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Linking structure and function: Development of lateral spatial interactions in macaque monkeys

Published online by Cambridge University Press:  10 October 2013

DA-PENG LI
Affiliation:
Center for Neural Science, New York University, New York, New York State Key Laboratory of Brain and Cognitive Sciences, Institute of Biophysics, Chinese Academy of Sciences, Beijing, China
MAUREEN A. HAGAN
Affiliation:
Center for Neural Science, New York University, New York, New York
LYNNE KIORPES*
Affiliation:
Center for Neural Science, New York University, New York, New York
*
Address correspondence to: Lynne Kiorpes, Center for Neural Science, 4 Washington Place, Room 809, New York University, New York, NY 10003. E-mail: [email protected]

Abstract

Lateral spatial interactions among elements of a scene, which either enhance or degrade visual performance, are ubiquitous in vision. The neural mechanisms underlying lateral spatial interactions are a matter of debate, and various hypotheses have been proposed. Suppressive effects may be due to local inhibitory interactions, whereas facilitatory effects are typically ascribed either to the function of long-range horizontal projections in V1 or to uncertainty reduction. We investigated the development of lateral spatial interactions, facilitation and suppression, and compared their developmental profiles to those of potential underlying mechanisms in the visual system of infant macaques. Animals ranging in age from 10 weeks to 3 years were tested with a lateral masking paradigm. We found that suppressive interactions are present from very early in postnatal life, showing no change over the age range tested. However, facilitation develops slowly over the first year after birth. Our data suggest that the early maturation of suppressive interactions is related to the relatively mature receptive field properties of neurons in early visual cortical areas near birth in infant macaques, whereas the later maturation of facilitation is unlikely to be explained by development of local or long-range connectivity in primary visual cortex. Instead our data favor a late developing feedback or top-down cognitive process to explain the origin of facilitation.

Type
Linking performance and neural mechanisms in development and disability
Copyright
Copyright © Cambridge University Press 2013 

