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Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly

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Summary

  1. 1.

    Intracellular recordings from photoreceptors and large monopolar cells (LMC's) of the flyCalliphora stygia, and the dragonflyHemicordulia tau, were used to examine the peripheral light adaptation processes of the insect compound eye.

  2. 2.

    Photoreceptor and lamina adaptation mechanisms were separated by comparing the response waveforms and intensity/response functions (plotted as V/log I curves) of receptors (Figs. 1 and 3) and LMC's (Figs. 2 and 4), subjected to identical regimes of adaptation.

  3. 3.

    Photoreceptor adaptation occurs in two phases, a rapid one lasting 100 ms, and a slow phase taking up to 60 s to complete (Fig. 1). This adaptation shifts theV/logI curves to higher intensities without changing their shape or slope (Fig. 3). Adaptation is negligible at low intensities but with stronger adaptation range sensitivity changes approach proportionality to background increments (Fig. 7).

  4. 4.

    Lamina adaptation mechanisms adjust the LMCV/logI curve in response to new background levels within 200 ms, producing a phasic response waveform within which background signals are annihilated (Figs. 1, 3, 8). The shape and amplitude of the saturated LMC ‘on’ and ‘off’ transient responses change with light adaptation (Figs. 2, 3).

  5. 5.

    At all background intensities examined the slopes of the LMC V/log I curves remain about 8–10 times that of the photoreceptors under the same conditions, implying that lamina adaptation does not change the voltage gain of the first synapse. We propose that light induced depolarisation of the lamina extracellular space subtracts away the standing background signal from the photoreceptor terminals.

  6. 6.

    During dark adaptation the faster lamina mechanism can be superimposed upon slower photoreceptor processes (Fig. 9).

  7. 7.

    A comparison of our findings with studies of higher order neurons of the compound eye suggests that peripheral adaptation mechanisms play an important role in determining the response of the entire visual system.

  8. 8.

    The peripheral light adaptation processes of fly and dragonfly are similar, and the intensity/response functions of retinula cells and LMC's resemble those of vertebrate cones and bipolar cells respectively (Fig. 11). We propose that this analogy has a functional basis. Both vertebrate and invertebrate systems use a ‘log transform-subtraction-multiplication” strategy to match the response bandwidth of peripheral neurons to the expected intensity fluctuation about any one mean, and in so doing maximise the image detail sent to higher centres.

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Abbreviations

R1–6 :

The six peripheral receptors in a fly's ommatidium

LMC :

Large monopolar cell

L1 and L2 :

Two subclasses of LMC's

DCMD :

Descending contralateral motion detector-a command interneuron in the locust

S/N :

Signal to noise ratio

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Thanks to Steve McGinness for technical assistance, Pam Coote for typing, Sandy Smith for preparing the figures and Kevin Downing for maintaining our equipment. Martin Wilson and Steve Shaw have contributed to the interpretation and formulation of our results.

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Laughlin, S.B., Hardie, R.C. Common strategies for light adaptation in the peripheral visual systems of fly and dragonfly. J. Comp. Physiol. 128, 319–340 (1978). https://doi.org/10.1007/BF00657606

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