Faculty of 1000 evaluation for Feedback from horizontal cells to rod photoreceptors in vertebrate retina (original) (raw)
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Feedback from Horizontal Cells to Rod Photoreceptors in Vertebrate Retina
Journal of Neuroscience, 2008
Retinal horizontal cells (HCs) provide negative feedback to cones, but, largely because annular illumination fails to evoke a depolarizing response in rods, it is widely believed that there is no feedback from HCs to rods. However, feedback from HCs to cones involves small changes in the calcium current (I Ca) that do not always generate detectable depolarizing responses. We therefore recorded I Ca directly from rods to test whether they were modulated by feedback from HCs. To circumvent problems presented by overlapping receptive fields of HCs and rods, we manipulated the membrane potential of voltage-clamped HCs while simultaneously recording from rods in a salamander retinal slice preparation. Like HC feedback in cones, hyperpolarizing HCs from Ϫ14 to Ϫ54, Ϫ84, and Ϫ104 mV increased the amplitude of I Ca recorded from synaptically connected rods and caused hyperpolarizing shifts in I Ca voltage dependence. These effects were blocked by supplementing the bicarbonate-buffered saline solution with HEPES. In rods lacking light-responsive outer segments, hyperpolarizing neighboring HCs with light caused a negative activation shift and increased the amplitude of I Ca. These changes in I Ca were blocked by HEPES and by inhibiting HC light responses with a glutamate antagonist, indicating that they were caused by HC feedback. These results show that rods, like cones, receive negative feedback from HCs that regulates the amplitude and voltage dependence of I Ca. HC-to-rod feedback counters light-evoked decreases in synaptic output and thus shapes the transmission of rod responses to downstream visual neurons.
The Journal of Physiology, 2009
We tested whether horizontal cells (HCs) provide feedback that regulates the Ca 2+ current (I Ca) of rods in salamander and mouse retinas. In both species, hyperpolarizing HCs by puffing a glutamate antagonist, 6,7-dinitro-quinoxaline-2,3-dione (DNQX), onto HC processes caused a negative shift in the voltage dependence of rod I Ca and increased its peak amplitude. Conversely, depolarizing HCs by puffing kainic acid (KA) into the outer plexiform layer (OPL) caused a positive voltage shift and decreased rod I Ca. Experiments on salamander retina showed that these effects were blocked by addition of the pH buffer, Hepes. Intracellular calcium concentration ([Ca 2+ ] i) was examined in rods by confocal microscopy after loading salamander and mouse retinal slices with Fluo-4. Rods were depolarized to near the dark resting potential by bath application of high K + solutions. Hyperpolarizing HCs with 2,3-dihydroxy-6-nitro-7-sulphamoylbenzo[f]quinoxaline (NBQX) enhanced high K +-evoked Ca 2+ increases whereas depolarizing HCs with KA inhibited Ca 2+ increases. In both species these effects of NBQX and KA were blocked by addition of Hepes. Thus, like HC feedback in cones, changes in HC membrane potential modulate rod I Ca thereby regulating rod [Ca 2+ ] i at physiological voltages, in both mouse and salamander retinas. By countering the reduced synaptic output that accompanies hyperpolarization of rods to light, HC feedback will subtract spatially averaged luminance levels from the responses of individual rods to local changes. The finding that HC to rod feedback is present in both amphibian and mammalian species shows that this mechanism is highly conserved across vertebrate retinas.
Brain Research, 1997
We examined the contribution of two intrinsic voltage-dependent calcium channels to the light-evoked responses of a non-spiking Ž . retinal neuron, the horizontal cell HC . HC's isolated from the Xenopus retina were studied by the whole cell version of the patch clamp. In a mixture of agents which suppressed Na-and K-dependent currents, we identified a transient, low voltage-activated Ca current 2q 2q Ž . suppressed by Ba and blocked by Ni T-type and a sustained, high voltage-activated, dihydropyridine-sensitive Ca current that was 2q Ž . enhanced by Ba L-type . We made simultaneous intracellular recordings from rods and HC's in the intact, dark-adapted Xenopus retina. Under certain stimulus conditions, transient oscillations appeared in HC responses but were absent in rod light-evoked waveforms.
Chloride currents in cones modify feedback from horizontal cells to cones in goldfish retina
The Journal of Physiology, 2012
• The GABAergic pathway modulates feedback between retinal horizontal cells (HCs) and cone photoreceptors, but is not mediating negative feedback, as previously hypothesized. • Opening of GABA-gated chloride channels in cone photoreceptors reduces the amplitude of feedback responses generated by HCs. • Activation of a different presynaptic chloride current, the calcium-dependent chloride current, in individual cones has a similar effect on feedback as application of GABA. • Modulation of the strength of feedback from HCs seems to be a general consequence of activation of presynaptic chloride currents in cones. • This puts the functional role of these currents in a new perspective; GABA acts as a slow and global neuromodulator enhancing feedback in the light-and attenuating feedback in the dark-adapted retina, whereas the calcium-dependent chloride current modulates feedback fast and locally to tune the size of feedback to local light conditions.
