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First published online October 18, 2006
Journal of Experimental Biology 209, 4262-4272 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02499

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Electrophysiological evidence for linear polarization sensitivity in the compound eyes of the stomatopod crustacean Gonodactylus chiragra

Sonja Kleinlogel^* and N. Justin Marshall

Vision Touch and Hearing Research Centre, School of Biomedical Sciences, University of Queensland, Brisbane QLD 4072, Australia

View larger version (24K): [in a new window]   Fig. 1. Preparation. (A) The isolated apposition compound eye was mounted on a plastic rod with the aid of low melting point bee's wax/dental wax and placed into a glass bubble filled with saline so that the mid-band was oriented horizontally. The intracellular electrode was lowered through a small hole cut into the cornea of the dorsal (or ventral) hemisphere. (B) Frontal view of a left eye of Gonodactylus chiragra mounted as in A. The eye is divided into a dorsal and a ventral hemisphere by an equatorial mid-band formed by six rows of enlarged ommatidia. The mid-band rows are numbered 1 to 6 from dorsal to ventral. Ommatidia in rows 1-4 belong to type II, whereas ommatidia in rows 5 and 6 belong to type I (see Fig. 2). D, dorsal; V, ventral; L, lateral; M, medial. Scale bar, 1 mm.

View larger version (37K): [in a new window]   Fig. 2. The two rhabdom types within the retina. Type I (left) is found in mid-band rows 5 and 6 and both hemispheres, whereas type II (right) is only found in MB rows 1-4. Each rhabdom has a distally placed eighth retinula cell (R8) that overlies the main rhabdom composed of microvilli from retinula cells 1-7 (R1-R7). The R1-R7 cells are divided into two groups (Group I and Group II). In type I rhabdoms, R1-R7 contribute to the entire length of the main rhabdom and Group I (R1, R4, R5) and Group II (R2, R3, R6, R7) cells form mutually perpendicular, regular layers of microvilli. (A,B) Longitudinal electron microscopic sections through the main rhabdoms. (A) A row 5 rhabdom, which has very thin layers (5-6 microvilli deep) of orthogonal microvilli. In type II rhabdoms, the R1-R7 form two separate rhabdomal tiers, a distal (D) and a proximal (P) tier. The type II rhabdom is therefore three-tiered. In rows 1, 2P, 3 and 4 the microvilli within the rhabdoms are unordered, because each retinula cell produces microvilli in both orthogonal directions. (B) Rhabdom 2D is an exception. Here the four cells forming the rhabdom are also divided into 2 subgroups (R2, R6 and R3, R7), which form orthogonal layers of microvilli. However, the microvillar layers are about three times thicker (16-17 microvilli deep) than the layers found in rows 5 and 6. Scale bars, 2 µm.

View larger version (22K): [in a new window]   Fig. 3. (A) Comparison of the e-vector angle-response amplitudes of a colour receptor (row 4P R6), a hemispheric receptor (DH R1) and a `high PS cell' (row 2D R2). All photoreceptors shown here possess similar response amplitudes to unpolarized white light, and nearly parallel response-intensity (R-log I) functions. They are all most sensitive to an e-vector orientation of linearly polarized light (max) of approximately +45°. (B) Intracellular recordings of the e-vector angle-response curves of two neighbouring photoreceptors (R3 and R4) within row 5. The two cells possess 90° phase-shifted max (max(R4)=+45° and max(R3)=-45°). Slight re-positioning of the microelectrode after completing the recording and staining of the first cell (R3) resulted in a 90° phase-shift of max. Subsequent Lucifer Yellow injection showed that the microelectrode tip had moved from R3 into the neighbouring retinula cell R4. R4 belongs to Group I and R3 to Group II cells amongst R1-R7, and they have their microvilli arranged at right angles. (C) To determine the polarization sensitivity of a photoreceptor, two R-log I curves were recorded at max and min, respectively. In this example, the intensity shift (i) of 0.72 log units between the linear parts of the two fitted standard Rushton intensity-response functions corresponds to a polarization sensitivity of 5.2.

View larger version (33K): [in a new window]   Fig. 4. (A) Photomicrograph of the mid-band region of the cornea. `High PS cells' are found within rows 2D, 5 and 6. (B) 7 µm frontal section through the retina showing a dye-filled R8 cell of the dorsal hemisphere (DH) and a R6 cell of row 2D. (C) Diagrams of the arrangement of retinula cells R1-R7 in rows 2D, 5 and 6 in a right eye (frontal view). Group I retinula cells are stippled and Group II retinula cells are plain. Note that the cell arrangement in row 6 is twisted 90° counterclockwise compared to row 5 as identified by the R8 axon position, the dark spot. (D) Preferred e-vector orientations (max) of the two retinula cell groups (Group I and Group II). The max of the two cell groups are perpendicular and coincide with the microvillar orientations within the corresponding photoreceptors. Row 2D (distal rhabdomal tier) is formed by only four retinula cells, which are also divided into two cell groups sensitive to orthogonal max (R2, R6 and R3, R7). See Marshall et al. (Marshall et al., 1991a) for anatomical details.

View larger version (13K): [in a new window]   Fig. 5. Histograms of polarization sensitivity values (PS). (A) UV receptors (R8 cells) with PS <2 (N=17); (B) colour receptors within rows 1, 2P, 3, 4 [PS=2.3±2 (s.d.), N=22]; (C) hemispheric receptors (ventral and dorsal hemispheres) with a `typical crustacean' design (PS=3.8±1.6, N=17); and (D) `high PS cells' within rows 2D, 5, 6 (PS=6.1±2, N=14). The PS of `high PS cells' is significantly higher than that of hemispheric receptors (t-test, P<0.005).

View larger version (31K): [in a new window]   Fig. 6. Averaged spectral sensitivity curves (±s.d.) of polarization sensitive photoreceptors from different eye regions in Gonodactylus chiragra. Ventral hemisphere (VH; A) and dorsal hemisphere (DH; B) receptors have broad spectral sensitivity curves with two maxima and similar overall sensitivity. The spectral sensitivity curves of 2D receptors (C) and row 5 and 6 receptors (D), which are in this study grouped together as `high PS cells', have very similar, narrow sensitivity curves with a bandwidth of less than 100 nm, peaking at around 565 nm. Only the spectral sensitivities of stained cells were averaged in C and D in order to avoid the incorrect inclusion of a cell with different identity.