Single cell integration of animate form, motion and location in the superior temporal cortex of the macaque monkey. Cereb. Cortex 14, 781-790.
56. Jellema, T., and Perrett, D. I. (2006). Neural representations of perceived bodily actions using a categorical frame of reference. Neuropsychologia 44, 1535-1546.
57. Jones, E. G., and Powell, T. P. (1970). An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain 93, 793-820.
58. Kable, J. W., and Chatterjee, A. (2006). Specifi city of action representations in the lateral occipitotemporal cortex. J. Cogn. Neurosci. 18, 1498-1517.
59. Kourtzi, Z., and Kanwisher, N. (2000). Activation in human MT/MST by static images with implied motion. J. Cogn. Neurosci. 12, 48-55.
60. Kourtzi, Z., and Kanwisher, N. (2001). Representation of perceived object shape by the human lateral occipital complex. Science 293, 1506-1509.
61. Krekelberg, B., Boynton, G. M., and van Wezel, R. J. (2006). Adaptation: from single cells to BOLD signals. Trends Neurosci. 29, 250-256.
62. Kriegeskorte, N., Simmons, W. K., Bellgowan, P. S., and Baker, C. I. (2009). Circular analysis in systems neuroscience: the dangers of double dipping. Nat. Neurosci. 12, 535-540.
63. Lange, J., Georg, K., and Lappe, M. (2006). Visual perception of biological motion by form: a template-matching analysis. J. Vis. 6, 836-849.
64. Lestou, V., Pollick, F. E., and Kourtzi, Z. (2008). Neural substrates for action understanding at different description levels in the human brain. J. Cogn. Neurosci. 20, 324-341.
65. Li, L., Miller, E. K., and Desimone, R. (1993). The representation of stimulus familiarity in anterior inferior temporal cortex. J. Neurophysiol. 69, 1918-1929.
66. Martin, A., and Weisberg, J. (2003). Neural foundations for understanding social and mechanical concepts. Cogn. Neuropsychol. 20, 575-587.
67. Materna, S., Dicke, P. W., and Thier, P. (2008). Dissociable roles of the superior temporal sulcus and the intraparietal sulcus in joint attention: a functional magnetic resonance imaging study. J. Cogn. Neurosci. 20, 108-119.
68. Meyer, M., Baumann, S., Marchina, S., and Jancke, L. (2007). Hemodynamic responses in human multisensory and auditory association cortex to purely visual stimulation. BMC Neurosci. 8, 14.
69. Michels, L., Kleiser, R., de Lussanet, M. H., Seitz, R. J., and Lappe, M. (2009). Brain activity for peripheral biological motion in the posterior superior temporal gyrus and the fusiform gyrus: dependence on visual hemifield and view orientation. Neuroimage 45, 151-159.
70. Michels, L., Lappe, M., and Vaina, L. M. (2005). Visual areas involved in the perception of human movement from dynamic form analysis. Neuroreport 16, 1037-1041.
71. Mistlin, A. J., and Perrett, D. I. (1990). Visual and somatosensory processing in the macaque temporal cortex: the role of 'expectation'. Exp. Brain Res. 82, 437-450.
72. Mitchell, J. P. (2008). Activity in right temporo-parietal junction is not selective for theory-of-mind. Cereb. Cortex 18, 262-271.
73. Muller, J. R., Metha, A. B., Krauskopf, J., and Lennie, P. (1999). Rapid adaptation in visual cortex to the structure of images. Science 285, 1405-1408.
74. Musselwhite, M. J., and Jeffreys, D. A. (1983). Visual evoked potentials to double-pulse pattern presentation. Vision Res. 23, 135-143.
75. Nelissen, K., Vanduffel, W., and 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.
76. Ono, M., Kubic, S., and Abernathy, C. D. (1991). Atlas of the Cerebral Sulci. Stuttgart, Georg Thieme Verlag.
77. Oram, M. W., and Perrett, D. I. (1994). Responses of anterior superior temporal polysensory (STPa) neurons to "biological motion" stimuli. J. Cogn. Neurosci. 6, 99-116.
78. Oram, M. W., and Perrett, D. I. (1996). Integration of form and motion in the anterior superior temporal polysensory area (STPa) of the macaque monkey. J. Neurophysiol. 76, 109-129.
79. Pandya, D. N., and Seltzer, B. (1982). Intrinsic connections and architectonics of posterior parietal cortex in the rhesus monkey. J. Comp. Neurol. 204, 196-210.
80. Pavlova, M., Staudt, M., Sokolov, A., Birbaumer, N., and Krageloh-Mann, I. (2003). Perception and production of biological movements in patients with early periventricular brain lesions. Brain 126(Pt. 3), 692-701.
81. Peelen, M. V., Glaser, B., Vuilleumier, P., and Eliez, S. (2009). Differential development of selectivity for faces and bodies in the fusiform gyrus. Dev. Sci. 12, F16-F25.
82. Peelen, M. V., Wiggett, A. J., and Downing, P. E. (2006). Patterns of fMRI activity dissociate overlapping functional brain areas that respond to biological motion. Neuron 49, 815-822.
83. Pelli, D. G. (1997). The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spatial Vis, 10, 437-442.
84. Pelphrey, K. A., Morris, J. P., Michelich, C. R., Allison, T., and McCarthy, G. (2005). Functional anatomy of biological motion perception in posterior temporal cortex: an fMRI study of eye, mouth and hand movements. Cereb. Cortex 15, 1866-1876.
