Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-27T16:45:15.908Z Has data issue: false hasContentIssue false
  • English
  • Français

Development of contour integration in macaque monkeys

Published online by Cambridge University Press:  22 January 2004

LYNNE KIORPES  and
SARAH A. BASSIN
LYNNE KIORPES
Affiliation:
Center for Neural Science, New York University, New York
SARAH A. BASSIN
Affiliation:
Center for Neural Science, New York University, New York
Get access Rights & Permissions [Opens in a new window]

Abstract

Studies of visual development show that basic metrics of visual development such as spatial resolution develop over the first 6–9 months in monkeys and over the first 6 or so years in humans. However, more complex visual functions may develop over different, or more protracted, time courses. To address the question of whether global perceptual processing is linked to or otherwise dependent on the development of basic spatial vision, we studied the development of contour integration, a global perceptual task, in comparison to that of grating acuity in macaque monkeys. We find that contour integration develops substantially later than acuity. Contour integration begins to develop at 5–6 months, near the time that acuity development is complete and continues to mature well into the second postnatal year. We discuss this later development in terms poor central efficiency and consider the relevant anatomy and physiology of the developing visual system. We conclude that contour integration is not likely to be limited by the same mechanisms that are permissive to acuity development, and may instead reflect the emergence of function central to V1.

