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Development of sensitivity to visual motion in macaque monkeys

Published online by Cambridge University Press:  25 February 2005

LYNNE KIORPES  and
J. ANTHONY MOVSHON
LYNNE KIORPES
Affiliation:
Center for Neural Science, New York University, New York
J. ANTHONY MOVSHON
Affiliation:
Center for Neural Science, New York University, New York
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Abstract

The development of spatial vision is relatively well documented in human and nonhuman primates. However, little is known about the development of sensitivity to motion. We measured the development of sensitivity to direction of motion, and the relationship between motion and contrast sensitivity in macaque monkeys as a function of age. Monkeys (Macaca nemestrina, aged between 10 days and 3 years) discriminated direction of motion in random-dot kinematograms. The youngest monkeys showed directionally selective orienting and the ability to integrate motion signals at large dot displacements and fast speeds. With age, coherence sensitivity improved for all spatial and temporal dot displacements tested. The temporal interval between the dots was far less important than the spatial offset in determining the animals' performance at all but the youngest ages. Motion sensitivity improved well beyond the end of the first postnatal year, when mid-spatial-frequency contrast sensitivity reached asymptote, and continued for at least 3 years. Sensitivity to contrast at high spatial frequencies also continued to develop beyond the end of the first year. We conclude that the development of motion sensitivity depends on mechanisms beyond the low-level filters presumed to limit acuity and contrast sensitivity, and most likely reflects the function of extrastriate visual areas.

Keywords

Visual developmentVisual motionContrast sensitivity
Type
Research Article
Information
Visual Neuroscience , Volume 21 , Issue 6 , November 2004 , pp. 851 - 859
Copyright
© 2004 Cambridge University Press