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References

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 2, 86338646.CrossRefGoogle Scholar
Baldwin, M.K., Kaskan, P.M., Zhang, B., Chino, Y.M. & Kaas, J.H. (2012). Cortical and subcortical connections of V1 and V2 in early postnatal macaque monkeys. The Journal of Comparative Neurology 520, 544569.CrossRefGoogle ScholarPubMed
Batardière, A., Barone, P., Knoblauch, K., Giroud, P., Berland, M., Dumas, A.M. & Kennedy, H. (2002). Early specification of the hierarchical organization of visual cortical areas in the macaque monkey. Cerebral Cortex 12, 453465.CrossRefGoogle ScholarPubMed
Blasdel, G., Obermeyer, K. & Kiorpes, L. (1995). Organization of ocular dominance and orientation columns in the striate cortex of neonatal macaque monkeys. Visual Neuroscience 12, 589603.CrossRefGoogle ScholarPubMed
Bonneh, Y.S., Sagi, D. & Polat, U. (2004). Local and non-local deficits in amblyopia: Acuity and spatial interactions. Vision Research 44, 30993110.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, 387396.CrossRefGoogle ScholarPubMed
Burkhalter, A. (1993). Development of forward and feedback connections between areas V1 and V2 of human visual cortex. Cerebral Cortex 3, 476487.CrossRefGoogle ScholarPubMed
Callaway, E.M. (1998). Prenatal development of layer-specific local circuits in primary visual cortex of the macaque monkey. The Journal of Neuroscience 18, 15051527.CrossRefGoogle ScholarPubMed
Cannon, M.W. & Fullenkamp, S.C. (1991). Spatial interactions in apparent contrast: Inhibitory effects among grating patterns of different spatial frequencies, spatial positions and orientations. Vision Research 31, 19851998.CrossRefGoogle ScholarPubMed
Chen, C.C. & Tyler, C.W. (2008). Excitatory and inhibitory interaction fields of flankers revealed by contrast-masking functions. Journal of Vision 8, 10.CrossRefGoogle ScholarPubMed
Chino, Y.M., Smith, E.L., Hatta, S. & Cheng, H. (1997). Postnatal development of binocular disparity sensitivity in neurons of the primate visual cortex. The Journal of Neuroscience 17, 296307.CrossRefGoogle ScholarPubMed
Coogan, T.A. & Van Essen, D.C. (1996). Development of connections within and between areas V1 and V2 of macaque monkeys. The Journal of Comparative Neurology 372, 327342.3.0.CO;2-4>CrossRefGoogle ScholarPubMed
El-Shamayleh, Y., Movshon, J.A. & Kiorpes, L. (2010). Development of sensitivity to visual texture modulation in macaque monkeys. Journal of Vision 10, 11.CrossRefGoogle ScholarPubMed
Ellemberg, D., Hess, R.F. & Arsenault, A.S. (2002). Lateral interactions in amblyopia. Vision Research 42, 24712478.CrossRefGoogle ScholarPubMed
Finney, D.J. (1971). Probit Analysis. New York: Cambridge University Press.Google Scholar
Gilbert, C.D. & Li, W. (2013). Top-down influences on visual processing. Nature Reviews. Neuroscience 14, 350363.CrossRefGoogle ScholarPubMed
Hall-Haro, C. & Kiorpes, L. (2008). Normal development of pattern motion sensitivity in macaque monkeys. Visual Neuroscience 25, 675684.CrossRefGoogle ScholarPubMed
Horton, J.C. & Hocking, D.R. (1996). An adult-like pattern of ocular dominance columns in striate cortex of newborn monkeys prior to visual experience. The Journal of Neuroscience 16, 17911807.CrossRefGoogle ScholarPubMed
Hou, C., Pettet, M.W., Sampath, V., Candy, T.R. & Norcia, A.M. (2003). Development of the spatial organization and dynamics of lateral interactions in the human visual system. The Journal of Neuroscience 23, 86308640.CrossRefGoogle ScholarPubMed
Huttenlocher, P.R. (1990). Morphometric study of human cerebral cortex development. Neuropsychologia 28, 517527.CrossRefGoogle ScholarPubMed
Ito, M., Westheimer, G. & Gilbert, C.D. (1998). Attention and perceptual learning modulate contextual influences on visual perception. Neuron 20, 11911197.CrossRefGoogle ScholarPubMed
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, 843856.CrossRefGoogle ScholarPubMed
Kapadia, M.K., Westheimer, G. & Gilbert, C.D. (2000). Spatial distribution of contextual interactions in primary visual cortex and in visual perception. Journal of Neurophysiology 84, 20482062.CrossRefGoogle ScholarPubMed