Keywords

Visual developmentContour integrationMonkey
Type
Research Article
Information
Visual Neuroscience , Volume 20 , Issue 5 , September 2003 , pp. 567 - 575
Copyright
2003 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abramov, I., Hainline, L., Turkel, J., Lemerise, E., Smith, H., Gordon, J., & Petry, S. (1984). Rocket-ship psychophysics. Assessing visual functioning in young children. Investigative Ophthalmology and Visual Science 25, 1307–1315.Google Scholar
Altmann, C.F., Bülthoff, H.H., & Kourtzi, Z. (2003). Perceptual organization of local elements into global shapes in the human visual cortex. Current Biology 13, 342–349.CrossRefGoogle Scholar
Angelucci, A., Levitt, J.B., Walton, E.J., Hupe, J.M., Bullier, J., & Lund, J.S. (2002). Circuits for local and global signal integration in primary visual cortex. Journal of Neuroscience 22, 8633–8646.Google Scholar
Atkinson, J. & Braddick, O. (1992). Visual segmentation of oriented textures by infants. Behavioural Brain Research 49, 123–131.CrossRefGoogle Scholar
Bachevalier, J., Hagger, C., & Mishkin, M. (1991). Functional maturation of the occipitotemporal pathway in infant rhesus monkeys. In Alfred Benzon Symposium 31, Brain Work and Mental Activity, ed. Lassen, N.A., Ingvar, D.H., Raichle, M.E. & Friberg, L., pp. 231–240. Copenahgen: Munksgaard.
Barlow, H.B. (1977). Retinal and central factors in human vision limited by noise. In Vertebrate Photoreception, ed. Barlow, H.B. & Fatt, P., pp. 337–358. New York: Academic Press.
Barone, P., Dehay, C., Berland, M., Bullier, J., & Kennedy, H. (1995). Developmental remodeling of primate visual cortical pathways. Cerebral Cortex 5, 22–38.CrossRefGoogle Scholar
Batardière, A., Barone, P., Knoblauch, K., Giroud, P., Berland, M., Dumas, A-M., & Kennedy, H. (2002). Early specialization of the hierarchical organization of visual cortical areas in the macaque monkey. Cerebral Cortex 12, 453–465.CrossRefGoogle Scholar
Bauer, R. & Heinze, S. (2002). Contour integration in striate cortex: Classic cell responses or cooperative selection? Experimental Brain Research 147, 145–152.Google Scholar
Beaudot, W.H. & Mullen, K.T. (2003). How long range is contour integration in human color vision? Visual Neuroscience 20, 51–64.Google Scholar
Birch, E.E. (1993). Stereopsis in infants and its developmental relation to visual acuity. In Early Visual Development: Normal and Abnormal, ed. Simons, K., pp. 224–236. New York: Oxford University Press.
Birch, E.E., Gwiazda, J., & Held, R. (1982). Stereoacuity development for crossed and uncrossed disparities in human infants. Vision Research 22, 507–513.CrossRefGoogle Scholar
Blasdel, G.G., Obermayer, K., & Kiorpes, L. (1995). Organization of ocular dominance and orientation columns in the striate cortex of neonatal macaque monkeys. Visual Neuroscience 12, 589–603.CrossRefGoogle 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.CrossRefGoogle Scholar
Bradley, A. & Freeman, R.D. (1982). Contrast sensitivity in children. Vision Research 22, 953–959.CrossRefGoogle Scholar
Brown, A.M. (1994). Intrinsic contrast noise and infanct visual contrast discrimination. Vision Research 34, 1947–1964.CrossRefGoogle Scholar
Brown, A.M. & Miracle, J.A. (2003). Early binocular vision in human infants: Limitations on the generality of the Superposition Hypothesis. Vision Research 43, 1563–1574.CrossRefGoogle Scholar
Burkhalter, A. (1993). Development of forward and feedback connections between areas V1 and V2 of human visual cortex. Cerebral Cortex 3, 476–487.CrossRefGoogle Scholar
Burkhalter, A., Bernardo, K.L., & Charles, V. (1993). Development of local circuits in human visual cortex. Journal of Neuroscience 13, 1916–1931.Google Scholar
Callaway, E.M. (1998). Prenatal development of layer-specific local circuits in primary visual cortex of the macaque monkey. Journal of Neuroscience 18, 1505–1527.Google Scholar
Callaway, E.M. & Katz, L.C. (1990). Emergence and refinement of clustered horizontal connections in cat striate cortex. Journal of Neuroscience 10, 1134–1153.Google Scholar
Carkeet, A., Levi, D.M., & Manny R.E. (1997). Development of vernier acuity in childhood. Optometry and Vision Science 74, 741–750.CrossRefGoogle Scholar
Cavanaugh, J.R., Bair, W., & Movshon, J.A. (2002). Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons. Journal of Neurophysiology 88, 2530–2546.CrossRefGoogle 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
Coogan, T.A. & Van Essen, D.C. (1996). Development of connections within and between areas V1 and V2 of macaque monkeys. Journal of Comparative Neurology 372, 327–342.3.0.CO;2-4>CrossRefGoogle Scholar
Curran, W., Braddick, O.J., Atkinson, J., Wattam-Bell, J., & Andrew, R. (1999). Development of illusory-contour perception in infants. Perception 28, 527–538.CrossRefGoogle Scholar
