SUMMARY1. The spread of electrical signals between rods in the salamander retina was examined by passing current into one rod and recording the voltage responses in nearby rods. Rod network behaviour, measured in this way, was simulated from data on rod membrane properties gathered in voltage-clamp experiments on single isolated rods.2. The network voltage responses to square current pulses became smaller, more transient, and had a longer time-to-peak, for rods further away from the site of current injection. Depolarizing currents produced smaller responses than hyperpolarizing currents of the same magnitude.3. Neighbouring rods and cones were coupled less strongly than neighbouring rods. 4. The response of the rod network to current injection was unaffected by 2 mMaspartate-, which eliminates transmission from receptors to horizontal cells.5. The input resistance of single isolated rods, measured at the resting potential, varied between 100 and 680 MQ. The lower values were probably due to damage by the micro-electrodes. Electrical coupling was found to be very strong between the rod inner and outer segments. 6. A strong 'instantaneous' outward rectification seen in isolated rods at potentials positive to -35 mV was reduced, but not abolished, by 15 mM-TEA.7. In normal solution, isolated rods exhibited a voltage-and time-dependent current, IA, whose kinetics were approximated by a single first-order gating variable, and whose activation curve spanned the range between -40 and -80 mV. The time constant for the current varied with voltage and was 60-200 msec between -140 and -40 mV.8. A reversal potential for IA could not be found between -140 and -40 mV in normal solution, and the fully activated current, IA, was approximately voltageindependent, with a magnitude of , 0*1 nA over this potential range. 9. By several criteria, IA behaved as a single inward current activated by hyperpolarization. Pharmacological studies suggest, however, that it is the sum of at least two currents with very similar kinetics.10. Most isolated rods exhibited a very slow (T , 3 see) increase in net outward
Miniature postsynaptic currents (minis) in cultured retinal amacrine cells, as in other central neurons, show large variations in amplitude. To understand the origin of this variability, we have exploited a novel form of synapse in which pre- and postsynaptic receptors sample the same quantum of transmitter. At these synapses, mini amplitudes measured simultaneously in the 2 cells show a strong correlation, accounting for, on average, more than half of the variance in amplitude. Two pieces of evidence support the conclusion that variations in the amount of transmitter in different quanta underlie this correlation. First, diazepam, which enhances GABA binding, increases mini amplitude, implying therefore that transmitter concentration is not saturating. Second, we show that amplitude distributions from all cells, even those with a small number of release sites, have the same shape, implying that most or all variance is intrinsic to each release site.
SUMMARY1. A quantitative description of the electrical properties of the photoreceptor layer in the salamander retina was obtained from earlier data on the characteristics of isolated rods and cones and on rod-rod coupling, and from new data on rod-cone and cone-cone coupling and on the rod photocurrent.2. Injecting -1 nA current into a rod elicits hyperpolarizations of about 20 mV in an adjacent rod and 4 mV in an adjacent cone. Responses of more distant receptors are smaller. Injecting -1 nA into a cone elicits hyperpolarizations of about 4 mV in an adjacent rod and 0-4 mV in a nearby cone. Depolarizing current evokes smaller responses.3. Assuming, in agreement with anatomical evidence, that each rod is electrically coupled to four rods and to four cones around it, and that there is no direct electrical coupling between cones, we found these results could be predicted from the properties of isolated rods and cones if adjacent rods are coupled by a resistance of 300 MC and adjacent rods and cones are coupled by a resistance of 5000 MC. The small cone-cone coupling seen is due to coupling via intervening rods.4. The two halves of double cones are not electrically coupled. The spectral sensitivity of both halves is a maximum around 620 nm wave-length. 6. The voltage responses of rods, single cones and double cones isolated from the retina obey the principle of univariance.7. Responses of receptors in the retina do not obey univariance. The main deviations from univariance observed can be explained if adjacent rods and cones are coupled by a resistance of 5000 MCI.8. Our data demonstrate that rod-cone coupling is relatively weak. We simplified our description of the photoreceptor network, by omitting cones, to investigate the spatiotemporal processing that the rod network is capable of.
