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Ability to Light-Induced Conductance Change of Arthropod Visual Cell

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Ability to Light-Induced Conductance Change of Arthropod Visual Cell Ability to Light-Induced Conductance Change of Arthropod Visual Cell Membrane, Indirectly Depending on Membrane Potential, during Depolarization by External Potassium or Ouabain * H. Stieve, M. Bruns, and H. Gaube Institut für Neurobiologie der Kernforschungsanlage Jülich GmbH (Z. Naturforsch. 32 c, 8 5 5 -8 6 9 [1977]; received July 12, 1977) Astacus and Limuluis Photoreceptors, Light Response, Membrane Conductance, Ouabain, Potassium Depolarization Light responses (ReP) and pre-stimulus membrane potential (PMP) and conductance of photo­ receptors of Astacus leptodactylus and Limulus polyphemus (lateral eye) were recorded and changes were observed when the photoreceptor was depolarized by the action of external ouabain or high potassium concentration application. 1 mM/1 ouabain application causes a transient increase of PMP and ReP in Limulus, followed by a decrease which is faster for the ReP (half time 34 min) than for the PMP (half time 80 min). Irreversible loss of excitability occurs when the PMP is still ca. 40% of the reference value. In both preparations high external potassium concentration leads to total depolarization (beyond zero line to +10— f-20mV) of the PMP and after a time lag of 10 min also to a loss of ex­ citability (intracellular recording). In extracellular recordings (Astacus ) the excitability remains at a low level of 15%. The effects are reversible and are similar whether no or 10% external sodium is present. In all experiments the light-induced changes of membrane conductance are about parallel to those of the light response. The fact that the ability of the photosensoric membrane to undergo light-induced conductance changes is membrane potential-dependent is discussed, leading to the explanation that dipolar membrane constituents such as channel forming molecules (probably not rhodopsin) have to be ordered by the membrane potential to keep the membrane functional for the photosensoric action. Introduction Stieve et al. 7). In order to interpret earlier experi­ ments dealing with ouabain poisoning of visual cells In the nerve membrane the sodium conductance (Stieve8,1) we wanted to study whether the ability changes during excitation occur only if the resting to permeability change of the visual cell membrane membrane potential is sufficiently high. At lower during the light response depends on the membrane membrane potentials following depolarization by potential. To this end photoreceptors of Astacus raising the external potassium concentration (Cole leptodactylus and Limulus polyphemus (lateral eye) and Curtis 2) the sodium permeability system is in­ were exposed to the depolarizing effect of ouabain activated. Hodgkin and Huxley3 found that de­ or high external potassium concentration. In part polarization by 20 mV inactivates more than 50% of the experiments light responses were recorded of the sodium conductance system of the squid nerve simultaneously by intra- and extracellular electrodes membrane. from the same preparation to get information on As opposed to the axon membrane the visual cell differences of these two recording methods. membrane is generally not electrically excitable — except for the fact that a small component of the M ethods light response can be elicited by an electrical de­ polarizing step (Purple and Dodge4, Millecchia and Slices of lateral eyes of the horseshoe crab Mauro 5) . Limulus polyphemus and of isolated retinas of the crayfish Astacus leptodactylus were superfused in In the arthropod photoreceptor a light-induced the experiments by a stream of test saline at a flow change of the membrane conductance causes the rate of 0.5 ml/min. The half time of the change of voltage signal at the cell membrane (Fuortes6, saline (until ca. 50% of the saline was exchanged at the preparation) was 10 min for Limulus and * Some of the results of this paper are already briefly de­ scribed by Stieve 1. less for Astacus. (For a description of the prepara­ tion technique and other details see Stieve et al. 9.) Requests for reprints should be sent to Prof. Dr. H. Stieve, Institut für Neurobiologie der Kernforschungs­ The ionic composition of the test salines is given anlage Jülich GmbH, Postfach 1913, D-5170 Jülich. in Table I. The crayfish retinas were kept in van 856 H. Stieve et al. • Light-Induced Conductance Change Table I. Ionic composition [mM/1] of salines used in the experiments. Na+ K+ C a^ M g^ c r S 0 42~ h c o 3~ Ouabain Limulus Lx (physiological 488.3 10.0 10.0 55.0 566.0 30.0 2.3 — saline) L2 (ouabain added) 488.3 10.0 10.0 55.0 566.0 30.0 2.3 1.0 L3 (K+ added) 498.3 10.0 55.0 566.0 30.0 2.3 Astacus A 1 (physiological 207.3 5.0 14.0 3.0 244.0 — 2.3 — saline) A2 (K+ added) — 212.3 14.0 3.0 244.0 — 2.3 — A3 (K+ added, 20.7 191.6 14.0 3.0 244.0 2.3 Na+ decreased to 10%) Harreveld’s 10 solution, and the Limuli in artificial period of 60 min constant stimuli every 10 or 5 min seawater (Table I), both at 15 °C. When the potas­ were applied. In the main period (60 to 120 min) sium concentration was increased a corresponding the preparation was exposed to the test saline, and amount of sodium was omitted to keep the osmotic in an after-^period of at least 60 min the original pressure constant. The pH of all salines was 7.5 physiological saline was applied again. to 8.0. Evaluation For intracellular measurement single visual cells In the intracellular recordings the membrane were penetrated by glass microelectrodes filled with potential of the visual cell before the light stimulus 0.5 M KC1 solution, and the light response was re­ could be measured (pre-stimulus membrane poten­ corded against an extracellular indifferent silver tial PMP; in the present experiments identical with chloride electrode. For extracellular measurement the dark potential DaP; in the figure both abbre­ two chlorided silver wires were in contact with the viations are used). The light responses (receptor distal and proximal sides of the retina slice. potential, ReP) were evaluated concerning their size The electronic recording system allowed DC com­ and shape by measuring the following parameters. pensation, current injection through the microelec­ trode, and compensated current pulses through the a) For short stimuli (r shorter than latent period): measuring circuit in order to measure the input /tmax [mV], maximal amplitude of transient; impedance (of cell membrane, cell and electrode in series). The data were FM recorded on magnetic fiat [ms], latent period, from light flash onset analogue tape (Ampex FR 1300) and photographed until intersection of tangent line in for evaluation by hand. They were parallelly re­ point of steepest increase of rising corded by a paper recorder (Helcoscriptor HE 16). phase with extrapolated level of base The time resolution of the system was 1 ms, the line; measuring accuracy was 1 mV (intracellular re­ £max [ms], time — to — peak (from light flash onset cording) and 0.01 mV (extracellular recording). until response maximum) ; In the experiments labelled JA a xenon high t2 [ms], time of half decrease (from Amax to pressure lamp (Osram XBO 900 W) with a maximal ^max/2) ? intensity of ca. 20000 lx (3.2 x 1016 photons'em-2 b) for long stimuli (t= 1000 ms), additionally •sec-1), and in the experiments labelled JB a mer­ to Amax and £max: cury super pressure lamp (Philips CS 100 W/2) with a maximal intensity of ca. 5500 lx (9 X 1015 he [mV], plateau-value (at the end of the stimu­ photons •cm2* sec-1) was used. Stimuli of maximal lus) ; intensity and two durations were applied: short /ia [mV], response amplitude 500ms after the stimuli (r = 10 ms for Astacus, r = 33 or 50 ms for end of the stimulus; Limulus ) and long stimuli (r = 1000 ms). hmaJ he , shape quotient. Procedure The changes of the ReP were expressed in per All experiments lasted at least three hours and cent of the reference values of the last ReP of the were carried out at 15 °C in the dark. During a pre­ pre-period. H. Stieve et al. • Light-Induced Conductance Change 857 Additionally impedance measurements (of the Ouabain Limulus 45JB input resistance, i. e. of the sum of the resistances of cell membrane, cell and electrode in series) were 3 0 -i 0---- ■----------------------- carried out using current pulses (0.5 —1.5 nA) mV P V v " '■*w c L through the intracellular electrode (20 ms duration ; r r r r r r r and 10 Hz frequency for short stimuli, 50 ms and 7 / 5 Hz for long stimuli). Measurements of the input 30 impedance in the dark (/?<*) and its changes at mV . various times of the ReP (ARm at the time of the maximal amplitude, etc.) are listed in some tables and figures. The values were normalized similarly as described for the receptor potential parameters. Results 1. Ouabain 10 -1 0 - In earlier experiments we could show by extra­ mV cellular recording (Stieve et al .7) that under in­ fluence of ouabain the excitability of the visual cells of the Astacus retina disappears; this happens the 10 faster, the stronger and more frequently the cells mV are stimulated by light. Intracellular recordings in Limulus retinular cells showed that the cells were inexcitable due to ouabain poisoning long before 0 1s the dark potential had become zero (Stieve8). This Fig. 1. Intraeellularly recorded receptor potentials of a is in agreement with the results of Smith et al . 11 Limulus retinular cell and simultaneous measurement of the membrane resistance change AR (difference between the and Brown and Lisman12 (who were using stro­ two recorded traces of each measurement, i.
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