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References

REFERENCES

Aslin, R.N. & Shea, S.L. (1990). Velocity thresholds in human infants—implications for the perception of motion. Developmental Psychology 2, 589–598.Google Scholar
Atkinson, J. (1979). Development of optokinetic nystagmus in the human infant and monkey infant: An analogue to development in kittens. In NATO Advanced Study Institute Series, Developmental Neurobiology of Vision, ed. Freeman, R.D., pp. 277–287. New York: Plenum Press.
Baker, C.L. & Braddick, O. (1985). Temporal properties of the short-range process in apparent motion. Perception 14, 181–192.Google Scholar
Banton, T., Dobkins, K., & Bertenthal, B.I. (2001). Infant direction discrimination thresholds. Vision Research 41, 1049–1056.Google Scholar
Birch, E.E., Gwiazda, J., Bauer, J.A., Naegele, J., & Held, R. (1983). Visual acuity and its meridional variations in children aged 7–60 months. Vision Research 23, 1019–1024.Google Scholar
Boothe, R.G., Kiorpes, L., Williams, R.A., & Teller, D.Y. (1988). Operant measurements of spatial contrast sensitivity in infant macaque monkeys during development. Vision Research 28, 387–396.Google Scholar
Braddick, O. (1993). Orientation and motion-selective mechanisms in infants. In Early Visual Development: Basic and Clinical Research, ed. Simons, K., pp. 163–177. New York: Oxford University Press.
Braddick, O., Atkinson, J., & Wattam-Bell, J. (2003). Normal and anomalous development of visual Motion processing: motion coherence and ‘dorsal-stream vulnerability’. Neuropsycologia 41, 1769–1784.Google Scholar
Bradley, A. & Freeman, R.D. (1982). Contrast sensitivity in children. Vision Research 22, 953–959.Google Scholar
Britten, K.H., Shadlen, M.N., Newsome, W.T., & Movshon, J.A. (1992). The analysis of visual motion: A comparison of neuronal and psychophysical performance. Journal of Neuroscience 12, 4745–4765.Google Scholar
Celebrini, S. & Newsome, W.T. (1995). Microstimulation of extrastriate area MST influences performance on a direction discrimination task. Journal of Neurophysiology 73, 437–448.Google Scholar
Chino, Y.M., Smith, E.L., III, Hatta, S., & Cheng, H. (1997). Postnatal development of binocular disparity sensitivity in neurons of the primate visual cortex. Journal of Neuroscience 17, 296–307.Google Scholar
Daw, N.W. (1998). Critical periods and amblyopia. Archives of Ophthalmology 116, 502–505.Google Scholar
Dobkins, K.R. & Teller, D.Y. (1996). Infant motion:detection (M:D) ratios for chromatically defined and luminance-defined moving stimuli. Vision Research 36, 3293–3310.Google Scholar
Dobkins, K.R., Anderson, C.M., & Lia, B. (1999). Infant temporal contrast sensitivity functions (tCSFs) mature earlier for luminance than for chromatic stimuli: Evidence for precocious magnocellular development? Vision Research 39, 3223–3239.Google Scholar
Ellemberg, D., Lewis, T.L., Liu, C.H., & Maurer, D. (1999). Development of spatial and temporal vision during childhood. Vision Research 39, 2325–2333.Google Scholar
Finlay, D.C., Chorlton, M.C., & Boulton, J.C. (1991). Motion thresholds in infants to sinusoidal gratings. Journal of General Psychology 118, 263–270.Google Scholar
Finney, D.J. (1971). Probit Analysis. New York: Cambridge University Press.
Giaschi, D. & Regan, D. (1997). Development of motion-defined figure-ground segregation in preschool and older children, using a letter-identification task. Optometry and Vision Science 74, 761–767.Google Scholar
Gunn, A., Cory, E., Atkinson, J., Braddick, O., Wattam-Bell, J., Guzzetta, A., & Cioni, G. (2002). Dorsal and ventral stream sensitivity in normal development and hemiplegia. NeuroReport 13, 843–847.Google Scholar
Hainline, L. & Abramov, I. (1997). Development of spatial contrast sensitivity from infancy to adulthood: Psychophysical data. Optometry and Vision Science 74, 785–789.Google Scholar
Hamer, R.D. & Norcia, A.M. (1994). The development of motion sensitivity during the first year of life. Vision Research 34, 2387–2402.Google Scholar
Hartmann, E.E. & Banks, M.S. (1992). Temporal contrast sensitivity in human infants. Vision Research 32, 1163–1168.Google Scholar
Harwerth, R.S., Smith, E.L., III, Duncan, G.C., Crawford, M.L., & von Noorden, G.K. (1986). Multiple sensitive periods in the development of the primate visual system. Science 232, 235–238.Google Scholar
Kiorpes, L. (1992). Development of vernier acuity and grating acuity in normally reared monkeys. Visual Neuroscience 9, 243–251.Google Scholar
Kiorpes, L. & Kiper, D.C. (1996). Development of contrast sensitivity across the visual field in macaque monkeys (Macaca nemestrina). Vision Research 36, 239–247.Google Scholar
Kiorpes, L. & Movshon, J.A. (1998). Peripheral and central factors limiting the development of contrast sensitivity in macaque monkeys. Vision Research 38, 61–70.Google Scholar