Light Evokes Ca2+ Spikes in the Axon Terminal of a Retinal Bipolar Cell
Neuron, 2000
transmitter release takes place. Thus, their output in Am Fassberg response to a synaptic input presumably depends criti-D-37077 Gö ttingen cally upon their passive electrotonic properties. Several † Max-Planck Institute for Brain Research types of bipolar cells have been classified in the verte-Deutschordenstrasse 46 brate retina according to their morphology and to the D-60528 Frankfurt am Main presynaptic elements they contact (Mills and Massey, Germany 1992; Euler et al., 1996; Sterling, 1998). In mammals, ‡ The Vollum Institute bipolar cells receive input from either rods or cones and Oregon Health Sciences University are thus termed rod or cone bipolars, while in cold-Portland, Oregon 97201 blooded vertebrates, some bipolars connect to both rods and cones and are thus named mixed bipolar (Mb) cells (Ishida et al., 1980). In the goldfish retina, for exam-Summary ple, the Mb1 cells (Sherry and Yazulla, 1993) contact some cones but receive most of their input from rods Bipolar cells in the vertebrate retina have been characand are thus part of the high-sensitivity, single photonterized as nonspiking interneurons. Using patch-clamp detecting pathway of the retina (Yang and Wu, 1997). recordings from goldfish retinal slices, we find, how-In dark-adapted retinae of the turtle (Schwartz, 1974), ever, that the morphologically well-defined Mb1 bipocarp (Mb1-type cells; Saito et al., 1979), dogfish (Ashlar cell is capable of generating spikes. Surprisingly, more and Falk, 1980), and rabbit (Dacheux and Raviola, in dark-adapted retina, spikes were reliably evoked by 1986
European Journal of Neuroscience, 2006
We examined the contribution of calcium-induced calcium release (CICR) to synaptic transmission from rod photoreceptor terminals. Whole-cell recording and confocal calcium imaging experiments were conducted on rods with intact synaptic terminals in a retinal slice preparation from salamander. Low concentrations of ryanodine stimulated calcium increases in rod terminals, consistent with the presence of ryanodine receptors. Application of strong depolarizing steps (−70 to −10 mV) exceeding 200 ms or longer in duration evoked a wave of calcium that spread across the synaptic terminals of voltage-clamped rods. This secondary calcium increase was blocked by high concentrations of ryanodine, indicating it was due to CICR. Ryanodine (50 μM) had no significant effect on rod calcium current (I ca) although it slightly diminished rod light-evoked voltage responses. Bath application of 50 μM ryanodine strongly inhibited light-evoked currents in horizontal cells. Whether applied extracellularly or delivered into the rod cell through the patch pipette, ryanodine (50 μM) also inhibited excitatory post-synaptic currents (EPSCs) evoked in horizontal cells by depolarizing steps applied to rods. Ryanodine caused a preferential reduction in the later portions of EPSCs evoked by depolarizing steps of 200 ms or longer. These results indicate that CICR enhances calcium increases in rod terminals evoked by sustained depolarization, which in turn acts to boost synaptic exocytosis from rods.
Proceedings of the National Academy of Sciences, 1996
According to the classical calcium hypothesis of synaptic transmission, the release of neurotransmitter from presynaptic terminals occurs through an exocytotic process triggered by depolarization-induced presynaptic calcium influx. However, evidence has been accumulating in the last two decades indicating that, in many preparations, synaptic transmitter release can persist or even increase when calcium is omitted from the perfusing saline, leading to the notion of a "calcium-independent release" mechanism. Our study shows that the enhancement of synaptic transmission between photoreceptors and horizontal cells of the vertebrate retina induced by low-calcium media is caused by an increase of calcium influx into presynaptic terminals. This paradoxical effect is accounted for by modifications of surface potential on the photoreceptor membrane. Since lowering extracellular calcium concentration may likewise enhance calcium influx into other nerve cells, other experimental obse...
The Journal of Neuroscience : The Official Journal of the Society for Neuroscience
We related rod to horizontal cell synaptic transfer to glutamate release by rods. Simultaneous intracellular records were obtained from dark-adapted rod-horizontal cell pairs. Steady-state synaptic gain (defined as the ratio of horizontal cell voltage to rod voltage evoked by the same light stimulus) was 3.35 +/- 0.60 for dim flashes and 1.50 +/- 0.03 for bright flashes. Under conditions of maintained illumination, there was a measurable increment of horizontal cell hyperpolarization for each light-induced increment of rod hyperpolarization over the full range of rod voltages. In separate experiments we studied glutamate release from an intact, light-responsive photoreceptor layer, from which inner retinal layers were removed. Steady light reduced glutamate release as a monotonic function of intensity; spectral sensitivity measures indicated that we monitored glutamate release from rods. The dependence of glutamate release on rod voltage was well fit by the activation function for a...
The Journal of neuroscience : the official journal of the Society for Neuroscience, 1997
We related rod to horizontal cell synaptic transfer to glutamate release by rods. Simultaneous intracellular records were obtained from dark-adapted rod-horizontal cell pairs. Steady-state synaptic gain (defined as the ratio of horizontal cell voltage to rod voltage evoked by the same light stimulus) was 3.35 +/- 0.60 for dim flashes and 1.50 +/- 0.03 for bright flashes. Under conditions of maintained illumination, there was a measurable increment of horizontal cell hyperpolarization for each light-induced increment of rod hyperpolarization over the full range of rod voltages. In separate experiments we studied glutamate release from an intact, light-responsive photoreceptor layer, from which inner retinal layers were removed. Steady light reduced glutamate release as a monotonic function of intensity; spectral sensitivity measures indicated that we monitored glutamate release from rods. The dependence of glutamate release on rod voltage was well fit by the activation function for a...