SUMMARY1. The properties of isolated single cones were studied using the voltage-clamp technique, with two micro-electrodes inserted under visual control.2. Single cones had input resistances, when impaled with two electrodes, of up to 270 MCI. This is probably lower than the true membrane resistance, because ofdamage by the impaling electrodes. The cone capacitance was about 85 pF. 4. The gated current, IB, is an inward current with a reversal potential around -25 mV. It is activated by hyperpolarization over the range -30 to -80 mV, and at constant voltage obeys first order (exponential) kinetics. The gating time constant is typically 50 ms at the resting potential of -45 mV, rises to 170 ms at -70 mV, and decreases for futher hyperpolarization.5. The spectral sensitivity curve of the cone light response peaks at 620 nm wave-length, and is narrower than the nomogram for vitamin A2-based pigments. The light responses of isolated cones are spectrally univariant.6. Voltage-clamped photocurrents were recorded at various membrane potentials, for light steps of various intensities. The photocurrent reversed at around -8 mV. The time course of the photocurrent, for a given intensity, was approximately independent of voltage (although its magnitude was voltage-dependent). The shape of the peak current-voltage relation of the light-sensitive current was independent of light intensity (although its magnitude was intensity-dependent).7. These results can be explained if: (a) light simply changes the number of photosensitive channels open, without altering the properties of an open channel; (b) the reactions controlling the production of internal transmitter, the binding of internal transmitter to the photosensitive channels, and the closing and opening of the channels are unaffected by the electric field in the cone membrane, even though at least some of these reactions take place in the membrane.8. IB plays only a small role in shaping the cone voltage response to light.
The properties of synapses between retinal neurons make an essential contribution to early visual processing. Light produces a graded hyperpolarization in photoreceptors, up to 25 mV in amplitude, and it is conventionally assumed that all of this response range is available for coding visual information. We report here, however, that the rod output synapse rectifies strongly, so that only potential changes within 5 mV of the rod dark potential are transmitted effectively to postsynaptic horizontal cells. This finding is consistent with the voltage-dependence of the calcium current presumed to control neurotransmitter release from rods. It suggests functional roles for the strong electrical coupling of adjacent rods and the weak electrical coupling of adjacent rods and cones. The existence of photoreceptor coupling resolves the apparent paradox that rods have a 25 mV response range, while signals greater than 5 mV in amplitude are clipped during synaptic transmission. We predict that the strengths of rod-rod and rod-cone coupling are quantitatively linked to the relationship between the rod response range and the synapse operating range.
The conduction of calcium ions through glutamate-gated channels is important in the induction of long-term potentiation and may trigger other cellular changes. In retinal bipolar cells, which lack the N-methyl-D-aspartate (NMDA) type of glutamate-gated channel, calcium permeability through non-NMDA channels was examined. Changes in extracellular calcium concentration unexpectedly affected the reversal potential for glutamate-induced currents in a manner consistent with these channels being highly permeable to calcium. External magnesium ions promote desensitization of these non-NMDA channels in a voltage-independent way. Thus, in addition to non-NMDA channels that conduct only sodium and potassium, there is a class that is also permeable to calcium.
SUMMARY1. Whole-cell patch clamping was used to study the membrane properties of isolated bipolar cells and the currents evoked in them by putative retinal neurotransmitters.2. Isolated bipolar cells show an approximately ohmic response to voltage steps over most of the physiological response range, with an average input resistance of 1-3 GfS and resting potential of -35 mV. These values are underestimates because of the shunting effect of the seal between the patch electrode and the cell membrane. Depolarization beyond -30 mV produces rapid activation (10-100 ms) ofan outward current (carried largely by potassium ions), which then inactivates slowly (05-2 s).3. Of five candidates for the photoreceptor transmitter, four (aspartate, Nacetylhistidine, cadaverine, putrescine) had no effect on bipolar cells. The fifth substance, L-glutamate, opened ionic channels with a mean reversal potential of -12 mV in some cells (presumed hyperpolarizing bipolar cells), and closed channels with a mean reversal potential, of -13 mV in other cells (presumed depolarizing bipolar cells); 4. The conductance increase induced by glutamate in presumed hyperpolarizing bipolar cells was associated with an increase in membrane current noise. Noise analysis suggested a single-channel conductance for the glutamate-gated channel of 5.4 pS. The power spectrum of the noise increase required the sum of two Lorentzian curves to fit it, suggesting that the channel can exist in three states.5. The conductance decrease induced by glutamate in presumed depolarizing bipolar cells was associated with a decrease in membrane current noise that could be described as the sum of two Lorentzian spectra, and which suggested a singlechannel conductance of 11 pS. The noise decrease implies that the channels closed by glutamate are not all open in the absence of the transmitter.6. GABA (y-aminobutyric acid) and glycine, transmitters believed to mediate lateral inhibition in the retina, open chloride channels in isolated bipolar cells, and increase the membrane current noise. Noise analysis suggested that the channels gated by GABA and glycine have conductances of 4-4 and 7-5 pS respectively. The noise spectra required the sum of two Lorentzian curves to fit them.t To whom all reprint requests should be sent.
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