Complex motion perception and its deficits

Current Opinion in Neurobiology

Volumn 8, Issue 4, 1998, Pages 494-502

  Vaina, Lucia M ^a,b  

^a Brain and Vision Research Laboratory   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN NERVE CELL; HUMAN; MOVEMENT PERCEPTION; PRIORITY JOURNAL; RECEPTIVE FIELD; REVIEW; TEMPORAL LOBE; VISUAL CORTEX;

EID: 0032143473     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0959-4388(98)80037-8     Document Type: Article

References (75)

1. Saito H-a, Yukie M, Tanaka K, Hikosaka K, Fukada Y, Iwai E. Integration of direction signals of image motion in the superior temporal sulcus of the macaque monkey. J Neurosci. 6:1986;145-157.
2. Tanaka K, Fukada Y, Saito H-a. Underlying mechanisms of the response specificity of expansion/contraction and rotation cells in the dorsal part of the medial superior temporal area of the macaque monkey. J Neurophysiol. 62:1989;642-656.
3. Duffy CJ, Wurtz RH. Sensitivity of MST neurons to optic flow stimuli. II. Mechanisms of response selectivity revealed by small field stimuli. J Neurophysiol. 65:1991;1346-1359.
4. Duffy CJ, Wurtz RH. Sensitivity of MST neurons to optic flow stimuli. I. A continuum of response selectivity to large-field stimuli. J Neurophysiol. 65:1991;1329-1345.
5. Orban GA, Lagae L, Verri A, Raiguel S, Xiao D, Maes H, Torre V. First-order analysis of optical flow in monkey brain. Proc Natl Acad Sci USA. 89:1992;2595-2599.
6. Graziano MS, Andersen RA, Snowden R. Tuning of MST neurons to spiral motions. J Neurosci. 124:1994;54-67.
7. Gibson JJ. The Perception of the Visual World. 1950;Houghton Mifflin, Boston.
8. Tanaka K, Hikosaka K, Saito H, Yukie M, Fukada Y, Iwai E. Analysis of local and wide-field movements in the superior temporal visual areas of the macaque monkey. J Neurosci. 6:1986;134-144.
9. Tanaka K, Saito H. 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. J Neurophysiol. 62:1989;626-641.
10. Wurtz RH, Duffy CJ. Neuronal correlates of optic flow stimulation. Ann NY Acad Sci. 656:1992;205-218.
11. Andersen RA, Snowden RJ, Treue S, Graziano M. Hierarchical processing of motion. Proceedings of the Cold Springs Harbor Symposium on The Brain. 1990;741-748 Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
12. Duffy CJ, Wurtz RH. Medial superior temporal areas respond to speed patterns in optic flow. of outstanding interest J Neurosci. 17:1997;2839-2851 The authors studied the responses of MSTd neurones to the speed of optical flow stimuli. They report a range of response profiles to the mean speed of a stimulus, but found that nearly 90% of the cells studied preferred stimuli containing a speed gradient to those in which all the dots moved at the same speed. They conclude that the sensitivity of MSTd neurones to patterns of speed, as well as to patterns of direction, strengthens the view that MSTd is involved in the analysis of optical flow for representation of the structure of the three-dimensional visual environment.
13. Britten K, Van Wezel R. Electrical microstimulation of cortical area MST biases heading perception in monkeys. Nat Neurosci. 1:1998;59-64 Electrical microstimulation of MST neurones while trained monkeys performed a visual heading discrimination task induced a significant bias in the monkey's decision. This suggests that for forming heading judgements, monkeys use signals representing heading.
14. of outstanding interest Duffy CJ, Wurtz RH. Response of monkey MST neurons to optic flow stimuli with shifted centers of motion. J Neurosci. 15:1995;5192-5208.
15. Britten KH. Clustering of responses selectivity in the medial superior temporal area of extrastriate cortex in the macaque monkey. Vis Neurosci. 1998;. in press.
16. Lappe M, Bremmer F, Pekel M, Thiele A, Hoffmann KP. Optic flow processing in monkey STS: a theoretical and experimental approach. J Neurosci. 16:1996;6265-6285.
17. Bradley DC, Maxwell M, Andersen RA, Banks MS, Shenoy KV. Mechanisms of heading perception in primate visual cortex. Science. 273:1996;1544-1547.
