Development of sensitivity to global form and motion in macaque monkeys (Macaca nemestrina)

To explore the relative development of the dorsal and ventral extrastriate processing streams, we studied the development of sensitivity to form and motion in macaque monkeys (Macaca nemestrina). We used Glass patterns and random dot kinematograms (RDK) to assay ventral and dorsal stream function, respectively. We tested 24 animals, longitudinally or cross-sectionally, between the ages of 5 weeks and 3 years. Each animal was tested with Glass patterns and RDK stimuli with each of two pattern types--circular and linear--at each age using a two alternative forced-choice task. We measured coherence threshold for discrimination of the global form or motion pattern from an incoherent control stimulus. Sensitivity to global motion appeared earlier than to global form and was higher at all ages, but performance approached adult levels at similar ages. Infants were most sensitive to large spatial scale (Δx) and fast speeds; sensitivity to fine scale and slow speeds developed more slowly independently of pattern type. Within the motion domain, pattern type had little effect on overall performance. However, within the form domain, sensitivity for linear Glass patterns was substantially poorer than that for concentric patterns. Our data show comparatively early onset for global motion integration ability, perhaps reflecting early development of the dorsal stream. However, both pathways mature over long time courses reaching adult levels between 2 and 3 years after birth.

[1]  Janette Atkinson,et al.  Dorsal and ventral stream sensitivity in normal development and hemiplegia , 2002, Neuroreport.

[2]  L. Kiorpes,et al.  Scale-dependent loss of global form perception in strabismic amblyopia. , 2010, Journal of vision.

[3]  Lynne Kiorpes,et al.  Development of contour integration in macaque monkeys , 2003, Visual Neuroscience.

[4]  L. Kiorpes,et al.  Behavioral measurement of temporal contrast sensitivity development in macaque monkeys (Macaca nemestrina) , 2008, Vision Research.

[5]  Kevin J. Riggs,et al.  Motion processing in autism: evidence for a dorsal stream deficiency , 2000, Neuroreport.

[6]  L. Kiorpes Macaque Models of Visual Development and Disability , 2008 .

[7]  Vision Research , 1961, Nature.

[8]  Z. Kourtzi,et al.  Neural coding of global form in the human visual cortex. , 2008, Journal of neurophysiology.

[9]  J. Movshon,et al.  Development of sensitivity to visual texture modulation in macaque monkeys. , 2010, Journal of Vision.

[10]  L. Kiorpes Development of vernier acuity and grating acuity in normally reared monkeys , 1992, Visual Neuroscience.

[11]  Franco Lepore,et al.  Comparison of sensitivity to first- and second-order local motion in 5-year-olds and adults. , 2003, Spatial vision.

[12]  Marcello G P Rosa,et al.  Hierarchical development of the primate visual cortex, as revealed by neurofilament immunoreactivity: early maturation of the middle temporal area (MT). , 2006, Cerebral cortex.

[13]  K. H. Britten,et al.  Responses of neurons in macaque MT to stochastic motion signals , 1993, Visual Neuroscience.

[14]  H. Bülthoff,et al.  Perceptual Organization of Local Elements into Global Shapes in the Human Visual Cortex , 2003, Current Biology.

[15]  H. Wilson,et al.  Concentric orientation summation in human form vision , 1997, Vision Research.

[16]  I. Kovács Human development of perceptual organization , 2000, Vision Research.

[17]  I. Kovács,et al.  Late maturation of visual spatial integration in humans. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[18]  A. Burkhalter,et al.  Development of local circuits in human visual cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  J. Atkinson,et al.  Motion- and orientation-specific cortical responses in infancy , 2005, Vision Research.

[20]  Akos Feher,et al.  Detection of contour continuity and closure in three-month-olds , 2004, Vision Research.

[21]  Nicole C. Rust,et al.  Receptive field properties of MT neurons in infant macaques , 2004 .

[22]  D. Maurer,et al.  Development of spatial and temporal vision during childhood , 1999, Vision Research.

[23]  J. Atkinson,et al.  Normal and anomalous development of visual motion processing: motion coherence and ‘dorsal-stream vulnerability’ , 2003, Neuropsychologia.

[24]  J. Movshon,et al.  The analysis of visual motion: a comparison of neuronal and psychophysical performance , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  W. Newsome,et al.  A selective impairment of motion perception following lesions of the middle temporal visual area (MT) , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  Daniel C. Kiper,et al.  Development of contrast sensitivity across the visual field in macaque monkeys (Macaca nemestrina) , 1996, Vision Research.

[27]  T. L. Lewis,et al.  Differential vulnerability of global motion, global form, and biological motion processing in full-term and preterm children , 2009, Neuropsychologia.

[28]  C. Gilbert,et al.  Contour Saliency in Primary Visual Cortex , 2006, Neuron.

