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Coupling between locust photoreceptors revealed by a study of quantum bumps

Summary

  1. 1.

    Very dim illumination was used to elicit responses from dark-adapted photoreceptors of the compound eye of the locust (Locusta migratoria). Light intensities which deliver only a few photons per second per eye facet elicit waves of membrane depolarisation called bumps. These bumps are easily distinguished as discrete responses because of their large size (1 to 10 mV) and are here called L (Large) bumps.

  2. 2.

    Besides these L bumps, there is an additional voltage response during illumination which appears as an increase in membrane voltage noise. The additional voltage response can be resolved into small discrete depolarisations called S (Small) bumps. These S bumps are both slower in time course and of smaller amplitude than L bumps.

  3. 3.

    S bumps have the same statistical properties as L bumps. During constant illumination they are distributed randomly in time according to the Poisson distribution and increase in frequency linearly with the number of photons hitting the eye. S and L bumps are statistically independent of each other in time. However, S bumps occur about twice as frequently as L bumps. The mutual independence of all bumps (S and L) seen in any one cell, and their frequency relative to incident photons, restricts the set of hypotheses which could account for the origin of S bumps.

  4. 4.

    The spectral and polarisation sensitivities of L and S bumps and larger receptor potentials were compared as the results were bound to restrict the possible explanations of the origin of S bumps. The Polarisation Sensitivity (PS) Curves for L and S bumps are different in magnitude and phase. The PS of L bumps is larger than that of S bumps and the PS Curve shifted by, on average, 30° relative to the PS Curve of S bumps.

  5. 5.

    S bumps are responses from electrically coupled cells, i.e. they are passively conducted L bumps produced in cells neighboring the one being recorded from. This hypothesis explains the PS data and the statistical data. Furthermore, this hypothesis predicts the size and time-course of S bumps.

  6. 6.

    The relative maximum amplitudes of S and L bumps provide a measure of the degree of interreceptor coupling. However, some cells do not exhibit clear S bumps at all. Where S bumps were apparent, the ratio (S amplitude/L amplitude) varied from 0.14 to 0.25 in most cells, but reached a value of 0.30 to 0.35 in 2 out of 20 cells tested.

  7. 7.

    Two cell types with single-peaked spectral sensitivities compatible with Dartnall Nomograms are for the first time described in the locust eye. By combining varying ratios of these two rhodopsin types, a family of broad spectral sensitivity types can be constructed to which all other observed spectral sensitivity types can be fitted.

  8. 8.

    The spectral sensitivities of L bumps, S bumps and larger receptor potentials were identical in the cells tested. As these cells had broad spectral sensitivities, it is concluded that this broadness is due to the presence of two or more photopigments in the one cell.

  9. 9.

    The Bump-Amplitude Distribution is invariant with the wavelength of light stimulus. This means that where two or more photopigments are present in one cell, the gain of phototransduction is identical for each. This is essential if intrinsic noise in the photoreceptor is to be minimized.

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Additional information

I thank Drs. S.B. Laughlin and S.R. Shaw for useful discussions. The recording of bumps from the eye of a mantis was made jointly with Sam Rossel.

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Lillywhite, P.G. Coupling between locust photoreceptors revealed by a study of quantum bumps. J. Comp. Physiol. 125, 13–27 (1978). https://doi.org/10.1007/BF00656827

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Keywords

  • Spectral Sensitivity
  • Light Stimulus
  • Membrane Voltage
  • Intrinsic Noise
  • Voltage Noise