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Normal development of pattern motion sensitivity in macaque monkeys

Published online by Cambridge University Press:  01 September 2008

CYNTHIA HALL-HARO  and
LYNNE KIORPES
CYNTHIA HALL-HARO
Affiliation:
Center for Neural Science, New York University, New York
LYNNE KIORPES*
Affiliation:
Center for Neural Science, New York University, New York
*
*Address correspondence to: Dr. Lynne Kiorpes, Center for Neural Science, New York University, 4 Washington Pl. Room 809, New York, NY 10012. E-mail: [email protected]
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Abstract

We studied the development of sensitivity to complex motion using plaid patterns. We hypothesized, based on neurophysiological data showing a dearth of pattern direction–selective (PDS) cells in area medial temporal (MT) of infant macaques, that sensitivity to pattern motion would develop later than other forms of global motion sensitivity. We tested 10 macaque monkeys (Macaca nemestrina) ranging in age from 7 weeks to 109–160 weeks (adult). The monkeys discriminated horizontal from vertical pattern motion; sensitivity for one-dimensional (1D) direction discrimination and detection were tested as control tasks. The results show that pattern motion discrimination ability develops relatively late, between 10 and 18 weeks, while performance on the 1D control tasks was excellent at the earliest test ages. Plaid discrimination performance depends on both the speed and spatial scale of the underlying patterns. However, development is not limited by contrast sensitivity. These results support the idea that pattern motion perception depends on a different mechanism than other forms of global motion perception and are consistent with the idea that the representation of PDS neurons in MT may limit the development of complex motion perception.

Keywords

Pattern motionPlaidVisual developmentMonkeyMT
Type
Research Articles
Information
Visual Neuroscience , Volume 25 , Issue 5-6 , September 2008 , pp. 675 - 684
Copyright
Copyright © Cambridge University Press 2008