85. Perrett, D. I., Smith, P. A., Mistlin, A. J., Chitty, A. J., Head, A. S., Potter, D. D., Broennimann, R., Milner, A. D., and Jeeves, M. A. (1985a). Visual analysis of body movements by neurones in the temporal cortex of the macaque monkey: a preliminary report. Behav. Brain Res. 16, 153-170.
86. Perrett, D. I., Smith, P. A., Potter, D. D., Mistlin, A. J., Head, A. S., Milner, A. D., and Jeeves, M. A. (1985b). Visual cells in the temporal cortex sensitive to face view and gaze direction. Proc. R. Soc. Lond., B, Biol. Sci. 223, 293-317.
87. Peuskens, H., Vanrie, J., Verfaillie, K., and Orban, G. A. (2005). Specificity of regions processing biological motion. Eur. J. Neurosci. 21, 2864-2875.
88. Puce, A., and Perrett, D. (2003). Electrophysiology and brain imaging of biological motion. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 358, 435-445.
89. Pyles, J. A., Garcia, J. O., Hoffman, D. D., and Grossman, E. D. (2007). Visual perception and neural correlates of novel 'biological motion'. Vision Res. 47, 2786-2797.
90. Pyles, J. A., and Grossman, E. D. (2009). Neural adaptation for novel objects during dynamic articulation. Neuropsychologia 47, 1261-1268.
91. Riesenhuber, M., and Poggio, T. (1999). Hierarchical models of object recognition in cortex. Nat. Neurosci. 2, 1019-1025.
92. Riesenhuber, M., and Poggio, T. (2002). Neural mechanisms of object recognition. Curr. Opin. Neurobiol. 12, 162-168.
93. Rizzolatti, G., and Craighero, L. (2004). The mirror-neuron system. Annu. Rev. Neurosci. 27, 169-192.
94. Saxe, R., Xiao, D. K., Kovacs, G., Perrett, D. I., and Kanwisher, N. (2004). A region of right posterior superior temporal sulcus responds to observed intentional actions. Neuropsychologia 42, 1435-1446.
95. Saygin, A. P., and Sereno, M. I. (2008). Retinotopy and attention in human occipital, temporal, parietal, and frontal cortex. Cereb. Cortex 18, 2158-2168.
96. Saygin, A. P., Wilson, S. M., Hagler, D. J., Bates, E., and Sereno, M. I. (2004). Point-light biological motion perception activates human premotor cortex. J. Neurosci. 24, 6181-6188.
97. Self, M. W., and Zeki, S. (2005). The integration of colour and motion by the human visual brain. Cereb. Cortex 15, 1270-1279.
98. Seltzer, B., and Pandya, D. N. (1978). Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey. Brain Res. 149, 1-24.
99. Serences, J. T. (2004). A comparison of methods for characterizing the eventrelated BOLD timeseries in rapid fMRI. Neuroimage 21, 1690-1700.
100. Sobotka, S., and Ringo, J. L. (1994). Stimulus specifi c adaptation in excited but not in inhibited cells in inferotemporal cortex of macaque. Brain Res. 646, 95-99.
101. Talairach, J., and Tournoux, P. (1988). Co-planar Stereotaxic Atlas of the Human Brain. New York, Thieme Medical.
102. Tanaka, K. (1996). Inferotemporal cortex and object vision. Annu. Rev. Neurosci. 19, 109-139.
103. Taylor, J. C., Wiggett, A. J., and Downing, P. E. (2007). Functional MRI analysis of body and body part representations in the extrastriate and fusiform body areas. J. Neurophysiol. 98, 1626-1633.
104. Taylor, J. C., Wiggett, A. J., and Downing, P. E. (2009). FMRI-adaptation studies of viewpoint tuning in the extrastriate and fusiform body areas. J. Neurophysiol. 98, 1626-1633.
105. Thompson, B., Hansen, B. C., Hess, R. F., and Troje, N. F. (2007). Peripheral vision: good for biological motion, bad for signal noise segregation? J. Vis. 7, 12: 11-17.
106. Thompson, J. C., Clarke, M., Stewart, T., and Puce, A. (2005). Configural processing of biological motion in human superior temporal sulcus. J. Neurosci. 25, 9059-9066.
107. Thurman, S. M., and Grossman, E. D. (2008). Temporal "Bubbles" reveal key features in point-light biological motion perception. J. Vis. 8, 28: 1-11.
108. Vaina, L. M., Cowey, A., Eskew, R. T. Jr., LeMay, M., and Kemper, T. (2001a). Regional cerebral correlates of global motion perception: evidence from unilateral cerebral brain damage. Brain 124(Pt. 2), 310-321.
109. Vaina, L. M., Solomon, J., Chowdhury, S., Sinha, P., and Belliveau, J. W. (2001b). Functional neuroanatomy of biological motion perception in humans. Proc. Natl. Acad. Sci. U.S.A. 98, 11656-11661.
110. Vangeneugden, J., Pollick, F., and Vogels, R. (2009). Functional differentiation of macaque visual temporal cortical neurons using a parametric action space. Cereb. Cortex 19, 593-611.
111. Wachsmuth, E., Oram, M. W., and Perrett, D. I. (1994). Recognition of objects and their component parts: responses of single units in the temporal cortex of the macaque. Cereb. Cortex 5, 509-522.
112. Wandell, B. A., Dumoulin, S. O., and Brewer, A. A. (2007). Visual field maps in human cortex. Neuron 56, 366-383.
113. Wheaton, K. J., Thompson, J. C., Syngeniotis, A., Abbott, D. F., and Puce, A. (2004). Viewing the motion of human body parts activates different regions of premotor, temporal, and parietal cortex. Neuroimage 22, 277-288.