Katz, L.C. & Callaway, E.M. (1992). Development of local circuits in mammalian visual cortex. Annual Review of Neuroscience 15, 3156.CrossRefGoogle ScholarPubMed
Kennedy, H. & Burkhalter, A. (2004). Ontogenesis of cortical connectivity. In The Visual Neurosciences, ed. Chalupa, L.M. & Werner, J.S., pp. 146158. Cambridge, MA: MIT Press.Google Scholar
Kiorpes, L. (1992). Development of vernier acuity and grating acuity in normally reared monkeys. Visual Neuroscience 34, 243251.CrossRefGoogle Scholar
Kiorpes, L. & Bassin, S.A. (2003). Development of contour integration in macaque monkeys. Visual Neuroscience 20, 567575.CrossRefGoogle ScholarPubMed
Kiorpes, L., Li, D. & Hagan, M. (2008). Crowding in primates: A comparison of humans and macaque monkeys. Perception 37, 37.Google Scholar
Kiorpes, L. & Movshon, J.A. (1998). Peripheral and central factors limiting the development of contrast sensitivity in macaque monkeys. Vision Research 38, 6170.CrossRefGoogle ScholarPubMed
Kiorpes, L. & Movshon, J.A. (2004). Neural limitations on visual development in primates. In The Visual Neurosciences, ed. Chalupa, L.M. & Werner, J.S., pp. 159173. Cambridge, MA: MIT Press.Google Scholar
Kiorpes, L., Price, T., Hall-Haro, C. & Movshon, J.A. (2012). Development of sensitivity to global form and motion in macaque monkeys (Macaca nemestrina). Vision Research 63, 3442.CrossRefGoogle ScholarPubMed
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 United States of America 96, 1220412209.CrossRefGoogle ScholarPubMed
Kozma, P. & Kiorpes, L. (2003). Contour integration in amblyopic monkeys. Visual Neuroscience 20, 577588.CrossRefGoogle ScholarPubMed
Levi, D.M. & Carney, T. (2011). The effect of flankers on three tasks in central, peripheral, and amblyopic vision. Journal of Vision 11, 10.CrossRefGoogle ScholarPubMed
Levi, D.M., Klein, S.A. & Hariharan, S. (2002). Suppressive and facilitatory spatial interactions in foveal vision: Foveal crowding is simple contrast masking. Journal of Vision 2, 140166.Google ScholarPubMed
Levi, D.M., Yu, C., Kuai, S.G. & Rislove, E. (2007). Global contour processing in amblyopia. Vision Research 47, 512524.CrossRefGoogle ScholarPubMed
Li, W., Piëch, V. & Gilbert, C.D. (2004). Perceptual learning and top-down influences in primary visual cortex. Nature Neuroscience 7, 651657.CrossRefGoogle ScholarPubMed
Li, W., Piëch, V. & Gilbert, C.D. (2008). Learning to link visual contours. Neuron 57, 442451.CrossRefGoogle ScholarPubMed
Lund, J.S., Boothe, R.G. & Lund, R.D. (1977). Development of neurons in the visual cortex (area 17) of the monkey (Macaca nemestrina): A Golgi study from fetal day 127 to postnatal maturity. The Journal of Comparative Neurology 176, 149188.CrossRefGoogle ScholarPubMed
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
Malach, R., Amir, Y., Harel, M. & Grinvald, A. (1993). Relationship between intrinsic connections and functional architecture revealed by optical imaging and in vivo targeted biocytin injections in primate striate cortex. Proceedings of the National Academy of Sciences of the United States of America 90, 1046910473.CrossRefGoogle ScholarPubMed
Morgan, M.J. & Dresp, B. (1995). Contrast detection facilitation by spatially separated targets and inducers. Vision Research 35, 10191024.CrossRefGoogle ScholarPubMed
Norcia, A.M., Sampath, V., Hou, C. & Pettet, M.W. (2005). Experience-expectant development of contour integration mechanisms in human visual cortex. Journal of Vision 5, 116130.CrossRefGoogle ScholarPubMed
Petrov, Y., Verghese, P. & McKee, S.P. (2006). Collinear facilitation is largely uncertainty reduction. Journal of Vision 6, 170178.CrossRefGoogle ScholarPubMed
Polat, U. (2009). Effect of spatial frequency on collinear facilitation. Spatial Vision 22, 179193.CrossRefGoogle ScholarPubMed
Polat, U., Bonneh, Y., Ma-Naim, T., Belkin, M. & Sagi, D. (2005). Spatial interactions in amblyopia: Effects of stimulus parameters and amblyopia type. Vision Research 45, 14711479.CrossRefGoogle ScholarPubMed
