Behaviour of the rod network in the tiger salamander retina mediated by membrane properties of individual rods

Abstract

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

Characterization of a voltage-gated K+ channel that accelerates the rod response to dim light

“…As signals spread through the rod network they become more transient, suggesting that response acceleration in individual rods is important in network function (Attwell and Wilson, 1980). Detwiler et al (1978) found that the voltage response to a bar of light peaked earlier in rods farther away from the bar.…”

“…Since this voltage waveform is unchanged by Cs + (Fain et al, 1978;Owen and Torre, 1983), there has been speculation that currents other than I h shape small signals (Fain et al, 1978;Werblin, 1979;Attwell and Wilson, 1980;Fain and Lisman, 1981;Owen andTorre, 1981, 1983;Baylor et al, 1984). These may be K + currents because the "negative conduction velocity" of small transient signals propagating in the rod network, which is mediated by voltage-gated ion channels (Detwiler et al, 1978;Attwell and Wilson, 1980), is inhibited by high external K + concentrations (Owen and Torre, 1983).…”

“…Attwell and Wilson (1980) have suggested that one of two current components contributing to the net current elicited by hyperpolarization was a deactivating outward current, I x , which could be recorded in the presence of Cs + and reversed in the region of the K + equilibrium potential. Bader et al (1982) have described a voltage-gated K + current (I K ) and a Ca 2+ -activated K + current, but the role of these currents in the response to dim light has not been addressed.…”

Direct Evidence for Daily Plasticity of Electrical Coupling between Rod Photoreceptors in the Mammalian Retina

“…Electrical coupling between rod photoreceptors has been extensively explored using both experimental and modeling approaches (Copenhagen and Owen, 1976;Lamb and Simon, 1976;Schwartz, 1976;Detwiler et al, 1978;Werblin, 1978;Attwell and Wilson, 1980;Attwell et al, 1984;Tessier-Lavigne and Attwell, 1988;Hornstein et al, 2005;Zhang and Wu, 2005;Li et al, 2012). Coupling shapes the rod network properties and the light response of each rod (Attwell and Wilson, 1980;Attwell et al, 1984;Tessier-Lavigne and Attwell, 1988;Hornstein et al, 2005;Li et al, 2012).…”

“…Coupling shapes the rod network properties and the light response of each rod (Attwell and Wilson, 1980;Attwell et al, 1984;Tessier-Lavigne and Attwell, 1988;Hornstein et al, 2005;Li et al, 2012). Estimates of the rod junctional conductance, a direct measure of the rod-rod coupling strength, range between 0 and Ͼ600 pS (Zhang and Wu, 2005;Li et al, 2012).…”