Daw, N.W. (1998). Critical periods and amblyopia. Archives of Ophthalmology 116, 502–505.CrossRefGoogle Scholar
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 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.CrossRefGoogle Scholar
Felleman, D.J. & Van Essen, D.C. (1987). Receptive field properties of neurons in area V3 of macaque monkey extrastriate cortex. Journal of Neurophysiology 57, 889–920.Google Scholar
Field, D.J., Hayes, A., & Hess, R.F. (1993). Contour integration by the human visual system: Evidence for a local ‘association field’. Vision Research 33, 173–193.CrossRefGoogle Scholar
Finney, D.J. (1971). Probit Analysis. New York: Cambridge University Press.
Gattass, R., Gross, C.G., & Sandell, J.H. (1981). Visual topography of V2 in the macaque. Journal of Comparative Neurology 201, 519–539.CrossRefGoogle Scholar
Geisler, W.S., Perry, J.S., Super, B.J., & Gallogly, D.P. (2001). Edge co-occurrence in natural images predicts contour grouping performance. Vision Research 41, 711–724.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
Gilbert, C.D., Das, A., Ito, M., Kapadia, M., & Westheimer, G. (1996). Spatial integration and cortical dynamics. Proceedings of the National Academy of Sciences of the U.S.A. 93, 615–622.CrossRefGoogle 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
Hatta, S., Kumagami, T., Quin, J., Thornton, M., Smith, E.L.III, & Chino, Y.M. (1998). Nasotemporal directional bias of V1 neurons in young infant monkeys. Investigative Ophthalmology and Visual Science 39, 2259–2267.Google Scholar
Herzog, M.H. & Fahle, M. (2002). Effects of grouping in contextual modulation. Nature 415, 433–436.CrossRefGoogle Scholar
Hess, R.F. & Field, D.J. (1999). Integration of contours: New insights. Trends in Cognitive Sciences 3, 480–486.CrossRefGoogle Scholar
Hubel, D.H. & Wiesel, T.N. (1968). Receptive fields and functional architecture of monkey striate cortex. Journal of Physiology 195, 215–243.CrossRefGoogle Scholar
Johnson, S.P. & Aslin, R.N. (1998). Young infants' perception of illusory contours in dynamic displays. Perception 27, 341–353.CrossRefGoogle Scholar
Kapadia, M.K., Ito, M., Gilbert, C.D., & Westheimer, G. (1995). Improvement in visual sensitivity by changes in local context: Parallel studies in human observers and in v1 of alert monkeys. Neuron 15, 843–856.CrossRefGoogle Scholar
Kavšek, M.J. (2002). The perception of static subjective contours in infancy. Child Development 73, 331–344.CrossRefGoogle Scholar
Kiorpes, L. (1992). Development of vernier acuity and grating acuity in normally reared monkeys. Visual Neuroscience 9, 243–251.CrossRefGoogle Scholar
Kiorpes, L. & Movshon, J.A. (1995). The effects of blur and positional jitter on vernier acuity in normal and amblyopic macaque monkeys. Perception 24S: 38.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.CrossRefGoogle 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 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., MIT Press, in press.
Kiorpes, L., Kiper, D.C., & Movshon, J.A. (1993). Contrast sensitivity and vernier acuity in amblyopic monkeys. Vision Research 33, 2301–2311.CrossRefGoogle Scholar
Kiorpes, L., Bassin, S.A., & Movshon, J.A. (2000). Development of contour integration. Society for Neuroscience Abstracts 26, 1080.Google Scholar
Kiorpes, L., Bassin, S.A., & Movshon, J.A. (2001). Development of contour integration. Investigative Ophthalmology and Visual Science (Suppl.) 42, 122.Google Scholar
Kiorpes, L., Tang, C., Hawken, M.J., & Movshon, J.A. (2003). Front-end limitations on the development of spatial contrast sensitivity in macaque monkeys. Journal of Vision (in press).Google Scholar
Knierim, J.J. & Van Essen, D.C. (1992). Neuronal responses to static texture patterns in area V1 of alert macaque monkey. Journal of Neurophysiology 67, 961–980.Google Scholar
Knoblauch, K., Vital-Durand, F., & Barbur, J.L. (2001). Variation of chromatic sensitivity across the life span. Vision Research 41, 23–36.CrossRefGoogle Scholar
Kourtzi, Z., Tolias, A.S., Altmann, C.F., Augath, M., & Logothetis, N.K. (2003). Integration of local features into global shapes: Monkey and human fMRI studies. Neuron 37, 333–346.CrossRefGoogle Scholar
Kovács, I. (1996). Gestalten of today: Early processing of visual contours and surfaces. Behavioural Brain Research 82, 1–11.Google Scholar
Kovács, I. (2000). Human development of perceptual organization. Vision Research 40, 1301–1310.CrossRefGoogle 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.CrossRefGoogle Scholar
Kozma, P. & Kiorpes, L. (2003). Contour integration in amblyopic monkeys. Visual Neuroscience (companion paper).CrossRefGoogle Scholar
