Specialized photoreceptors at the dorsal rim of the honeybee's compound eye: Polarizational and angular sensitivity

Abstract

1. The spectral, polarizational and angular sensitivities of photoreceptor cells In the honeybee compound eye are examined by intracellular electrophysiological recordings. The specific aim of this paper is to compare the characteristics of receptor cells in the anatomically specialized dorsal rim area of the eye (containing non-twisted retinulae which are composed of 9 long receptor cells) with those of receptors in the remainder of the eye (containing twisted retinulae which are composed of 8 long cells and 1 short cell). 2. The direction of the optical axis for each cell investigated was determined within a coordinate system of space that takes into consideration the head position of the flying bee. All the cells studied (except those in the frontal part of the eye) looked upwards in directions close to the zenith (Fig. 2). 3. The UV-cells of the dorsal rim area exhibit high polarizational sensitivities (PS). The actual PS values depend on the amount of coupling between UV- and green-cells (Fig. 5a): UV-cells having relative green-sensitivities of >10% exhibit an average PS of 3.8; if the green-sensitivity is <10% it is 5.6 and rises to more than 10 for cells which either do not respond or hyperpolarize to green light. The overall average PS is 6.6. In marked contrast to this finding, most UV-cells in the remainder of the eye (in twisted retinulae) have PS <2.0 (Fig. 5b). 4. Polarizational sensitivities of green-cells are only slightly higher in the dorsal rim area (PS =1.8) than in the other parts of the eye (PS=1.3) (Fig 5c, d). 5. By measuring the direction of maximal sensitivity to the e-vector of linearly polarized light (Φmax), two populations of UV-receptors have been found in the dorsal rim area; theirΦmax values differ by 90° (Fig. 6). 6. Angular sensitivity functions having unconventional shapes are measured in most receptors of the dorsal rim area. They show a relatively narrow peak in the center and a wide, flat brim in which the average sensitivity decreases from 8% at 7° off axis to 2% at 30° (Fig. 3b, d; 7). If UV-cells having this type of visual field are tested with off-axial (20–30°) stimuli, PS is still high andΦmax is the same as for on-axial stimulation. Thus, the UV-cells of the dorsal rim area are wide-field e-vector analyzers. Apparently, the wide visual fields are caused by corneal specializations in that part of the eye. Control experiments in other parts of the eye confirm the narrow visual fields as they have been described by former authors (Fig. 3a, c). 7. The results are discussed in the light of recent behavioral and anatomical investigations on polarization vision. It is concluded that e-vector detection in the honeybee is performed mainly by the UV-receptors of the dorsal rim area.