Microvillar Components of Light Adaptation in Blowflies

The process o f light adaptation in blowfly photoreceptors was analyzed using intracellular recording techniques and double and triple flash stimuli. Adapting flashes o f increasing intensity caused a progressive reduction in the excitability o f the photoreceptors, which became temporarily suppressed when 3 x 106 quanta were absorbed by the cell. This suppression was confirmed by subsequently applying an intense test flash that photoactivated a considerable fraction o f the 108 visual pigment molecules in the cell. The period o f temporary desensitization is referred to as the refractory period. The stimulus intensity to render the receptor cell refractory was found to be independent of the extracellular calcium concentration over a range of 10 -4 and 10 -2 M. During the refractory period (3040 ms after the adapting flash) the cell appears to be "protected" against further light adaptation since light absorption during this period did not affect the recovery o f the cell's excitability. Calculations showed that the number o f quantum absorptions necessary to induce receptor refractoriness is just sufficient to photoactivate every microvillus o f the rhabdomere. This coincidence led to the hypothesis that the refractoriness o f the receptor ceils is due to the refractoriness o f the individual microvilli. The sensitivity o f the receptor cells after relatively weak adapting flashes was reduced considerably more than could be accounted for by the microvilli becoming refractory. A quantitative analysis o f these results suggests that a photoactivated microvillus induces a local adaptation over a relatively small area o f the rhabdomere around it, which includes several tens o f microvilli. After light adaptation with an intense flash, photoactivation o f every microvillus by the absorption of a few quanta produced only a small receptor response whereas photoactivation o f every rhodopsin molecule in every microvillus produced the maximum response. The excitatory efficiency of the microvilli therefore increases with the number o f quanta that are absorbed simultaneously. I N T R O D U C T I O N In invertebrates pho to recep to r excitation takes place in highly specialized structures, the rhabdomeres , which are composed o f a hexagonal array o f microvilli (see E1-Gammal et al., 1987). Recep to r excitation is t hough t to be mediated by a bioAddress reprint requests to Dr. P. Hochstrate, Institut ftir Tierphysiologie, Ruhr-Universidit, 4630 Bochum 1, Federal Republic of Germany. J. GEN. PHYSIOL. ~) The Rockefeller University Press 9 0022-1295/90/05/0891/20 $2.00 Volume 95 May 1990 891-910 891 on Jne 5, 2017 D ow nladed fom Published May 1, 1990