Development of sensitivity to visual texture modulation in macaque monkeys

Abstract

In human and non-human primates, higher form vision matures substantially later than spatial acuity and contrast sensitivity, as revealed by performance on such tasks as figure-ground segregation and contour integration. Our goal was to understand whether delayed maturation on these tasks was intrinsically form-dependent or, rather, related to the nature of spatial integration necessary for extracting task-relevant cues. We used an intermediate-level form task that did not call for extensive spatial integration. We trained monkeys (6–201 weeks) to discriminate the orientation of pattern modulation in a two-alternative forced choice paradigm. We presented two families of form patterns, defined by texture or contrast variations, and luminance-defined patterns for comparison. Infant monkeys could discriminate texture- and contrast-defined form as early as 6 weeks; sensitivity improved up to 40 weeks. Surprisingly, sensitivity for texture- and contrast-defined form matured earlier than for luminance-defined form. These results suggest that intermediate-level form vision develops in concert with basic spatial vision rather than following sequentially. Comparison with earlier results reveals that different aspects of form vision develop over different time courses, with processes that depend on comparing local image content maturing earlier than those requiring “global” linking of multiple visual elements across a larger spatial extent.

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

“…The colored open circles and associated lines along the abscissa indicate this age, along with a bootstrap estimate of the standard deviation for each data set. Analysis of these computed half-peak ages revealed no significant differences (rotation vs. concentric Glass: p=0.53; translation vs. linear Glass: p=0.45; see 2.3 Methods; El-Shamayleh, Kiorpes & Movshon, 2010), suggesting that sensitivity to RDKs and Glass patterns mature at similar rates. The range of individual variation in threshold for all pattern types is quite large, even among the adults, making it difficult to reliably quantify an “age at maturation”.…”

“…A number of prior studies, using behavioral or evoked potential (VEP) measures, have documented sensitivity to texture boundaries and orientation cues by about 5 months of age in humans ( Atkinson & Braddick, 1992 ; Sireteanu & Rieth, 1992; Norcia et al, 2005; Palomares et al, 2010). Sensitivity to texture-defined form also develops comparatively early in nonhuman primates (El-Shamayleh, Movshon & Kiorpes, 2010). However, the appreciation of global structure in textured displays appears to require additional maturation, since VEP correlates of global organization become evident after 6 months (Norcia et al, 2005; Pei, Pettet & Norcia, 2007; Arcand et al, 2007).…”

Receptive-Field Subfields of V2 Neurons in Macaque Monkeys Are Adult-Like Near Birth

“…While low-level spatial vision depends on identification of forms defined by differences in luminance cues, complex global form vision depends on perceptual grouping of local features over an extended region of space. For example, the sensitivity to texture-defined form is influenced by the ability to extract the appropriate image properties, to integrate these properties, and to segment the shape that is represented (Geisler et al, 2001; 2008; Ing et al, 2010; El-Samayleh et al, 2010; 2011). …”

“…However, newborn human infants are capable of discriminating the orientation of luminance-defined contours of low spatial frequencies near birth (Atkinson et al, 1988). Infant macaque monkeys can discriminate texture- or contrast-defined form as early as 6–8 weeks of age (El- Shamayleh et al, 2010). Human infants also perform well in similar visual tasks near birth (Sireteanu et al; 2005; Norcia et al, 2005; but see Hou et al, 2003).…”

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

“…Testing procedures and stimulus generation methods were typical for the laboratory (see Kiorpes & Movshon, 1998; Kiorpes & Bassin, 2003; Stavros & Kiorpes, 2008; Hall-Haro & Kiorpes, 2008; El-Shamayleh, Movshon & Kiorpes, 2010; Kiorpes et al, 2012). Briefly, visual stimuli were generated by a Dell PC via a VSG2/3 video card (Cambridge Research Systems) and presented on a 21-inch video monitor (Nanao T660i).…”