Late Development of Sensory Thresholds for Horizontal Relative Disparity in Human Visual Cortex in the Face of Precocial Development of Thresholds for Absolute Disparity

Abstract

Immaturities exist at multiple levels of the developing human visual pathway, starting with immaturities in photon efficiency and spatial sampling in the retina and on through immaturities in the early and later stages of cortical processing. Here, we use steady-state visual evoked potentials (SSVEPs) and controlled visual stimuli to determine the degree to which sensitivity to horizontal retinal disparity is limited by the visibility of the monocular half-images, the ability to encode absolute disparity, or the ability to encode relative disparity. Responses were recorded from male and female human participants at average ages of 5.3 ± 1.6 months, 4.7 ± 1.3 years, and 25.3 ± 6 years. Horizontal disparity sensitivity was measured using planar stereograms that modulated absolute disparity and stereograms portraying disparity gratings that additionally contained relative disparity. Disparity thresholds for absolute disparity changed little over development, but those for relative disparity changed by a factor of ∼10. SSVEPs were also recorded in response to contrast and blur modulation of dynamic random-dot patterns to measure sensitivity to the spatiotemporal content of the monocular half-images. Equating subjective contrast and blur levels between infants, children, and adults based on these measurements did not equate disparity sensitivity. The protracted developmental sequence for horizontal relative disparity coding shown in our measurements is not simply inherited from immaturities in encoding absolute disparity or retinal image contrast but rather reflects immaturities in the computations needed to represent relative disparity that likely involves extrastriate cortical areas where relative disparity is first extracted.

Keywords: binocular disparity; evoked potentials; human; stereopsis; visual cortex; visual development.

Figure 1.

A, Schematic random-dot stereopair used in the main experiment. The stereograms comprised a zero-disparity fusion lock (i), a circular region depicting a sinusoidal disparity grating (crossed disparity when cross-fused, ii), a small ring of uncorrelated dots (iii), and a dichoptic fixation target (red lines). The dots in the actual experiment were dynamic. B, Top-down schematic illustration of disparity plane (absolute) and disparity grating (relative plus absolute disparity) stimuli. Fixation point N (nonius lines) is on the zero-disparity plane defined by the horopter (approximated as the green Vieth–Müller circle). Point 1 (purple) is also on the horopter and angles ${\alpha }_{\mathrm{L}}$ and ${\alpha }_{\mathrm{R}}$ are equal, meaning that the absolute disparity given by ${\alpha }_{\mathrm{L}}-{\alpha }_{\mathrm{R}}$ is zero. Point 2 (orange) is either on a second, disparate plane (dotted line) or on the peak of a disparity grating (sinusoidal line). Here, the absolute disparity, ${\beta }_{\mathrm{L}}-{\beta }_{\mathrm{R}}$, is nonzero. The relative disparity is the difference between the two absolute disparities, ( ${\alpha }_{\mathrm{L}}-{\alpha }_{\mathrm{R}})-({\beta }_{\mathrm{L}}-{\beta }_{\mathrm{R}})$, and varies depending on the location on the sinewave, but its magnitude is independent of fixation. Disparity along the second plane (dotted line) is constant at a nonzero value. C, Schematic of disparity plane stimulus (1) that involves the temporal modulation at 2 Hz between crossed disparity, “disparity on” and zero disparity, “disparity off” phases. Schematic illustration of disparity grating stimuli (2, 3) that involve 2 Hz temporal modulation between a cyclopean grating portrayed with crossed disparity and a zero-disparity plane. Adult participants were asked to detect a brief color change on the nonius fixation lines (red lines in A, red and blue lines in B).

Figure 2.

Schematic top view of electrode locations used for the extraction of vergence (A) and version (B) eye movements from EEG electrodes at locations above the nasion (b) and near the outer canthi of the left (a) and right (c) eyes. Convergence is indicated by blue arrows and divergence by red arrows in A. The rightward version (dextroversion) is indicated by blue arrows in B, with the leftward version (levoversion) being indicated by red arrows in B. The EOG comprises a current dipole whose axis is oriented along the direction of the lines, with corresponding opposite polarities at a versus b and b versus c.

Figure 3.

RC1 topographies for responses to the disparity plane (0 cpd) and disparity grating (0.5 and 1.2 cpd) stimuli in infants, children, and adults. Topographies were learned on the 1F1–4F1 disparity response and were maximal over a cluster of midline occipital electrodes. Generally, the response to grating stimuli was more diffuse than the response to plane stimuli, and responses to the monocular image manipulations (contrast and blur) were the most focal.

Figure 4.

Disparity response functions measured at 1F1 (left) and 2F1 (right) for adults (n = 22), children (n = 37), and infants (n = 15) over different spatial conditions: disparity plane (green), 0.5 cpd disparity grating (purple), and 1.2 cpd disparity grating (orange) stimulus conditions.

Figure 5.

Dominant harmonic disparity tuning disparity response functions for adults (n = 22), children (n = 37), and infants (n = 15) over different spatial conditions replotted from Figure 4 after amplitude normalization. A, Disparity plane responses measured at 2F1 for adults (green), children (purple), and infants (orange). B, Disparity grating response functions measured at 1F1 and 0.5 cpd, color convention as in A. C, As in B but for a 1.2 cpd grating (children and adults). The vertical lines indicate the estimated value of Dmin for each group.

Figure 6.

Amplitude-normalized contrast response functions for infants (orange), children (purple), and adults (green) for 1F1 (A) and 2F1 (B) response components. The vertical lines indicate the estimated contrast threshold for each group.

Figure 7.

Amplitude-normalized blur response functions for adults (green), children (purple), and infants (orange) at 1F1 (A) and 2F1 (B) response harmonics. The vertical lines indicate the estimated blur threshold for each group.

Figure 8.

Infant and child data from Figure 5 are replotted with adult data measured at equal subjective contrast. Thresholds for children are approximately equal to those of adults for the disparity plane and the two disparity grating conditions. Infant thresholds are approximately equal for the disparity plane condition but still differ by a factor of ∼10 for the 0.5 cpd grating condition. The vertical lines indicate the estimated value of Dmin for each group.

Figure 9.

Infant and child data from Figure 5 are replotted with adult data at equal subjective blur levels. Thresholds for children are equal to those of adults for the disparity plane and the two disparity grating conditions. Infant thresholds are higher by factors of 5.6 and 8.8 for 4 and 8 arcmin blur levels, respectively.

Figure 10.

Vergence (A) and version (B) signals in response to 2 Hz changes of absolute disparity for the disparity plane [absolute disparity stimulus for infants, children, and adults at 1F1 (orange) and 2F1 (purple)]. Error bars indicate ±1 SEM.