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Neural integration in the first optic neuropile of dragonflies

I. Signal amplification in dark-adapted second-order neurons

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Summary

  1. 1.

    The responses of retinula cells and large monopolar cells (LMC's) to axial light flashes were recorded intracellularly in dark-adapted dragonflies (Figs. 1 and 4).

  2. 2.

    LMC's respond to retinal illumination with a triphasic graded hyperpolarisation whose amplitude and waveform is intensity dependent. An initial hyperpolarising “on” transient is followed by a smaller amplitude sustained plateau. A rapid positive going “off” transient follows the cessation of the stimulus. Intensity is encoded as hyperpolarisation amplitude for action potentials are not recorded in these cells.

  3. 3.

    Measurements of the difference between LMC and retinula response latency (2 msec, Fig. 6) and the LMC angular sensitivity (Fig. 7) confirm the previous anatomical studies suggesting that the LMC's are post-synaptic to retinula axons and receive their major input from axons with the same fields of view.

  4. 4.

    Comparison of retinula and LMC response/intensity functions (Fig. 2) suggests that the visual signal is amplified when it is transferred from the retinula cell soma to a LMC.

  5. 5.

    The derivation of average normalised response/intensity functions (Fig. 3) leads to an estimation of gain during the transfer of the LMC “on” transient and plateau amplitudes (Fig. 8). Their maximum values are times 14 and times 12, respectively.

  6. 6.

    The possible mechanisms for producing amplification at this level in the visual system are discussed together with the significance of amplification in terms of the performance of the visual system.

  7. 7.

    The synaptic noise level in the LMC's is high, from 4.2% to 15.6% of the maximum response amplitude with an average value of 8.6%. It is shown that this is equivalent to a receptor signal of 400 μV at threshold. It is proposed that the high noise level is the result of multiple synapses. It is shown that multiple synapses increase the visual signal: synaptic noise ratio in proportion to the square root of the number of synapses, in a manner analagous to a signal averager.

  8. 8.

    It is concluded that the retinula-LMC pathway acts, in thedark-adapted state as a high sensitivity detection system, and shows several adaptations to maximise the signal:noise ratio.

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Authors and Affiliations

  1. Department of Neurobiology, The Australian National University, Canberra

    Simon B. Laughlin

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  1. Simon B. Laughlin
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Additional information

I am deeply indebted to Rainer Geppert who caught many of the dragonflies used in this study and whose knowledge of the local ecology ensured their constant supply. I am also grateful to Dave Cameron and Bob Fox and the staff of the Forest Research Institute, Darwin, for providing me with laboratory facilities there. I would like to thank my supervisors: Professor G. A. Horridge, for his encouragement and guidance, and Professor Randolf Menzel for many fruitful discussions arising out of the preparation of this paper. Finally I must thank Dr. R.B. Northrop who has made available to me his multiplicative model to explain anomalous acuity in locust and has verified the synaptic noise reduction model by providing a similar but more rigorous proof.

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Laughlin, S.B. Neural integration in the first optic neuropile of dragonflies. J. Comp. Physiol. 84, 335–355 (1973). https://doi.org/10.1007/BF00696346

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  • DOI: https://doi.org/10.1007/BF00696346

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