Polat, U. & Norcia, A.M. (1996). Neurophysiological evidence for contrast dependent long-range facilitation and suppression in the human visual cortex. Vision Research 36, 20992109.CrossRefGoogle ScholarPubMed
Polat, U. & Sagi, D. (1993). Lateral interactions between spatial channels: Suppression and facilitation revealed by lateral masking experiments. Vision Research 33, 993997.CrossRefGoogle ScholarPubMed
Polat, U. & Sagi, D. (1994 a). Spatial interactions in human vision: From near to far via experience-dependent cascades of connections. Proceedings of the National Academy of Sciences of the United States of America 91, 12061209.CrossRefGoogle ScholarPubMed
Polat, U. & Sagi, D. (1994 b). The architecture of perceptual spatial interactions. Vision Research 34, 7378.CrossRefGoogle ScholarPubMed
Polat, U., Sagi, D. & Norcia, A.M. (1997). Abnormal long-range spatial interactions in amblyopia. Vision Research 37, 737744.CrossRefGoogle ScholarPubMed
Ramalingam, N., McManus, J.N.J., Li, W. & Gilbert, C.D. (2013). Top-down modulation of lateral interactions in visual cortex. The Journal of Neuroscience 33, 17731789.CrossRefGoogle ScholarPubMed
Sokol, S., Zemon, V. & Moskowitz, A. (1992). Development of lateral interactions in the infant visual system. Visual Neuroscience 8, 38.CrossRefGoogle ScholarPubMed
Solomon, J.A. & Morgan, M.J. (2000). Facilitation from collinear flanks is cancelled by non-collinear flanks. Vision Research 40, 279286.CrossRefGoogle ScholarPubMed
Solomon, J.A., Sperling, G. & Chubb, C. (1993). The lateral inhibition of perceived contrast is indifferent to on-center/off-center segregation, but specific to orientation. Vision Research 33, 26712683.CrossRefGoogle ScholarPubMed
Stavros, K.A. & Kiorpes, L. (2008). Behavioral measurement of temporal contrast sensitivity development in macaque monkeys (Macaca nemestrina). Vision Research 48, 13351344.CrossRefGoogle ScholarPubMed
Stettler, D.D., Das, A., Bennett, J. & Gilbert, C.D. (2002). Lateral connectivity and contextual interactions in macaque primary visual cortex. Neuron 36, 739750.CrossRefGoogle ScholarPubMed
Teller, D.Y. & Boothe, R.G. (1979). Development of vision in infant primates. Transactions of the Ophthalmological Societies of the United Kingdom 99, 333337.Google ScholarPubMed
Teller, D.Y. (1984). Linking propositions. Vision Research 24, 12331246.CrossRefGoogle ScholarPubMed
Ts’o, D.Y., Gilbert, C.D. & Wiesel, T.N. (1986). Relationships between horizontal interactions and functional architecture in cat striate cortex as revealed by cross-correlation analysis. The Journal of Neuroscience 6, 11601170.CrossRefGoogle ScholarPubMed
Wiesel, T.N. & Hubel, D.H. (1974). Ordered arrangements of orientation columns in monkeys lacking visual experience. The Journal of Comparative Neurology 158, 307318.CrossRefGoogle ScholarPubMed
Wong, E.H., Levi, D.M. & McGraw, P.V. (2005). Spatial interactions reveal inhibitory cortical networks in human amblyopia. Vision Research 45, 28102819.CrossRefGoogle ScholarPubMed
Yoshioka, T., Blasdel, G.G., Levitt, J.B. & Lund, J.S. (1996). Relation between patterns of intrinsic lateral connectivity, ocular dominance, and cytochrome oxidase-reactive regions in macaque monkey striate cortex. Cerebral Cortex 6, 297310.CrossRefGoogle ScholarPubMed
Zhang, B., Tao, X., Shen, G., Smith, E.L. III, Ohzawa, I. & Chino, Y.M. (2013). Receptive-field subfields of V2 neurons in macaque monkeys are adult-like near birth. The Journal of Neuroscience 33, 26392649.CrossRefGoogle ScholarPubMed
Zhang, B., Zheng, J., Watanabe, I., Maruko, I., Bi, H., Smith, E.L. III & Chino, Y. (2005). Delayed maturation of receptive field center/surround mechanisms in V2. Proceedings of the National Academy of Sciences of the United States of America 102, 58625867.CrossRefGoogle ScholarPubMed
Zheng, J., Zhang, B., Bi, H., Maruko, I., Watanabe, I., Nakatsuka, C., Smith, E.L. III & Chino, Y.M. (2007). Development of temporal response properties and contrast sensitivity of V1 and V2 neurons in macaque monkeys. Journal of Neurophysiology 97, 39053916.CrossRefGoogle ScholarPubMed