18. Lappe M, Pekel M, Hoffmann KP. Optokinetic eye movements elicited by radial optic flow in the macaque monkey. of outstanding interest J Neurophysiol. 79:1998;1461-1480 This detailed and thorough neurophysiology paper investigates whether spontaneous eye movements in macaque monkeys are elicited by radial optic flow. The authors were interested to determine whether optic flow stimuli simulating self-movement would induce optokinetic eye movements and, if so, to characterise the attributes of these movements. The authors found strong evidence that an optokinetic system exists in the monkey. First, the experimental results suggest that, at least in part, eye movements are elicited passively by retinal slip occurring in optic flow fields, especially when the eyes deviate from the focus of expansion. Second, the deviation of the eye movements direction from the local direction on the fovea provides evidence for the integration of the surrounding motion vectors that is typical for the optokinetic system. Another important, although controversial, finding of this study is that the monkeys tend to shift the median eye position into the focus of expansion, but contraction stimuli produce shifts in the opposite direction. Furthermore, the median eye position was strongly affected by head position, suggesting that the reference of the median eye position is the naso-temporal axis. The authors also provide an elegant discussion of the properties of slow phase eye movements and their stimulus specificity. Of value is the comparison of their data with respect to eye movements occurring during real self-motion and the discussion of the retinal flow fields in the context of an ecological framework. This paper will be of lasting importance in the field.
19. Duffy CJ, Wurtz RH. Optic flow, posture, and the dorsal visual pathway. Ono T, McNaughton BL, Molotchnikoff S, Rolls ET, Nishijo H. Perception, Memory and Emotion: Frontiers in Neuroscience. 1996;63-77 Elsevier Science, Oxford.
20. Maunsell JH, Van Essen DC. Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. J Neurophysiol. 49:1983;1127-1147.
21. Ungerleider LG, Desimone R. Cortical connections of visual area MT in the macaque. J Comp Neurol. 24:1986;190-222.
22. Schaafsma SJ, Duysens J, Gielen CCAM. Responses in ventral intraparietal area of awake macaque monkey to optic flow patterns corresponding to rotation of planes in depth can be explained by translation and expansion effects. Vis Neurosci. 14:1997;633-646 It is well known that MST neurones respond to rotation in depth. As MST projects to the ventral intraparietal area (VIP), these authors questioned whether neurones in VIP also respond to motion in depth. The authors recorded the responses to a fanning stimulus of 161 neurones in area VIP of two awake macaque monkeys, simulating the rotation of a plane in three-dimensional space. This stimulus activated many VIP neurones, suggesting that this area, also, responds to optic flow patterns portraying rotation of planes in depth.
23. of special interest Read HL, Siegel R. Modulation of responses to optic flow in area 7a by retinotopic and oculomotor cues in monkeys. Cereb Cortex. 7:1997;647-661 The paper elegantly demonstrates that neurones in area 7a strongly respond to optic flow and retinotopic stimulus position. The conclusion of the study is that as a result of this multiple selectivity and sensitivity, neurones in area 7a are in a position to provide an appropriate substrate for spatial representation while the animal is moving in its environment.
24. of special interest Andersen RA. Multimodal integration for the representation of space in the posterior parietal cortex. of outstanding interest Philos Trans R Soc Lond [Biol]. 352:1997;1421-1428 The paper concludes that although MSTd is particularly relevant for navigation and underlies the perceptual stability of motion signals, areas LIP and 7a are important for specifying the location of the targets for actions (i.e. reaching or eye movements).
25. Steiner V, Blake R, Rose D. Interocular transfer of expansion, rotation and translation motion aftereffects. Perception. 23:1994;1197-1202.
26. Takeuchi T. Visual search of expansion and contraction. Vision Res. 37:1997;2083-2090 The authors used a visual search paradigm task to examine the perception of radial motion in the human visual system. The time taken to find an expanding target among contracting distractors did not vary with the number of distractors; however, the search time for a contracting target among expanding distractors increased with the number of distractors. These results suggest that expansion and contraction are processed by higher-order units in the visual system that respond asymmetrically to exansion and contraction.
27. of special interest Regan D, Beverley KI. Looming detectors in the human visual pathway. Vision Res. 18:1978;415-421.
28. Regan D. Visual processing of four kinds of relative motion. Vision Res. 26:1986;127-145.
29. Freeman TC, Harris MG. Human sensitivity to expanding and rotating motion: effects of complementary masking and directional structure. Vision Res. 32:1992;81-87.
30. Lappin JS, Norman JF, Mowafy L. The detectability of geometric structure in rapidly changing optical patterns. Perception. 20:1991;513-528.
