Summary
-
1.
The impulse-response was used to measure the dynamics of the photoresponse of 8 species of insects from 6 orders in both light- and dark-adapted states.
-
2.
The impulse-responses of all cells were well fitted by the two-parameter log-normal curve.
-
3.
In the dark-adapted state, the time-to-peak of the response varies from 38 ms in the drone-fly to 55 ms in the locust. Though interspecies variation is small, the house-flyMusca (41 ms) is significantly faster than the locust. In the light-adapted state, there are highly significant variations in the time-to-peak between species. The order is: housefly (12.0 ms), drone-fly (16.5 ms), dragonfly (17.5 ms), mantid (18.1 ms), locust (21.9 ms) and cricket (22.1 ms). This variation in speed correlates with flight behavior.
-
4.
There are significant, though small, differences in the shape of the dark-adapted impulseresponse, with that of the cockroach more symmetrical and the dragonfly more skew than the others. The impulse-response of the fly in the lightadapted state is more symmetrical than that of the other species and results in an even higher frequency response.
-
5.
Despite these differences in shape, it is concluded that all species have a similar transduction mechanism. Interspecies differences in time-scale can, at first approximation, be accounted for by the change of a single time-constant.
-
6.
The insects' impulse-responses were compared to those of verbrates by using the cascade models of Fuortes and Hodgkin (1964) and Baylor et al. (1974). A large number of stages were required (between 10 and 50) and a greater than 50% variation in the number of stages was needed in order to fit response from different cells within a single species. Furthermore, the basic assumption of Fuortes and Hodgkin (1964) that the timecourse is causally linked to the gain does not hold in the insect. We conclude that no first-order system of chemical cascades can sensibly predict either the time-course of the photoresponse in insects, or the effects of light adaptation and hence that the insect transduction mechanism is fundamentally different to that of vertebrates. Finally, we find that a model using two first order poles, two underdamped second order poles and a pure time delay (French 1980a, b) provides as good a fit to the frequency response as does the log-normal model.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Autrum H (1950) Die Belichtungspotentiale und das Sehen der Insekten (Untersuchungen anCalliphora undDixippus). Z Vergl Physiol 32:176–227
Autrum H (1958) Electrophysiological analysis of the visual systems in insects. Exp Cell Res [Suppl] 5:426–439
Baylor DA, Hodgkin AL, Lamb TD (1974) The electrical responses of turtle cones to flashes and steps of light. J Physiol (London) 242:685–727
Bertrand D, Fuortes MGF, Pochobradsky J (1978) Actions of EGTA and high calcium on the cones in the turtle retina. J Physiol (London) 275:419–437
Borsellino A, Fuortes MGF, Smith TG (1965) Visual responses inLimulus. Cold Spring Harbor Symp Quant Biol 30:429–443
Dubs A (1981) Non-linearity and light adaptation in the fly photoreceptor. J Comp Physiol 144:53–59
Dubs A, Laughlin SB, Srinivasan MV (1981) Single photon signals in fly photoreceptors and first order interneurons at behavioural threshold. J Physiol (London) 317:317–334
French AS (1980a) Phototransduction in the fly compound eye exhibits temporal resonances and a pure time delay. Nature 283:200–202
French AS (1980b) The linear dynamic properties of phototransduction in the fly compound eye. J Physiol (London) 308:385–401
French AS, Järvilehto M (1978) The dynamic behaviour of the photoreceptor cells in the fly in response to random (white noise) stimulation at a range of temperatures. J Physiol (London) 274:311–322
Fuortes MGF, Hodgkin AL (1964) Changes in the time scale and sensitivity in the ommatidia ofLimulus. J Physiol (London) 172:239–263
Gemperlein R, Smola U (1972) Übertragungseigenschaften der Sehzelle der SchmeissfliegeCalliphora erythrocephala. I. Abhängigkeit vom Ruhepotential. J Comp Physiol 78: 30–52
Hamdorf K, Kirschfeld K (1980) ‘Pre-bumps’: evidence for double-hits at functional subunits in a rhabdomeric photoreceptor. Z Naturforsch 35c: 173–174
Hengstenberg R (1972) Eye movements in the house-flyMusca domestica. In: Wehner R (ed) Information processing in the visual systems of arthropods. Springer, Berlin Heidelberg New York, pp 93–96
Horridge GA, Marcelja L, Jahnke R, Matic T (1983) Single electrode studies on the retina of the butterflyPapilio. J Comp Physiol 150:271–294
Howard J (1981) Temporal resolving power of the photoreceptors ofLocusta migratoria. J Comp Physiol 144:61–66
Howard J, Snyder AW (1983) Transduction as a limitation on compound eye function and design. Proc R Soc London Ser B 217:287–307
Laughlin SB (1976) The sensitivities of dragonfly photoreceptors and the voltage gain of transduction. J Comp Physiol 111:221–247
Laughlin SB (1981a) Neural principles in vision. In: Autrum H (ed) Vision in invertebrates (Handbook of sensory physiology, vol VII/6B). Springer, Berlin Heidelberg New York, pp 133–280
Laughlin SB (1981b) A simple coding procedure enhances a neuron's information capacity. Z Naturforsch 36c:910–912
Leutscher-Hazelhoff JT (1975) Linear and non-linear performance of transducer and pupil inCalliphora retinula cells. J Physiol (London) 246:333–350
Lillywhite PG (1977) Single photon signals and transduction in an insect eye. J Comp Physiol 122:189–200
Matthews G, Baylor DA (1981) The photocurrent and dark current of retinal rods. In: Miller WH (ed) Current topics in membranes and transport. vol. 15: Molecular mechanisms of photoreceptor transduction. Academic Press, New York, pp 3–18
Menzel R, Blakers M (1976) Colour receptors in the bee eye: Morphology and spectral sensitivity. J Comp Physiol 108:11–33
Muijser H (1979) The receptor potential of retinula cells of the blowflyCalliphora: the role of sodium, potassium and calcium ions. J Comp Physiol 132:87–95
Payne R (1981) Chemical modifications of transduction in an insect eye. PhD thesis. Australian National University
Payne R, Howard J (1981) Response of an insect photoreceptor: a simple log-normal model. Nature 290:415–416
Pinter RB (1972) Frequency and time domain properties of retinula cells of the desert locust (Schistocerca gregaria) and the house cricket (Acheta domesticus). J Comp Physiol 77:383–397
Rossel S (1979) Regional differences in photoreceptor performance in the eye of the praying mantis. J Comp Physiol 131:95–112
Scholes JH (1964) Discrete subthreshold potentials from the dimly lit insect eye. Nature 202:572–573
Smola U, Gemperlein R (1972) Übertragungseigenschaften der Sehzelle der SchmeissfliegeCalliphora erythrocephala. 2. Die Abhängigkeit vom Ableitort: Retina-Lamina ganglionaris. J Comp Physiol 79:363–392
Snyder AW (1977) Acuity of compound eyes: physical limitations and design. J Comp Physiol 116:161–182
Srinivasan MV, Bernard GD (1975) The effect of motion on visual acuity of the compound eye: a theoretical analysis. Vision Res 15:515–525
Zettler F (1969) Die Abhängigkeit des Übertragungsverhaltens von Frequenz und Adaptationszustand, gemessen am einzelnen Lichtrezeptor vonCalliphora erythrocephala. Z Vergl Physiol 64:432–449
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Howard, J., Dubs, A. & Payne, R. The dynamics of phototransduction in insects. J. Comp. Physiol. 154, 707–718 (1984). https://doi.org/10.1007/BF01350224
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01350224