Though this method can easily measure the disarray among the cones, the main conclusion is that the disarray is, in fact, very small.
Figure 5 illustrates the lack of disarray when we project the axes of the disarrayed photoreceptors into the pupil plane of the eye. The average disarray has a full width at half maximum of 0.41 mm (from 0.17 sigma), which corresponds to an angle of 1 deg subtending only 13% of a 3-mm pupil diameter. The results are tabulated in
Table 1. Corrections for blur, variations in illumination beam intensity, and effects of the finite aperture are included in the tabulated results.
Our results agree with
Burns et al. (1996),
Marcos and Burns (1999), and
MacLeod (1974), all of whom concluded that there must be very little photoreceptor disarray. MacLeod calculated the disarray to be 0.32 mm (standard deviation of pupil intercept position), which is in reasonable agreement with our average finding of 0.17 mm. MacLeod’s larger value may be due to the larger 2-deg test field size that he used versus our contiguous patch of cones of approximately 0.25-deg diameter. Our disarray is expected to be slightly narrower because of the correlation in pointing direction between neighboring cones. Furthermore, MacLeod measured the disarray 6 deg from the fovea compared to 1 deg for our measurement. Areal coverage by blood vessels anterior to the photoreceptors increases from zero at the foveal avascular zone to as high as 30% in the periphery (
Snodderly, Weinhaus, & Choi, 1992), and a measurement of increased disarray in the periphery might be due to effective changes in the pointing direction of the cones caused by blood vessels.
Photoreceptor alignment is governed by a phototropic mechanism that actively aligns the cones to point toward the entrance pupil of the eye (
Enoch & Lakshminarayanan, 1991). The best evidence for this is the active realignment of the Stiles-Crawford peak toward the pupil center in a patient following removal of a cataract that obscured all but the margin of the pupil on one side (
Smallman, MacLeod, & Doyle, 2001).
The mechanism for realignment is unknown. Is the precision that we have observed in photoreceptor alignment the property of a phototropic mechanism in individual cones or groups of cones? A uniform pointing direction among the cones is desirable, but there is no clear benefit of the extent to which the cones are so uniformly aligned in the human eye. For example, the disarray we measured accounts for less than 1% of the breadth of the overall tuning function. A 4-fold increase in disarray for G.Y. would only broaden the overall tuning by 7.3%. Furthermore, any reduction in disarray will generate only tiny increases in detected image-forming light, or corresponding decreases in detected nonimaging light. These benefits are small, especially in light of the fact that J.P. detects about 25% fewer photons through a 4-mm pupil because his angular tuning peak is displaced 1.41-mm nasal. Displacements of this amount are common and average about 0.5 mm in the nasal direction (
Dunnewold, 1964;
Applegate & Lakshminarayanan, 1993). The idea that the alignment mechanism resides in each individual cone is not unreasonable given that motor movements of photoreceptors are reported in other vertebrate species (
Burnside, 2001). A sophisticated feedback system is not a necessity for an individual cone mechanism to be effective because the fine alignment most likely is augmented by the physical properties of the ensemble of cones, which are long, thin, and close-packed into a nearly hexagonal matrix. Observations that implicate physical/biomechanical factors in controlling the directionality of cones in the retina have been those that disrupt ideal photoreceptor orientation. For example, shifts in pointing direction have been observed in large patches of photoreceptors near the optic disc of high myopes (
Enoch, Choi, Kono, Lakshminarayanan, & Calvo, 2001) and in eyes with proliferative diabetic retinopathy
(Bresnick, Smith, & Pokorny, 1981), both of which are thought to be caused by tractional forces in the retina. On a more local scale, cones demonstrate an inability to compensate for apparent peak displacements caused by prismatic effects along the slope of the foveal pit (
Williams, 1980). This work identifies a case where the same biomechanical factors enhance the uniformity in pointing direction of the cones.