31. Snowden RJ, Milne AB. The effects of adapting to complex motions: position invariance and tuning to spiral motions. J Cogn Neurosci. 8:1996;412-429.
32. Snowden RJ, Milne AB. Phantom motion aftereffects - evidence of detectors for the analysis of optic flow. of special interest Curr Biol. 7:1997;717-722 The paper presents psychophysical evidence of specialised detectors for the analysis of optical flow patterns in the human visual system. The authors used adapting stimuli containing motion in two non-adjacent quadrants of a circular stimulus aperture, then tested using stimuli with elements in only the other two quadrants. Using a nulling technique, they found that adaptation to the two-quadrant stimuli gave rise to 'phantom' aftereffects in the other two quadrants. For example, adaptation to two segments that contained upwards and downwards motion induced the perception of leftwards and rightwards motion in other parts of the visual field, suggesting that mechanisms sensitive to complex motions were being adapted.
33. Te Pas S, Kappers A, Koenderink JJ. Detection of first-order structure in optic flow fields. Vision Res. 36:1996;259-270.
34. Morrone C, Burr D, Vaina LM. Two stages of visual processing for radial and circular motion. Nature. 376:1995;507-509.
35. Burr DC, Morrone MC, Vaina LM. Large receptive fields for optic flow detection in humans. of outstanding interest Vision Res. 38:1998;1731-1743 This paper provides further support for spatial integration of optic flow field in the human visual system. Further to to their previous study [34], the authors aimed to probe the limits of integration by obtaining an estimate size of the receptive fields of the mechanisms underlying optic flow detection in humans. The extent of the spatial summation observed was between 30° - 70°, suggesting very large receptive fields for circular, translational and radial motion. The size of the receptive fields determined psychophysically in this study is consistent with the receptive field size of MSTd neurones.
36. Beardsley S, Clifford CWG, Vaina LM. Discrimination of shifted centers of motion in complex stimuli [abstract]. Invest Ophthalmol Vis Sci. 39:1998;S621.
37. Watamaniuk SNJ, Sekuler R. Temporal and spatial integration in dynamic random-dot stimuli. Vision Res. 32:1992;2341-2347.
38. Smith AT, Snowden RJ, Milne AB. Is global motion really based on spatial integration of local motion signals? Vision Res. 34:1994;2425-2430.
39. Ohtani Y, Tanigawa M, Ejima Y. Motion assimilation for expansion/contraction and rotation and its spatial properties. of special interest Vision Res. 38:1998;429-438 This study demonstrates the existence and spatial limits of motion assimilation for complex motion stimuli. Motion was induced in a test grating by the presence of three other gratings that moved in a manner consistent with a single complex motion. Motion assimilation was found to extend beyond the limit of spatial summation to 14°-21° (of visual angle), suggesting that the perceived motion of the test grating was attributable to the interaction of local and global motion detectors.
40. Geesaman BJ, Qian N. A novel speed illusion involving expansion and rotation patterns. Vision Res. 36:1996;3281-3292.
41. Geesaman BJ, Qian N. The effect of complex motion pattern on speed perception. Vision Res. 38:1998;1223-1231.
42. Sekuler AB. Simple-pooling of unidirectional motion predicts speed discrimination for looming stimuli. Vision Res. 32:1992;2277-2288.
43. Verghese P, Stone L. Spatial layout effects speed discrimination. Vision Res. 37:1997;397-406.
44. Verghese P, Stone L. Combining speed information across space. Vision Res. 35:1995;2811-2824.
45. Verghese P, Stone L. Perceived visual speed constrained by image segmentation. Nature. 381:1996;161-163.
46. Bex PJ, Makous W. Radial motion looks faster. of special interest Vision Res. 37:1997;3399-3405 To investigate the perception of speed in complex motion patterns, the authors compared the perceived speed of radial and vertical gratings. They found that the speed of radial gratings was consistently overestimated by 20-60% relative to translational gratings. They speculate that the greater apparent speed of radial motion is related to the apparent motion-in-depth of expanding and contracting patterns.
47. Warren WH, Hannon DJ. Direction of self-motion is perceived from optical flow. Nature. 336:1988;162-163.
48. Warren W, Morris M, Kalish M. Perception of translational heading from optical flow. J Exp Psychol [Hum Percept Perform]. 14:1988;646-660.
49. Crowell JA, Royden CS, Banks MS, Swenson KH, Sekuler AB. Optic flow and heading judgements [abstract]. Invest Ophthalmol Vis Sci. 31:1990;2564.
