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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Alawi, A.A., Pak, W.L.: On-transient of insect ERG-its cellular origin. Science172, 1055–1057 (1971)
Araki, T., Otani, T.: Response of single motorneurons to direct stimulation in toad's spinal cord. J. Neurophysiol.18, 472–485 (1955)
Ascher, P.: Inhibitory and excitatory effects of dopamine onAplysia neurones. J. Physiol. (Lond.)225, 173–209 (1972)
Atwood, M.W.: The effect of barium and TEA on the ocellar electroretinogram. J. Insect Physiol.16, 661–670 (1970)
Autrum, H., Zettler, F., Järvilehto, M.: Postsynaptic potentials from a single monopolar neuron of the ganglion opticum I of the blowflyCalliphora. Z. vergl. Physiol.70, 414–424 (1970)
Beers, Y.: Introduction to the theory of error. Reading, Massachusetts: Addison-Wesley 1957
Boschek, C.B.: On the fine structure of the peripheral retina and lamina ganglionaris of the fly,Musca domestica. Z. Zellforsch.118, 369–409 (1971)
Brecher, L.: Physiko-chemische und chemische Untersuchungen am Raupen- und Puppenblute (Pieris brassicae, Vanessa urti-cae). Z. vergl. Physiol.2, 691–713 (1925)
Brown, J.E., Muller, K.J., Murray, G.: Reversal potential for an electrophysiological event generated by conductance changes: mathematical analysis. Science174, 318 (1971)
Brown, K.T., Flaming, D.G.: Beveling of fine micropipette electrodes by a rapid precision method. Science185, 693–695 (1974)
Burtt, E.T., Catton, W.T.: The potential profile of the compound eye of the locust. J. Physiol.163, 49P-51P (1962)
Burtt, E.T., Catton, W.T.: The potential profile of the insect compound eye and optic lobe. J. Insect Physiol.10, 1689–1710 (1964)
Byzov, A., Mazohkin-Porshnyakov, G.: Analysis of insect retinograms. Biofizika8, 487–497 (1963)
Campos-Ortega, J.A., Strausfeld, N.J.: Columns and layers in the second synaptic region of the fly's visual system: The case for two superimposed neuronal architectures. In: Information processing in the visual systems of arthropods, pp. 31–36 (ed. R. Wehner). Berlin-Heidelberg-New York: Springer 1972
Chappell, R.L., Dowling, J.E.: Neural organization of the median ocellus of the dragonfly. I. Intracellular electrical activity. J. gen. Physiol.60, 121–147 (1972)
Cosens, D.J.: Extracellular potentials in the locust eye and optic lobe. J. Insect Physiol.13, 1373–1386 (1967)
Faber, D.S., Korn, H.: A neuronal inhibition mediated electrically. Science179, 575–578 (1973)
Fouchard, R., Carricaburu, P.: Analyse de l'electrorétinographique de l'insecte. Vision Res.12, 1–15 (1972)
Freeman, J.A., Nicholson, C.: Experimental optimization of current source—density technique for anuran cerebellum. J. Neurophysiol.38, 369–382 (1975)
Furukawa, T., Furshpan, E.J.: Two inhibitory mechanisms in the Mauthner neurons of goldfish. J. Neurophysiol.26, 140–176 (1963)
Goldsmith, T.H.: The nature of the retinal action potential and the spectral sensitivities of UV and green receptor systems in the compound eye of the worker honeybee. J. gen. Physiol.43, 775–799 (1960)
Good, N.E., Winget, G.D., Winter, W., Connolly, T.N., Izawa, S., Singh, R.M.M.: Hydrogen ion buffers for biological research. Biochemistry5, 467–477 (1966)
Hagins, W.A., Penn, R.D., Yoshikami, S.: Dark current and photocurrent in retinal rods. Biophysical J.10, 380–412 (1970)
Heisenberg, M.: Separation of receptor and lamina potentials in the electroretinogram of normal and mutantDrosophila. J. exp. Biol.55, 85–100 (1971)
Hille, B.: The selective inhibition of delayed potassium currents in nerve by tetraethylammonium ion. J. gen. Physiol.50, 1287–1302 (1967)
Hubbard, J.I., Llinás, R., Quastel, D.M.J.: Electrophysiological analysis of synaptic transmission. London: Edward Arnold 1969
Järvilehto, M., Zettler, F.: Electrophysiological-histological studies on some functional properties of visual cells and second-order neurons of an insect retina. Z. Zellforsch.136, 291–306 (1973)
Katz, B.: Nerve, muscle, and synapse. New York: McGraw-Hill 1966
Kehoe, J.: Ionic mechanisms of a two-component cholinergic inhibition inAplysia neurones. J. Physiol. (Lond.)225, 85–114 (1972)
Kikuchi, R., Takeda, Y.: Effect on retinal potentials of intracellularly applied tetraethylammonium ions. Naturwissenschaften53, 227–228 (1966)
Korenbrot, J.I., Cone, R.A.: Dark ionic flux and the effects of light in isolated rod outer segments. J. gen. Physiol.60, 20–45 (1972)
Kripke, B.R., Ogden, T.E.: A technique for beveling fine micropipettes. Electroencephalogr. Clin. Neurophysiol.36, 323–326 (1974)
