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Neural integration in the first optic neuropile of dragonflies

III. The transfer of angular information

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Summary

  1. 1.

    The transfer ofangular sensitivity from photoreceptors (retinula cells) to second order neurons (large monopolar cells — LMC's) is investigated by means of intracellular recordings from the retina and lamina ofHemicordulia tau. Angular sensitivity is measured by using a single point light source in two different ways. In the first, the constant intensity test flash method, responses to test flashes delivered at different angles of incidence are compared with the axial intensity/response function of the unit (Pig. 1). In the second, the off-axis intensity/ response function method, complete LMC intensity/response functions are derived at a number of angular inclinations toaxis (defined as the point of maximum sensitivity within the unit's visual field) (Fig. 4, 5).

  2. 2.

    The constant intensity test flash method shows that dragonfly retinula cells have a high angular sensitivity when compared to other insects. The horizontal and vertical acceptance angles are 1.46°±0.44 and 1.31°±0.23 respectively. Application of this same method to LMC's demonstrates that they retain retinal acuity for their angular sensitivity functionsappear to be the same as those of retinula cells (Pig. 2, Table 1).

  3. 3.

    The off-axis intensity/response functions show that the shape of the triphasic LMC response waveform depends upon the angular inclination of the stimulus to axis. The relative amplitudes of “on” transient and plateau (Pig. 3) vary independantly with angle (Pig. 4). The slope of the plateau response/log intensity curve decreases as the stimulus moves off axis but the “on” transient curve's slope remains relatively constant (Pig. 5).

  4. 4.

    Constant intensity test flash methods cannot measure LMC angular sensitivity because the slope of the response/log intensity curves depend upon stimulus inclination. The off-axis intensity/response function method shows that lateral inhibition narrows the LMC visual fields (Fig. 6) and angular sensitivity is increased during the transfer of visual information (Pig. 7).

  5. 5.

    Examination of the LMC response waveform (Fig. 8) and the intensity/response characteristics (Fig. 5) shows that two types of inhibition shape the response to square wave stimuli. Intracartridge inhibition acts at the level of the first synapses to attenuate the response to maintained stimuli. Intercartridge inhibition acts with a time delay to depolarise the LMC membrane and increase angular sensitivity.

  6. 6.

    It is concluded that LMC's integrate retinal input by acting as high sensitivity detectors of contrast differences within the spatial domain. Their role as an input to the visual system is discussed in relationship to visual behaviour and its experimental analysis.

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Authors and Affiliations

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

    Simon B. Laughlin

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  1. Simon B. Laughlin
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Additional information

During the preparation of this and the previous paper many people gave freely of their time and expertise. My supervisors Professors G. A. Horridge and Randolf Menzel guided and encouraged me, Margaret Blakers expertly processed much of the raw experimental data and Mike Bate and Mark Leggett made sense of the original manuscripts. Finally I would like to thank Professor Kuno Kirschfeld for his constructive suggestions on the presentation and interpretation of these results.

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Laughlin, S.B. Neural integration in the first optic neuropile of dragonflies. J. Comp. Physiol. 92, 377–396 (1974). https://doi.org/10.1007/BF00694708

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  • DOI: https://doi.org/10.1007/BF00694708

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