50. Crowell JA, Banks MS. Perceiving heading with different retinal regions and types of optic flow. Percept Psychophys. 53:1993;325-337.
51. Warren W, Blackwell A, Kurtz K, Hatsopoulos N, Kalish M. On the sufficiency of the velocity field for perception of heading. Biol Cybern. 65:1991;311-320.
52. Van den Berg AV. Robustness of perception of heading from optic flow. Vision Res. 32:1992;1285-1296.
53. Warren WH, Hannon DJ. Eye movements and optical flow. J Opt Soc Am. 7:1989;160-169.
54. Warren WH, Mestre DR, Blackwell AW, Morris MW. Perception of circular heading from optical flow. J Exp Psychol [Hum Percept Perform]. 17:1991;28-43.
55. Royden CS, Banks MS, Crowell JA. The perception of heading during eye movements. Nature. 360:1992;583-585.
56. Royden CS, Crowell JA, Banks MS. Estimating heading during eye movements. Vision Res. 34:1994;3197-3214.
57. Van den Berg AV, Brenner E. Humans combine the optic flow with static depth cues for robust perception of heading. Vision Res. 34:1994;2153-2168.
58. Busettini C, Masson GS, Miles FA. Radial optic flow induces vergence eye movements with ultra-short latencies. of special interest Nature. 390:1997;512-515 This psychophysical study demonstrated that forward motion, encoded by centrifugal flow (expansion), increases the angle of the vergence eye movements, whereas the centripetal flow (contraction) decreases it. Because such vergence eye movements are present when the observers are viewing motion display in the temporal field of one eye, it means that these responses do not result from anisotropies in motion processing, but from a mechanism sensitive to the radial pattern of optic flow. The authors suggest that flow-induced vergence eye movements is an ocular reflex that compensates for the translational disturbance of the observer and is mediated by the superior temporal cortex.
59. Royden C, Hildreth E. Human heading judgments in the presence of moving objects. Percept Psychophys. 58:1996;836-856.
60. Warren WH, Saunders JA. Perceiving heading in the presence of moving objects. Perception. 24:1995;315-331.
61. Warren W, Kurtz K. The role of central and peripheral vision in perceiving the direction of self-motion. Percept Psychophys. 51:1992;443-454.
62. Jornales V, Jakav M, Barton JS, Vaina LM. Deficits on complex motion perception, spatial discrimination and eye-movements in a patient with bilateral occipital-parietal lesions [abstract]. Invest Ophthalmol Vis Sci. 38:1997;S72.
63. Zihl J, Baker CL, Hess RH. The 'motion-blind' patient: low-level spatial and temporal filters. J Neurosci. 9:1989;1628-1640.
64. Vaina LM. Functional segregation of color motion processing in the human visual cortex: clinical evidence. Cereb Cortex. 4:1994;555-572.
65. Vaina LM, LeMay M, Bienfang DC, Choi AY, Nakayama K. Intact 'biological motion' and 'structure from motion' perception in a patient with impaired motion mechanisms: a case study. Vis Neurosci. 5:1990;353-369.
66. McLeod P, Dittrich W, Driver J, Perret D, Zihl J. Preserved and impaired detection of structure from motion by a 'motion blind' patient. Vis Cogn. 3:1996;363-391.
67. Vaina LM, Stratton NA, LeMay M, Lessell IM. Selective motion and depth deficits in the right visual field of a patient with a focal left occipital-parietal lesion [abstract]. Invest Ophthalmol Vis Sci. 32:1991;776.
68. Vaina LM, Grzywacz NM, Kikinis R. Segregation of computation underlying perception of motion discontinuity and coherence. Neuroreport. 5:1994;2289-2294.
69. Newsome WT, Pare EB. A selective impairment of motion perception following lesions of the middle temporal visual area (MT). J Neurosci. 8:1988;2201-2211.
70. Vaina LM, Grzywacz NM, Jolesz F, Kikinis R, Jakab M, Bienfang DC. Selective deficits of motion integration and segregation mechanisms with unilateral extrastriate brain lesions. Neuroimage. 1998;. in press.
71. Vaina LM, Royden C, Bienfang DC, Kennedy D. Normal perception of heading in a patient with impaired structure-from-motion. Neuroreport. 1998;. in press.
72. Haarmeier T, Their P, Repnow M, Petersen D. False perception of motion in a patient who cannot compensate for eye movements. Nature. 389:1997;849-852.
73. Newsome WT, Wurtz RH, Komatsu H. Relation of cortical areas MT and MST to a pursuit eye movements. II. Differentiation of retinal from extraretinal inputs. J Neurophysiol. 60:1988;604-620.
74. Assad JA, Maunsell JHR. Neuronal correlates of inferred motion in primate parietal cortex. Nature. 373:1995;518-521.
75. Colby CL, Duhamel J-R, Goldberg ME. The analysis of visual space by the lateral intraparietal area of the monkey: the role of extraretinal signals. Hicks TP, Molotchnikof S, Ono T. Progress in Brain Research. 95:1993;307-316 Elsevier Science, Amsterdam.