Cues for the control of ocular accommodation and vergence during postnatal human development

Abstract

Accommodation and vergence help maintain single and focused visual experience while an object moves in depth. The relative importance of retinal blur and disparity, the primary sensory cues to accommodation and vergence, is largely unknown during development; a period when growth of the eye and head necessitate continual recalibration of egocentric space. Here we measured the developmental importance of retinal disparity in 192 typically developing subjects (1.9 months to 46 years). Subjects viewed high-contrast cartoon targets with naturalistic spatial frequency spectra while their accommodation and vergence responses were measured from both eyes using a PowerRefractor. Accommodative gain was reduced during monocular viewing relative to full binocular viewing, even though the fixating eye generated comparable tracking eye movements in the two conditions. This result was consistent across three forms of monocular occlusion. The accommodative gain was lowest in infants and only reached adult levels by 7 to 10 years of age. As expected, the gain of vergence was also reduced in monocular conditions. When 4- to 6-year-old children read 20/40-sized letters, their monocular accommodative gain reached adult-like levels. In summary, binocular viewing appears necessary under naturalistic viewing conditions to generate full accommodation and vergence responses in typically developing humans.

Figure 1

(A) A colored high-contrast cartoon target. (B) A photorefractor image from a 2.2-year-old subject taking part in the binocular condition (top panel) and in the monocular condition (bottom panel). The right eye was occluded in the monocular condition using an infrared Wratten #87 filter mounted on an adult-sized spectacle frame. The white arrowheads in the bottom panel of (B) indicate the medial edges of the IR filter. (C) The experimental equipment. The core components are labeled.

Figure 2

Accommodative, vergence, and left gaze position responses, displaced vertically for clarity, from four representative individuals plotted as a function of time. Stimulus position is plotted at the top in Figures 2A to 2H, followed by the left gaze position, vergence, and finally, accommodation responses. The gray bar (Figure 2D) shows a stimulus epoch used for the gaze position correlation criterion. Asterisks indicate responses that met the inclusion criteria. Accommodation, vergence, and gaze position responses were also measured at 50 cm from some subjects (e.g., Figure 2C), but only responses from 80 and 33 cm were considered for analysis. (I) Comparison of binocular and monocular accommodation on an absolute scale, with no vertical shifting, from a representative subject (3 years old). Negative values in the ordinate indicate an increase in stimulus and response.

Figure 3

The gains of binocular (open circles) and monocular (filled circles) viewing accommodation (Figure 3A), vergence (Figure 3B), and left gaze position (Figure 3C) plotted as a function of age. The black dashed line in each panel denotes unity gain.

Movie 1

Example of a 5-month-old infant taking part in our experiment under binocular (first 1/3rd of the movie) and monocular (second 1/3rd of the movie) viewing conditions. The infant appears calm and cooperative under the binocular condition but becomes fussy and uncooperative when the IR filter is placed over the right eye (monocular condition). The last 1/3rd of the movie shows the infant taking part in the experiment with a ‘plano lens’ in front of the right eye (control experiment III). The infant remains calm and cooperative indicating that the presence of an object in front of the eye did not make the infants uncooperative.

Figure 4

The gain ratios of monocular to binocular viewing accommodation (Figure 4A), vergence (Figure 4B), and left gaze position (Figure 4C), plus binocular vergence to binocular accommodation (Figure 4D) and monocular vergence to monocular accommodation (Figure 4E) as a function of age. The functions were fit to the data using Equation 1, as described in the text. Only functions that showed a significant age-related trend are shown in the figure (Figures 4A and 4B).

Figure 5

(Figure 5A) Slope of the defocus and gaze position calibration functions plotted as a function of age of the subjects. (Figures 5B and 5C) Individually calibrated accommodation and vergence responses to the 1.75 D and 1.75 MA stimulus (black horizontal line) under binocular (Figure 5B) and monocular (Figure 5C) viewing conditions. Each pair of bars represents data from one subject. Individual subjects are arranged by their age in an ascending order.

Figure 6

(Figure 6A) Cycloplegic spherical equivalent refraction (SER) plotted as a function of age. (Figures 6B and 6C) The gain of accommodation and vergence plotted as a function of the SER under binocular and monocular viewing conditions.

Figure 7

Inter-session differences in the gain of accommodation and vergence for ten subjects. Each pair of red and blue circles represents data from one subject. The number of days between the two sessions is noted in parentheses for each subject.

Figure 8

The mean gains of accommodation and left gaze position obtained under binocular, IR filter, and patch viewing conditions (control experiment I) and under binocular, IR filter, and +20 D lens viewing conditions (control experiment II). The error bars indicate ±1-SEM.

Figure 9

The mean accommodative, vergence, and left gaze position gains obtained under binocular, IR filter, and plano lens viewing conditions (control experiment III). The error bars indicate ±1-SEM.

Figure 10

The mean gains of accommodation and vergence obtained when subjects watched the movie and read the letter targets under binocular and monocular viewing conditions (control experiment IV). The error bars indicate ±1-SEM.