Vertebrate detection of polarized light




Novales Flamarique, Inĩgo
Novales Flamarique, Inĩgo

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In addition to intensity and colour, the retinas of many invertebrates are capable of light detection based on its linear polarization (Wehner, 1983). The detection mechanism permitting this capability is based on the intrinsic dichroism of chromophores oriented along rhabdomeric microvilli. In vertebrates, however, except for anchovies (Fineran & Nicol, 1978), such axial dichroism is absent rendering vertebrate outer segments insensitive to the polarization of axially incident light. Nonetheless, there is evidence for polarization sensitivity in a few species of fish (goldfish, rainbow trout and sunfish). But the findings for goldfish and rainbow trout appear contradictory to those for the green sunfish (Parkyn & Hawryshyn, 1993), and a detection mechanism that could explain polarization sensitivity for lower vertebrates in general is unknown. This thesis was undertaken to try to solve some of these unknowns by investigating: 1) the neural polarization signal, at the level of the optic nerve, in fish species from four groups with distinct retinal cone mosaics (rainbow trout, green and pumpkinseed sunfishes, common white sucker, and northern anchovy), 2) the ultrastructure and light transmission properties of different cone types (single, twin and double cones) , and 3) the characteristics of the underwater polarized light field that could permit the observed laboratory behaviours in nature. I measured compound action potential (CAP) responses from the optic nerve of live anaesthetized fish to evaluate the possibility that a fish could detect the orientation of the electric field of linearly polarized light (mathematically-designated as the E-vector) . Results from these studies showed that rainbow trout and the northern anchovy were polarization-sensitive, but both species of sunfish and the common white sucker were not. In addition, CAP measurements conducted with rainbow trout exposed to light stimuli of varying polarization percentages showed, in conjunction with underwater polarized light measurements, that the use of polarized light in this animal was restricted to crepuscular time periods. To try to understand why some fish species were polarization-sensitive and others were not, I carried out microscopy studies of retinal cones. Optical measurements of transmitted polarized light through the length of cones showed: 1) small cone birefringence (retardance < 2nm) , and 2) preferential transmission of polarized light that was parallel to the partition dividing twin and double cones (single cones were isotropic). In addition, histological studies showed that the partition in trout double cones was tilted with respect to the vertical while that of twin cones in sunfish was straight. We envisioned that the higher index of refraction of the partition with respect to the surrounding cell cytoplasm would make it behave as a mirror, reflecting and polarizing incident light. A large optical model was built to test this idea consisting of two photodiodes evenly spaced on either side of a cover-slip "partition" upon which physiologically-relevant illumination was incident. Measurements using this model and theoretical calculations with refractive indices approaching those expected for double cone partitions and cytoplasm (Sidman, 1957) were consistent with the optical results obtained in situ. Thus the tilt in the partition of trout double cones relayed different amounts of light to each outer segment depending on the polarization of incident light, whereas a straight partition, as in sunfish, did not. Comparison of signals from orthogonally-arranged double cones and single cones in the centro-temporal retina of trout thus became the basis for a model neural network that could reproduce all the polarization sensitivity results known to date. To support the idea that an ordered (e.g. orthogonal) arrangement of double cones was a necessity for polarization detection, I showed that the common white sucker, a fish with double cones, had these arranged randomly in the centro-temporal retina (hence its lack of polarization sensitivity). Finally, the northern anchovy exhibited unique cones with lipid lamellae parallel to their lengths, forming a dichroic system for polarization detection somewhat analogous to that of cephalopods and decapod crustaceans.



Fishes, Light, Vertebrates