Kiorpes, L. & Movshon, J.A. (2003). Neural limitations on visual development in primates. In The Visual Neurosciences, ed. Chalupa, L.M. & Werner, J.S., pp. 159–173. Cambridge, Massachusetts: MIT Press.
Kiorpes, L. & Bassin, S.A. (2003). Development of contour integration in macaque monkeys. Visual Neuroscience 20, 567–575.Google Scholar
Kiorpes, L., Kiper, D.C., & Movshon, J.A. (1993). Contrast sensitivity and vernier acuity in amblyopic monkeys. Vision Research 33, 2301–2311.Google Scholar
Kovács, I., Kozma, P., Fehér, Á., & Benedek, G. (1999). Late maturation of visual spatial integration in humans. Proceedings of the National Academy of Sciences of the U.S.A. 96, 12204–12209.Google Scholar
Kozma, P. & Kiorpes, L. (2003). Contour integration in amblyopic monkeys. Visual Neuroscience 20, 577–588.Google Scholar
Mason, A.J.S., Braddick, O.J., & Wattam-Bell, J. (2003). Motion coherence thresholds in infants—different tasks identify at least two distinct motion systems. Vision Research 43, 1149–1157.Google Scholar
Mayer, D.L. & Dobson, V. (1982). Visual acuity development in infants and young children as assessed by operant preferential looking. Vision Research 22, 1141–1151.Google Scholar
Mikami, A. & Fujita, K. (1992). Development of the ability to detect visual motion in infant macaque monkeys. Developmental Psychobiology 25, 345–354.Google Scholar
Morgan, M.J. & Ward, R. (1980). Conditions for motion flow in dynamic visual noise. Vision Research 20, 431–435.Google Scholar
Movshon, J.A. & Kiorpes, L. (1988). Analysis of the development of spatial contrast sensitivity in monkey and human infants. Journal of the Optical Society of America A 5, 2166–2172.Google Scholar
Movshon, J.A., Kiorpes, L., Cavanaugh, J.R., & Hawken, M.J. (1999). Receptive field properties and surround interactions in V1 neurons in infant macaque monkeys. Society for Neuroscience Abstracts 25, 1048.Google Scholar
Movshon, J.A., Rust, N.C., Kohn, A., Kiorpes, L., & Hawken, M.J. (2003). Receptive-field properties of MT neurons in infant macaques. Society for Neuroscience Abstracts 126. 8.Google Scholar
Naegele, J.R. & Held, R. (1982). The postnatal development of monocular optokinetic nystagmus in infants. Vision Research 22, 341–346.Google Scholar
Neu, B. & Sireteanu, R. (1997). Monocular acuity in preschool children: Assessment with the Teller and Keeler acuity cards in comparison to the C-test. Strabismus 5, 185–201.Google Scholar
Newsome, W.T. & Pare, E.B. (1988). A selective impairment of motion perception following lesions of the middle temporal visual area (MT). Journal of Neuroscience 8, 2201–2211.Google Scholar
Pennefather, P.M., Chandna, A., Kovacs, I., Polat, U., & Norcia, A.M. (1999). Contour detection threshold: Repeatability and learning with ‘contour cards’. Spatial Vision 12, 257–266.Google Scholar
Rasengane, T.A., Allen, D., & Manny, R.E. (1997). Development of temporal contrast sensitivity in human infants. Vision Research 37, 1747–1754.Google Scholar
Regal, D.M. (1981). Development of critical flicker fusion frequency in human infants. Vision Research 21, 549–555.Google Scholar
Roessler, J.S. & Dannemiller, J.L. (1997). Changes in human infants' sensitivity to slow displacements over the first 6 months. Vision Research 37, 417–423.Google Scholar
Smith, M.A., Bair, W., & Movshon, J.A. (2002). Signals in macaque striate cortical neurons that support the perception of glass patterns. Journal of Neuroscience 22, 8334–8345.Google Scholar
Swanson, W.H. & Birch, E.E. (1990). Infant spatiotemporal vision: Dependence of spatial contrast sensitivity on temporal frequency. Vision Research 30, 1033–1048.Google Scholar
Teller, D.Y., Lindsey, D.T., Mar, C.M., Succop, A., & Mahal, M.R. (1992). Infant temporal contrast sensitivity at low temporal frequencies. Vision Research 32, 1157–1162.Google Scholar
Volkman, F.C. & Dobson, M.V. (1976). Infant responses of ocular fixation to moving visual stimuli. Journal of Experimental Child Psychology 22, 86–99.Google Scholar
Wattam-Bell, J. (1991). Development of motion-specific cortical responses in infancy. Vision Research 31, 287–297.Google Scholar
Wattam-Bell, J. (1992). Development of maximum displacement limits for discrimination of motion direction in infancy. Vision Research 32, 621–630.Google Scholar
Wattam-Bell, J. (1994). Coherence thresholds for discrimination of motion direction in infants. Vision Research 34, 887–883.Google Scholar
Wattam-Bell, J. (1996). Development of visual motion processing. In Infant Vision, ed. Vital-Durand, F., Atkinson, J. & Braddick, O., pp. 79–94. Oxford: Oxford University Press.
Wilson, H.R. & Bergen, J.R. (1979). A four mechanism model for threshold spatial vision. Vision Research 19, 19–32.Google Scholar