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References

Adelson, E.H. & Movshon, J.A. (1982). Phenomenal coherence of moving visual patterns. Nature 300, 523–525.CrossRefGoogle ScholarPubMed
Atkinson, J. (2000). The Developing Visual Brain. Oxford: Oxford University Press.Google Scholar
Banton, T. & Bertenthal, B.I. (1997). Multiple developmental pathways for motion processing. Optometry and Vision Science 74, 751–760.CrossRefGoogle ScholarPubMed
Banton, T., Dobkins, K. & Bertenthal, B.I. (2001). Infant direction discrimination thresholds. Vision Research 41, 1049–1056.CrossRefGoogle ScholarPubMed
Boothe, R.G., Dobson, V. & Teller, D.Y. (1985). Postnatal development of vision in human and nonhuman primates. Annual Review of Neuroscience 8, 495–545.CrossRefGoogle ScholarPubMed
Boothe, R.G., Kiorpes, L., Williams, R.A. & Teller, D.Y. (1988). Operant measurements of contrast sensitivity in infant macaque monkeys during normal development. Vision Research 28, 387–396.CrossRefGoogle ScholarPubMed
Braddick, O., Atkinson, J. & Wattam-Bell, J. (2003). Normal and anomalous development of visual motion processing: Motion coherence and ‘dorsal stream vulnerability’. Neuropsychologia 41, 1769–1784.CrossRefGoogle ScholarPubMed
Britten, K.H., Newsome, W.T., Shadlen, M.N., Celebrini, S. & Movshon, J.A. (1996). A relationship between behavioral choice and the visual responses of neurons in macaque MT. Visual Neuroscience 13, 87–100.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle Scholar
Delicato, L.S. & Derrington, A.M. (2005). Coherent motion perception fails at low contrast. Vision Research 45, 2310–2320.CrossRefGoogle ScholarPubMed
Distler, C., Bachevalier, J., Kennedy, C., Mishkin, M. & Ungerleider, L.G. (1996). Functional development of the corticocortical pathway for motion analysis in the macaque monkey: A 14C-2-deoxyglucose study. Cerebral Cortex 6, 184–195.CrossRefGoogle ScholarPubMed
Distler, C. & Hoffmann, K.-P. (2003). Development of the optokinetic response in macaques: A comparison with cat and man. Annals of the New York Academy of Sciences 1004, 10–18.CrossRefGoogle ScholarPubMed
Distler, C., Vital-Durand, F., Korte, R., Korbmacher, H. & Hoffmann, K.-P. (1999). Development of the optokinetic system in macaque monkeys. Vision Research 39, 3909–3919.CrossRefGoogle ScholarPubMed
Dobkins, K.R., Fine, I., Hsueh, A.C. & Vitten, C. (2004). Pattern motion integration in infants. Journal of Vision 4, 144–155.CrossRefGoogle ScholarPubMed
Ellemberg, D., Lewis, T.L., Dirks, M., Maurer, D., Ledgeway, T., Guillemot, J.P. & Lepore, F. (2004). Putting order into the development of sensitivity to global motion. Vision Research 44, 2403–2411.CrossRefGoogle ScholarPubMed
Ellemberg, D., Lewis, T.L., Liu, C.H. & Maurer, D. (1999). Development of spatial and temporal vision during childhood. Vision Research 39, 2325–2333.CrossRefGoogle ScholarPubMed
Finney, D.J. (1971). Probit Analysis. New York: Cambridge University Press.Google Scholar
Hall, C. (2008). Normal Development of Perceptual and Cognitive Functions in the Macaque Monkey. PhD Dissertation. New York University.Google Scholar
Hall-Haro, C., Johnson, S.P., Price, T.A., Vance, J.A. & Kiorpes, L. (2008). Development of object concepts in macaque monkeys. Developmental Psychobiology 50, 278–287.CrossRefGoogle ScholarPubMed
Huk, A.C. & Heeger, D.J. (2002). Pattern-motion responses in human visual cortex. Nature Neuroscience 5, 72–75.CrossRefGoogle ScholarPubMed
Kiorpes, L. (1992). Development of vernier acuity and grating acuity in normally reared monkeys. Visual Neuroscience 9, 243–251.CrossRefGoogle ScholarPubMed
Kiorpes, L. & Bassin, S.A. (2003). Development of contour integration in macaque monkeys. Visual Neuroscience 20, 567–575.CrossRefGoogle ScholarPubMed
Kiorpes, L. & Kiper, D.C. (1996). Development of contrast sensitivity across the visual field in macaque monkeys (Macaca nemestrina). Vision Research 36, 239–247.CrossRefGoogle ScholarPubMed
Kiorpes, L., Kohn, A., Hawken, M.J., Rust, N.C. & Movshon, J.A. (2007). What does MT contribute to the development of sensitivity to visual motion? Perception 36S (ECVP Abstract).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.CrossRefGoogle ScholarPubMed
Kiorpes, L. & Movshon, J.A. (2004 a). Neural limitations on visual development in primates. In The Visual Neurosciences, ed. Chalupa, L.M. & Werner, J.S., pp. 159–173. Cambridge, MA: MIT Press.Google Scholar
Kiorpes, L. & Movshon, J.A. (2004 b). Development of sensitivity to visual motion in macaque monkeys. Visual Neuroscience 21, 851–859.CrossRefGoogle ScholarPubMed
Kovacs, I. (2000). Human development of perceptual organization. Vision Research 40, 1301–1310.CrossRefGoogle ScholarPubMed
Kovacs, I., Kozma, P., Feher, A. & Benedek, G. (1999). Late maturation of visual spatial integration in humans. Proceedings of the National Academy of Sciences U S A 96, 12204–12209.CrossRefGoogle ScholarPubMed
Lewis, T.L., Ellemberg, D., Maurer, D., Dirks, M., Wilkinson, F. & Wilson, H.R. (2004). A window on the normal development of sensitivity to global form in Glass patterns. Perception 33, 409–418.CrossRefGoogle ScholarPubMed
Manny, R.E. & Fern, K.D. (1990). Motion coherence in infants. Vision Research 30, 1319–1329.CrossRefGoogle ScholarPubMed
Mason, A.J., 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.CrossRefGoogle ScholarPubMed
Mikami, A. & Fujita, K. (1992). Development of the ability to detect visual motion in infant macaque monkeys. Developmental Psychobiology 25, 345–354.CrossRefGoogle ScholarPubMed
Movshon, J.A., Adelson, E.H., Gizzi, M.S. & Newsome, W.T. (1985). The analysis of moving visual patterns. In Pattern Recognition Mechanisms, ed.Chagas, C., Gattass, R. & Gross, C., pp. 117–151. Rome, Italy: Vatican Press.CrossRefGoogle Scholar
Movshon, J.A., Rust, N.C., Kohn, A., Kiorpes, L. & Hawken, M.J. (2004). Receptive field properties of MT neurons in infant macaques. Perception 33S (ECVP Abstract).Google Scholar
Newsome, W.T., Britten, K.H. & Movshon, J.A. (1989). Neuronal correlates of a perceptual decision. Nature 341, 52–54.CrossRefGoogle ScholarPubMed
Newsome, W.T. & Paré, E.B. (1988). A selective impairment of motion perception following lesions of the middle temporal visual area (MT). Journal of Neuroscience 8, 2201–2211.CrossRefGoogle ScholarPubMed
Parrish, E.E., Giaschi, D.E., Boden, C. & Dougherty, R. (2005). The maturation of form and motion perception in school age children. Vision Research 45, 827–837.CrossRefGoogle ScholarPubMed
Rodman, H.R. & Albright, T.D. (1989). Single-unit analysis of pattern-motion selective properties in the middle temporal visual area (MT). Experimental Brain Research 75, 53–64.CrossRefGoogle ScholarPubMed
Salzman, C.D., Britten, K.H. & Newsome, W.T. (1990). Cortical microstimulation influences perceptual judgments of motion direction. Nature 346, 174–177.CrossRefGoogle Scholar
Stavros, K.A. & Kiorpes, L. (2008). Behavioral measurement of temporal contrast sensitivity development in macaque monkeys (Macaca nemestrina). Vision Research 48, 1335–1344.CrossRefGoogle ScholarPubMed
Stoner, G.R. & Albright, T.D. (1992). Neural correlates of perceptual motion coherence. Nature 358, 412–414.CrossRefGoogle ScholarPubMed
Teller, D.Y. (1997). First glances: The vision of infants. The Friedenwald lecture. Investigative Ophthalmology and Visual Science 38, 2183–2203.Google ScholarPubMed
Teller, D.Y. & Boothe, R.G. (1979). Development of vision in infant primates. Transactions of the Ophthalmological Society of the UK 99, 333–337.Google ScholarPubMed
Wattam-Bell, J. (1994). Coherence thresholds for discrimination of motion direction in infants. Vision Research 34, 877–883.CrossRefGoogle ScholarPubMed
Wattam-Bell, J. (1996 a). Visual motion processing in one-month-old infants: Habituation experiments. Vision Research 36, 1679–1685.CrossRefGoogle ScholarPubMed
Wattam-Bell, J. (1996 b). Visual motion processing in one-month-old infants: Preferential looking experiments. Vision Research 36, 1671–1677.CrossRefGoogle ScholarPubMed