Single electrode studies on the retina of the butterfly Papilio

Abstract

Summary 1. The butterfly retina exhibits strong interactions between photoreceptor responses recorded intracellularly. In general, the receptor which is locally giving the largest response suppresses the responses of neighbouring receptors that are less strongly stimulated. The effect enhances the differences between the primary photo-receptors and reduces responses to stimuli that excite all receptors together.

2. The interaction is explained in terms of a high extracellular resistance, so that receptor currents pass through other receptors in the opposite direction to those of their own responses. The result is that receptors are actively turned off by colours away from their own peak wavelength.

3. This effect applies most strongly to colour and to polarization plane when the stimulus is a point source on axis, and is therefore strong between the receptors of the same ommatidium.

4. The result is that spectral sensitivity peaks and angular sensitivity peaks are narrower, and polarisation sensitivity is greater, than expected from single retinula cells in isolation. The sensitivities measured electrophysiologically cannot be easily related to the physical properties of the visual pigments. Polarisation sensitivity (PS) can reach 50.

5. There are four types of primary photoreceptor, with peak near 380 nm, 450 nm, 550 nm and 610 nm. Cell marking usually reveals these as single retinula cells. Near the peak spectral sensitivity the responses are up to 60 mV positive-going, but away from the peak they can be negative-going.

6. Anatomically the retina ofPapilio has four distal, four proximal retinula cells, and a ninth basal cell. Narrow pigment cells and tracheoles squeeze through the substantial basement membrane along with each bundle of nine axons.

7. Two of the distal retinula cells contain red pigment grains near the rhabdom. The distal retinula cells are UV or blue sensitive. Green sensitive cells are proximal and can be coupled in opposite pairs. Red sensitive cells are proximal.

8. The UV sensitive cell with peak near 380 nm is the most sensitive of the cell types when measured by the position of theV/logI curve on the intensity axis at the spectral peak of each type. The red-sensitive cells are also sensitive. By its inhibitory effect, interaction between receptors reduces the sensitivity measurement on this scale.

9. Angular sensitivities measured with positive-going responses near the spectral peaks are narrow (Δρ-2°); when measured with negative-going responses they are wider (Δρ=3° to 5°).

10. One type of unit has only negative-going responses to −60 mV, with Δp=2° to 5°, spectral peak near 550 nm and sometimes also 380 nm or 450 nm. This type has not been marked and is regarded as a restricted channel for return current. ItsV/logI curve extends over an intensity range of 106.

11. The variety of the units suggests that their responses are not due to a simple regular network with all units connected indiscriminately to all others at all times through their terminals. There are selective channels for current flow and some retinula cells appear to be little influenced by others.

12. Theory shows that when there is a direct electrical coupling between a pair of retinula cells (not passing through the extracellular space) it is possible to balance out the negative interactions caused by current flow through their terminals. Far from degenerating the signals, direct electrical coupling can cancel the negative interaction, and this may be its normal function.