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Field potential analysis and the physiology of second-order neurons in the visual system of the fly

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Summary

The extracellular standing voltage in the eye and optic lobe of the dark-adapted fly was measured in conjunction with dye-marking techniques. A peripheral extracellular voltage drop of up to −55 mV is located in the synaptic region of the lamina ganglionaris. A larger, more proximal voltage of as much as −70 mV is located in the medulla. Analysis indicates that these regions correspond to current sinks. A hypothesis is proposed that the dark current sink in the lamina is produced by tonic depolarization of the second-order monopolar neuron by synaptic input from cells other than the photoreceptors. The effect of the dark depolarizing input is to increase the dynamic range of the hyperpolarizing light response of the second-order cell.

The resistance of the extracellular current paths in the fly eye and optic lobe was examined by direct measurement. Perfusion of flies with a tracer that demonstrated the relative accessibility of the tissues to the general circulation showed a correspondence with tissue resistance measurements. These experiments show that the synaptic layer of the lamina is a region of high resistance, and that it is bounded by regions of relatively low resistance, which are shunted to the general circulation. This is consistent with the effects of high magnesium concentrations on the focal electroretinogram recorded in the lamina, which suggest that the synaptic conductances form a significant return path for extracellular current. In agreement with Shaw, it is suggested that whether the low resistance shunt to the general circulation is distal or proximal to the lamina in a given species determines whether the corneal electroretinogram is simple and monophasic or also includes prominent on and off-transients.

Pharmacological experiments were performed during intracellular recordings from the laminar second-order monopolar neurons of the fly,Phormia regina. The average dark resting potential with respect to the cornea was −48±2 mV (mean±standard error of the mean,N=58).

The hyperpolarizing response to light is accompanied by a decrease in input resistance. Both the on-transient and the plateau potential can be reversed by applied currents that further hyperpolarize the cell, indicating reversal potentials negative to the dark resting potential. The response to light can be reduced or abolished by intracellular injection of tetraethylammonium (TEA), indicating that the hyperpolarizing potential is mediated by an increase in potassium conductance.

When synaptic transmission is blocked by high extracellular concentrations of magnesium or cobalt, the dark resting potential or the second-order monopolar neuron is hyperpolarized and the response to light is reduced. Application of picrotoxin or bicuculline, agents which block transmission at GABAergic synapses, also hyperpolarize the dark resting potential and reduce the light response of the second-order monopolar neuron. These experiments support the hypothesis that the second-order monopolar neuron is tonically depolarized in the dark and suggest that the transmitter at this synapse may be gamma-aminobutyric acid.

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Additional information

Dr. Timothy H. Goldsmith has encouraged and supported this work through all stages. His critical comments on the manuscript were much appreciated. This paper is based on a dissertation submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy at Yale University. Dr. Robert De Voe read the dissertation and made many useful suggestions, Dr. Bertram Sacktor kindly provided thePhormia mutants. Supported by a NSF Predoctoral Fellowship and NIH research grand USPHS EY 00222 to Dr. Timothy H. Goldsmith.

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Zimmerman, R.P. Field potential analysis and the physiology of second-order neurons in the visual system of the fly. J. Comp. Physiol. 126, 297–316 (1978). https://doi.org/10.1007/BF00667100

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Keywords

  • Bicuculline
  • Picrotoxin
  • Optic Lobe
  • Synaptic Conductance
  • GABAergic Synapse