Dichroism and absorption by photoreceptors

Summary

Photoreceptor membrane is dichroic, i.e. its absorption depends on the direction of the electric vectorE of linearly polarised light. Dichroism depends on the arrangement and packing of the membrane (form dichroism) in addition to the orientation and dichroic properties of the chromophores associated with the membrane (intrinsic dichroism).

• 1. The amount of light absorbed by a photoreceptor depends on the orientation of the dipoles within its membrane. There is an optimum orientation for the photoreceptor to have a maximum absolute sensitivity tounpolarised light andthis orientation depends on the photoreceptor structure. In both vertebrate discs and fly rhabdomeres 1 to 6, the optimum dipole orientation is a random alignment within the plane of the membrane; while in fused rhabdoms the dipoles must be highly aligned with the microvillus axis for maximum absolute sensitivity to unpolarised light. Measurements of dichroism indicate that this optimum dipole orientation is indeed present in vertebrate outer segments, fly rhabdomeres 1 to 6 and the crustacean rhabdom. This furnishes strong evidence for the view that dipoles are orientated in the plane of the membrane to provide the majority of photoreceptors with maximum absolute sensitivity to unpolarised light. Membrane dichroism is only a secondary consequence of this objective [See Section VII].

• 2. The measured side-on dichroism of vertebrate outer segments is shown to represent aproduct of form and intrinsic dichroism, where the form factor is approximately 1.6. MSP measurements must be corrected for form dichroism to obtain the intrinsic dichroism.

• 3. An extremely simple derivation is given for the dichroism of microvilli (rhabdomeric photoreceptor) membranes in which each miorovillus is treated as if constructed from 4 vertebrate outer segment discs. The analysis accounts for both form and intrinsic dichroism.

• 4. The dichroic ratio of microvilli is estimated using contemporary knowledge of membrane and its associated chromophores. We find that the long (dipole) axis of the chromophore shows preferential axial alignment whenever the dichroic ratio of microvilli exceeds 1.67 to 1. This is to be contrasted to the value of 2 to 1 determined from the ideal (but unrealizable) model of Moody and Parriss (1962). An alignment of about 17° with the microvillus axis gives a dichroism of about 10 to 1 while perfect alignment gives 20 to 1.

• 5. We propose that the microvillus is fluid membrane rolled into a cylindrical shell. The bending causes the preferential dipole alignment when the rhodopsin molecule is asymmetrical in the membrane plane; a spherical molecule is associated with random dipole orientation in thecunved microvillus. Thus, the shape of the rhodopsin molecule is postulated to be asymmetric in crustacea and spherical in fly 1–6 microvilli.