Lasansky, A., Wald, F.: The extracellular space in the toad retina as defined by the distribution of ferricyanide. A light and electron microscope study. J. Cell Biol.15, 463–479 (1962)
Laughlin, S.B.: Neural integration in the first optic neuropile of dragonflies. III. The transfer of angular information. J. comp. Physiol.92, 377–396 (1974a)
Laughlin, S.B.: Resistance changes associated with the response of insect monopolar neurons. Z. Naturforsch.29c, 449–450 (1974b)
Laughlin, S.B.: The function of the lamina ganglionaris. In: The compound eye and vision in insects (ed. G.A. Horridge). London: Oxford University Press 1975
Leutscher-Hazelhoff, J.T., Kuiper, J.W.: Responses of the blowfly (Calliphora erythrocephala) to light flashes and to sinusoidally modulated light. Doc. Ophthalmol.18, 275–283 (1964)
Loew, E.R.: Component analysis of the mass electrical response (ERG) of the flySarcophaga bullata. Ph.D. Thesis, University of California, Los Angeles (1973)
Miller, R.F., Dowling, J.E.: Intracellular responses of the Müller (glial) cells of mudpuppy retina: their relation to the b-wave of the electroretinogram. J. Neurophysiol.33, 323–341 (1970)
Mori, S., Miller, W.H., Tomita, T.: Müller cell function during spreading depression in frog retina. Proc. Nat. Acad. Sci.73, 1351–1354 (1976)
Mote, M.I.: Focal recording of response evoked by light in the lamina ganglionaris of the flySarcophaga bullata. J. exp. Zool.175, 149–158 (1970)
Neal, H.: Effects of L-glutamate and other drugs on some membrane properties of muscle fibers of Diptera. J. Insect Physiol.21, 1771–1778 (1975)
Olsen, R.W., Ban, M., Miller, T., Johnston, G.A.R.: Chemical instability of the GABA antagonist bicuculline under physiological conditions. Brain Res.98, 383–387 (1975)
Rodieck, R.W.: The vertebrate retina. Principles of structure and function. San Francisco: W.H. Freeman and Company
Rosser, B.L.: A study of the afferent pathways of the dragonfly lateral ocellus from extracellularly recorded spike discharges. J. exp. Biol.60, 135–160 (1974)
Scholes, J.: The electrical responses of the retinal receptors and the lamina in the visual system of the flyMusca. Kybernetik6, 149–162 (1969)
Shaw, S.R.: Organization of the locust retina. Symp. Zool. Soc. Lond.23, 135–163 (1968)
Shaw, S.R.: Retinal resistance barriers and electrical lateral inhibition. Nature255, 480–483 (1975)
Shaw, S.R.: Restricted diffusion and extracellular space in the insect retina. J. comp. Physiol.113, 257–282 (1977)
Shaw, S.R.: The extracellular space and blood-eye barrier in an insect retina: an ultrastructural study. Cell Tiss. Res.188, 35–61 (1978)
Stieve, H., Malinowska, T.: The effect of tetrodotoxin, veratridine, and tetraethylammonium chloride on the receptor potential of the crayfish photoreceptor cell. Z. Naturforsch.28 c, 149–156 (1973)
Strausfeld, N.J.: The organization of the insect visual system (light microscopy). I. Projections of neurons in the lamina ganglionaris of Diptera. Z. Zellforsch.121, 377–441 (1971)
Strausfeld, N.J., Campos-Ortega, J.A.: Vision in insects: pathways possibly underlying neural adaptation and lateral inhibition. Science195, 894–897 (1977)
Tomita, T., Murakami, M., Sato, Y., Hashimoto, Y.: Further study of the so-called cone action potential (S-potential), its histological determination. Jap. J. Physiol.9, 63–69 (1959)
Toyoda, J.I., Nosaki, H., Tomita, T.: Light-induced resistance changes in single photoreceptors ofNecturus andGecko. Vision Res.9, 453–463 (1969)
Trujillo-Cenóz, O.: Some aspects of the structural organization of the intermediate retina of Dipterans. J. Ultrastruct. Res.13, 1–33 (1965)
Trujillo-Cenóz, O.: The structural organization of the compound eye in insects. In: Physiology of photoreceptor organs. In: Handbook of sensory physiology, Volume VII/2 (ed. M.G.F. Fuortes). Berlin-Heidelberg-New York: Springer 1972
Zettler, F., Järvilehto, M.: Decrement-free conduction of graded potentials along the axon of a monopolar neuron. Z. vergl. Physiol.75, 402–421 (1971)
Zettler, F., Järvilehto, M.: Active and passive axonal propagation of the non-spike signals in the retina ofCalliphora. J. comp. Physiol.85, 89–104 (1973)
Zuckerman, R.: Mechanisms of photoreceptor current generation inlight and darkness. Nature (Lond.) New Biol.234, 29–31 (1971)
Zuckerman, R.: Ionic analysis of photoreceptor membrane currents. J. Physiol. (Lond.)235, 333–354 (1973)
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
- Optic Lobe
- Synaptic Conductance
- GABAergic Synapse