[29]  L. Glass Moiré Effect from Random Dots , 1969, Nature.

[30]  Leslie G. Ungerleider,et al.  Cue-dependent deficits in grating orientation discrimination after V4 lesions in macaques , 1996, Visual Neuroscience.

[31]  M. Roy,et al.  Development of visual texture segregation during the first year of life: a high-density electrophysiological study , 2007, Experimental Brain Research.

[32]  Nikos K. Logothetis,et al.  Integration of Local Features into Global Shapes: Monkey and Human fMRI Studies , 2010 .

[33]  Leslie G. Ungerleider,et al.  Functional development of the corticocortical pathway for motion analysis in the macaque monkey: a 14C-2-deoxyglucose study. , 1996, Cerebral cortex.

[34]  Janette Atkinson,et al.  Visual segmentation of oriented textures by infants , 1992, Behavioural Brain Research.

[35]  Anthony M. Norcia,et al.  Sensitivity and configuration-specificity of orientation-defined texture processing in infants and adults , 2007, Vision Research.

[36]  D Regan,et al.  Development of Motion-Defined Figure-Ground Segregation in Preschool and Older Children, Using a Letter-Identification Task , 1997, Optometry and vision science : official publication of the American Academy of Optometry.

[37]  J. Atkinson,et al.  Reorganization of Global Form and Motion Processing during Human Visual Development , 2010, Current Biology.

[38]  L. Kiorpes,et al.  Normal development of pattern motion sensitivity in macaque monkeys , 2008, Visual Neuroscience.

[39]  D. Teller,et al.  Operant measurements of contrast sensitivity in infant macaque monkeys during normal development , 1988, Vision Research.

[40]  C. Gross,et al.  Response properties of neurons in temporal cortical visual areas of infant monkeys. , 1993, Journal of neurophysiology.

[41]  A. Burkhalter Development of forward and feedback connections between areas V1 and V2 of human visual cortex. , 1993, Cerebral cortex.

[42]  L. Chalupa,et al.  The visual neurosciences , 2004 .

[43]  D. Teller,et al.  First glances: the vision of infants. the Friedenwald lecture. , 1997, Investigative ophthalmology & visual science.

[44]  Leslie G. Ungerleider,et al.  Ventral and Dorsal Cortical Processing Streams , 2013 .

[45]  M. Landy,et al.  Orientation-selective adaptation to first- and second-order patterns in human visual cortex. , 2006, Journal of neurophysiology.

[46]  J. Lund,et al.  The hierarchical development of monkey visual cortical regions as revealed by the maturation of parvalbumin-immunoreactive neurons. , 1996, Brain research. Developmental brain research.

[47]  M. Pettet,et al.  Spatio-temporal tuning of coherent motion evoked responses in 4–6 month old infants and adults , 2009, Vision Research.

[48]  Ruxandra Sireteanu,et al.  Texture segregation in infants and children , 1992, Behavioural Brain Research.

[49]  Anthony M. Norcia,et al.  Development of Sensitivity to Texture and Contour Information in the Human Infant , 2005, Journal of Cognitive Neuroscience.

[50]  Jinhua Bao,et al.  The effect of blur adaptation on accommodative response and pupil size during reading. , 2010, Journal of vision.

[51]  Lynne Kiorpes,et al.  Development of sensitivity to visual motion in macaque monkeys , 2004, Visual Neuroscience.

[52]  T. L. Lewis,et al.  Putting order into the development of sensitivity to global motion , 2004, Vision Research.

[53]  H. A. Pham,et al.  Perceptual deficits after lesions of inferotemporal cortex in macaques. , 2000, Cerebral cortex.

[54]  J. Gaddum Probit Analysis , 1948, Nature.

[55]  N. Logothetis,et al.  Integration of Local Features into Global Shapes Monkey and Human fMRI Studies , 2003, Neuron.

[56]  C. Gilbert,et al.  Learning to Link Visual Contours , 2008, Neuron.

[57]  R. Dougherty,et al.  The maturation of form and motion perception in school age children , 2005, Vision Research.

[58]  W. Merigan Cortical area V4 is critical for certain texture discriminations, but this effect is not dependent on attention , 2000, Visual Neuroscience.

[59]  Grace Truong,et al.  Effects of speed, age, and amblyopia on the perception of motion-defined form , 2011, Vision Research.

[60]  R. Pérez,et al.  Perception of Random Dot Interference Patterns , 1973, Nature.

[61]  Anthony M. Norcia,et al.  Connecting the Dots: How Local Structure Affects Global Integration in Infants , 2010, Journal of Cognitive Neuroscience.

[62]  Daniel Brandeis,et al.  Maturation of luminance- and motion-defined form perception beyond adolescence: A combined ERP and fMRI study , 2006, NeuroImage.