Lamme, V.A.F. & Roelfsema, P.R. (2000). The distinct modes of vision offered by feedforward and recurrent processing. Trends in Neurosciences 23, 571–579.CrossRefGoogle Scholar
Lamme, V.A.F., Rodriguez-Rodriguez, V., & Spekreijse, H. (1999). Separate processing dynamics for texture elements, boundaries and surfaces in primary visual cortex of the macaque monkey. Cerebral Cortex 9, 406–413.CrossRefGoogle Scholar
Levi, D.M. & Carkeet, A. (1993). Amblyopia: A consequence of abnormal visual development. In Early Visual Development: Normal and Abnormal, ed. Simons, K., pp. 391–408. New York: Oxford University Press.
Levi, D.M., Sharma, V., & Klein, S.A. (1997). Feature integration in pattern perception. Proceedings of the National Academy of Sciences of the U.S.A. 94, 11742–11746.CrossRefGoogle Scholar
Levitt, J.B. & Lund, J.S. (1996). Asynchronous development of receptive field properties and clustered horizontal connections in macaque striate cortex. Society for Neuroscience Abstracts 22, 491.Google Scholar
Levitt, J.B. & Lund, J.S. (2002). The spatial extent over which neurons in macaque striate cortex pool visual signals. Visual Neuroscience 19, 439–452.CrossRefGoogle Scholar
Lund, J.S. & Levitt, J.B. (1996). Asynchronous development of receptive field properties and clustered horizontal connections in macaque striate cortex. Investigative Ophthalmology and Visual Science (Suppl.) 37, 482.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.CrossRefGoogle 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.CrossRefGoogle 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., Kiorpes, L., Cavanaugh, J.R., & Hawken, M.J. (2000). Developmental reorganization of receptive field surrounds in V1 neurons in macaque monkeys. Investigative Ophthalmology and Visual Science (Suppl.) 41, 333.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.CrossRefGoogle Scholar
O'Dell, C. & Boothe, R.G. (1997). The development of stereoacuity in infant rhesus monkeys. Vision Research 37, 2675–2684.CrossRefGoogle Scholar
Pelli, D.G. (1990). The quantum efficiency of vision. In Vision: Coding and Efficiency, ed. Blakemore, C., pp. 3–24. Cambridge: Cambridge University Press.
Pelli, D.G. & Farell, B. (1999). Why use noise? Journal of the Optical Society of America A 16, 647–653.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.CrossRefGoogle Scholar
Pettet, M.W., McKee, S.P., & Grzywacz, N.M. (1998). Constraints on long range interactions mediating contour detection. Vision Research 38, 865–879.CrossRefGoogle Scholar
Polat, U., Sagi, D., & Norcia, A.M. (1997). Abnormal spatial interactions in amblyopia. Vision Research 37, 737–744.CrossRefGoogle Scholar
Rieth, C. & Sireteanu, R. (1994). Texture segregation and ‘pop-out’ in infants and children: The effect of test field size. Spatial Vision 8, 173–191.CrossRefGoogle Scholar
Rodman, H.R. (1994). Development of inferior temporal cortex in the monkey. Cerebral Cortex 4, 484–498.CrossRefGoogle Scholar
Rodman, H.R., Scalaidhe, S.P., & Gross, C.G. (1993). Response properties of neurons in temporal cortical visual areas of infant monkeys. Journal of Neurophysiology 70, 1115–1136.Google Scholar
Sceniak, M.P., Hawken, M.J., & Shapley, R. (2001). Visual spatial characteristics of macaque V1 neurons. Journal of Neurophysiology 85, 1873–1887.Google Scholar
Shimojo, S. & Held, R. (1987). Vernier acuity is less than grating acuity in 2- and 3-month-olds. Vision Research 27, 77–86.CrossRefGoogle Scholar
Sireteanu, R. & Rieth, C. (1992). Texture segregation in infants and children. Behavioural Brain Research 49, 133–139.CrossRefGoogle Scholar
Skoczenski, A.M. & Norcia, A.M. (1999). Development of VEP acuity and grating acuity in human infants. Investigative Ophthalmology and Visual Science 40, 2411–2417.Google Scholar
Stettler, D.D., Das, A., Bennett, J., & Gilbert, C.D. (2002). Lateral connectivity and contextual interactions in macaque primary visual cortex. Neuron 36, 739–750.CrossRefGoogle Scholar
Teller, D.Y. (1997). First glances: The vision of infants. Investigative Ophthalmology and Visual Science 38, 2183–2203.Google Scholar
Wattam-Bell, J. (2003). Motion processing asymmetries and stereopsis in infants. Vision Research 43, 1961–1968.CrossRefGoogle Scholar
Wilkinson, F. & Crotogino, J. (1995). The late onset of visual texture segmentation in kittens. Behavioural Brain Research 68, 201–217.Google Scholar
Zanker, J., Mohn, G., Weber, U., Zeitler-Driess, K., & Fahle, M. (1992). the development of vernier acuity in human infants. Vision Research 32, 1557–1567.Google Scholar
Zipser, K., Lamme, V.A.F., & Schiller, P.H. (1996). Contextual modulation in primary visual cortex. Journal of Neuroscience 16, 7376–7389.Google Scholar