Abstract
Perception of depth is a fundamental challenge for the visual system, particularly for observers moving through their environment. The brain makes use of multiple visual cues to reconstruct the three-dimensional structure of a scene. One potent cue, motion parallax, frequently arises during translation of the observer because the images of objects at different distances move across the retina with different velocities. Human psychophysical studies have demonstrated that motion parallax can be a powerful depth cue1,2,3,4,5, and motion parallax seems to be heavily exploited by animal species that lack highly developed binocular vision6,7,8. However, little is known about the neural mechanisms that underlie this capacity. Here we show, by using a virtual-reality system to translate macaque monkeys (Macaca mulatta) while they viewed motion parallax displays that simulated objects at different depths, that many neurons in the middle temporal area (area MT) signal the sign of depth (near versus far) from motion parallax in the absence of other depth cues. To achieve this, neurons must combine visual motion with extra-retinal (non-visual) signals related to the animal’s movement. Our findings suggest a new neural substrate for depth perception and demonstrate a robust interaction of visual and non-visual cues in area MT. Combined with previous studies that implicate area MT in depth perception based on binocular disparities9,10,11,12, our results suggest that area MT contains a more general representation of three-dimensional space that makes use of multiple cues.
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Scene-relative object motion biases depth percepts
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References
Rogers, B. & Graham, M. Motion parallax as an independent cue for depth perception. Perception 8, 125–134 (1979)
Rogers, B. J. Motion parallax and other dynamic cues for depth in humans. Rev. Oculomot. Res. 5, 119–137 (1993)
Rogers, B. J. & Collett, T. S. The appearance of surfaces specified by motion parallax and binocular disparity. Q. J. Exp. Psychol. A 41, 697–717 (1989)
Rogers, B. J. & Graham, M. E. Similarities between motion parallax and stereopsis in human depth perception. Vision Res. 22, 261–270 (1982)
Bradshaw, M. F. & Rogers, B. J. The interaction of binocular disparity and motion parallax in the computation of depth. Vision Res. 36, 3457–3468 (1996)
Ellard, C. G., Goodale, M. A. & Timney, B. Distance estimation in the Mongolian gerbil: the role of dynamic depth cues. Behav. Brain Res. 14, 29–39 (1984)
van der Willigen, R. F., Frost, B. J. & Wagner, H. Depth generalization from stereo to motion parallax in the owl. J. Comp. Physiol. A 187, 997–1007 (2002)
Kral, K. Behavioural–analytical studies of the role of head movements in depth perception in insects, birds and mammals. Behav. Processes 64, 1–12 (2003)
DeAngelis, G. C., Cumming, B. G. & Newsome, W. T. Cortical area MT and the perception of stereoscopic depth. Nature 394, 677–680 (1998)
Uka, T. & DeAngelis, G. C. Contribution of middle temporal area to coarse depth discrimination: comparison of neuronal and psychophysical sensitivity. J. Neurosci. 23, 3515–3530 (2003)
Uka, T. & DeAngelis, G. C. Linking neural representation to function in stereoscopic depth perception: roles of the middle temporal area in coarse versus fine disparity discrimination. J. Neurosci. 26, 6791–6802 (2006)
Uka, T. & DeAngelis, G. C. Contribution of area MT to stereoscopic depth perception: choice-related response modulations reflect task strategy. Neuron 42, 297–310 (2004)
Farber, J. M. & McConkie, A. B. Optical motions as information for unsigned depth. J. Exp. Psychol. Hum. Percept. Perform. 5, 494–500 (1979)
Rogers, S. & Rogers, B. J. Visual and nonvisual information disambiguate surfaces specified by motion parallax. Percept. Psychophys. 52, 446–452 (1992)
Nawrot, M. Eye movements provide the extra-retinal signal required for the perception of depth from motion parallax. Vision Res. 43, 1553–1562 (2003a)
DeAngelis, G. C. & Uka, T. Coding of horizontal disparity and velocity by MT neurons in the alert macaque. J. Neurophysiol. 89, 1094–1111 (2003)
Maunsell, J. H. & Van Essen, D. C. Functional properties of neurons in middle temporal visual area of the macaque monkey. II. Binocular interactions and sensitivity to binocular disparity. J. Neurophysiol. 49, 1148–1167 (1983b)
Maunsell, J. H. & Van Essen, D. C. Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. J. Neurophysiol. 49, 1127–1147 (1983a)
Nover, H., Anderson, C. H. & DeAngelis, G. C. A logarithmic, scale-invariant representation of speed in macaque middle temporal area accounts for speed discriminiation performance. J. Neurosci. 25, 10049–10060 (2005)
Born, R. T. & Bradley, D. C. Structure and function of visual area MT. Annu. Rev. Neurosci. 28, 157–189 (2005)
Bradley, D. C., Qian, N. & Andersen, R. A. Integration of motion and stereopsis in middle temporal cortical area of macaques. Nature 373, 609–611 (1995)
Bradley, D. C., Chang, G. C. & Andersen, R. A. Encoding of three-dimensional structure-from-motion by primate area MT neurons. Nature 392, 714–717 (1998)
Dodd, J. V., Krug, K., Cumming, B. G. & Parker, A. J. Perceptually bistable three-dimensional figures evoke high choice probabilities in cortical area MT. J. Neurosci. 21, 4809–4821 (2001)
Cao, A. & Schiller, P. H. Neural responses to relative speed in the primary visual cortex of rhesus monkey. Vis. Neurosci. 20, 77–84 (2003)
Newsome, W. T., Wurtz, R. H. & Komatsu, H. Relation of cortical areas MT and MST to pursuit eye movements. II. Differentiation of retinal from extraretinal inputs. J. Neurophysiol. 60, 604–620 (1988)
Bremmer, F., Ilg, U. J., Thiele, A., Distler, C. & Hoffmann, K. P. Eye position effects in monkey cortex. I. Visual and pursuit-related activity in extrastriate areas MT and MST. J. Neurophysiol. 77, 944–961 (1997)
Nawrot, M. & Joyce, L. The pursuit theory of motion parallax. Vision Res. 46, 4709–4725 (2006)
Gu, Y., Watkins, P. V., Angelaki, D. E. & DeAngelis, G. C. Visual and nonvisual contributions to three-dimensional heading selectivity in the medial superior temporal area. J. Neurosci. 26, 73–85 (2006)
Gu, Y., DeAngelis, G. C. & Angelaki, D. E. A functional link between area MSTd and heading perception based on vestibular signals. Nature Neurosci. 10, 1038–1047 (2007)
Nguyenkim, J. D. & DeAngelis, G. C. Disparity-based coding of three-dimensional surface orientation by macaque middle temporal neurons. J. Neurosci. 23, 7117–7128 (2003)
Acknowledgements
We thank L. Snyder, A. Anzai, T. Sanada, Y. Gu and C. Fetsch for comments; C. Broussard for technical development; and A. Turner, E. White and K. Kocher for care and training of monkeys. This work was supported by a National Eye Institute (NEI) institutional National Research Service Award (to J.W.N.) and NEI grants to G.C.D. and D.E.A.
Author Contributions J.W.N. and G.C.D. designed the stimuli; J.W.N. collected the data; J.W.N., D.E.A. and G.C.D. refined the analysis and presentation of the data; J.W.N., D.E.A. and G.C.D. wrote the paper.
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Nadler, J., Angelaki, D. & DeAngelis, G. A neural representation of depth from motion parallax in macaque visual cortex. Nature 452, 642–645 (2008). https://doi.org/10.1038/nature06814
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DOI: https://doi.org/10.1038/nature06814
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