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1 Department of Physiology and Biophysics, University at Buffalo, 124 Sherman Hall, Buffalo, NY 14214, USA
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(Received 7 June 2005;
accepted after revision 1 September 2005;
first published online 1 September 2005)
Corresponding author M. M. Slaughter: Department of Physiology and Biophysics, University at Buffalo, 124 Sherman Hall, Buffalo, NY 14214, USA. Email: mslaught{at}buffalo.edu
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Introduction |
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One phenomenon these studies concentrated on was the visual afterimage. A remarkable demonstration of this phenomenon, performed on human rod achromats, was to present a supersaturating test image on top of a dimmer, but still saturating background. The test image was invisible to the observer. However, if the subject's eye were subsequently closed, then a positive afterimage became discernable (Sakitt, 1976). Sakitt speculated that the supersaturated test image is stored within the phototransduction process in rod outer segments (Baylor & Fuortes, 1970). This storage is encoded in the rod although it cannot be relayed to the retinal network until the cessation of the image. The supersaturating stimulus is not encoded in the peak voltage response of the rod, but in the delayed recovery of the rod voltage response. Brighter stimuli produce more delayed rod recovery. Sakitt postulated that the formation of positive afterimages was based on this increased latency of recovery of the rod response after a saturating light. The latency before the beginning of the recovery of the response depends on the incident light intensity (Penn & Hagins, 1972; Normann & Werblin, 1974; Yang & Wu, 1997) Rods illuminated by the higher intensity of the test signal had longer latencies than rods exposed to the background. A positive afterimage would occur if rods exposed to the test stimulus were more hyperpolarized than those exposed to the background stimulus. Consequently, Sakitt hypothesized that a positive afterimage could be formed in the time window when background rods recovered while test rods did not. This is because the rods responding to the test stimulus were less depolarized (slower to recover), and releasing less neurotransmitter, characteristics of brighter light and a positive image. If the intensities of the test and background stimuli were increased, it would take longer for a differential response of the affected rods. Thus, both the differential recovery and the positive afterimage are intensity dependent.
This model suggests the importance of rod responses to visual encoding during light exposure traditionally defined as saturating. The above model can explain the positive rod afterimage. However, the authors had difficulty explaining the origin of negative afterimages (Sakitt, 1976), which presumably also originate from photoreceptors. In this paper we report that rods can respond to saturating light with calcium action potentials during the recovery phase of the light response. These spikes encode the intensity of supersaturating light stimuli. Furthermore, these spikes can potentially encode both positive and negative afterimages.
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Methods |
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Larval tiger salamanders were obtained from Kons Direct (Germantown, WI, USA) and Charles Sullivan (Nashville, TN, USA) and were kept in tanks maintained at 4°C on a 12 h light–dark cycle. Retinal slices were prepared as previously described (Wu, 1987; Awatramani & Slaughter, 2000). A few wholemount retinal experiments were performed. In these experiments the retina was placed photoreceptor side down over a ring of filter paper and then covered by another ring of filter paper. This left the central retina exposed, for both light stimulation and patch clamp recording. Both the retinal slice and the wholemount retina were superfused with oxygenated Ringer solution. All procedures were performed in accordance with the US Animal Welfare Act and the National Institutes of Health Guide for the Care and Use of Laboratory Animals (publication 85-23) and were approved by the University Animal Care Committee. All operations were performed under infra-red illumination to keep the retina fully dark adapted.
Recordings were made using either the whole-cell ruptured patch technique or the gramicidin perforated patch method (Kyrozis & Reichling, 1995). The latter was used to preserve the cytosolic content of the cells. Second order neurones were identified by their response characteristics and their appearance after staining with Lucifer Yellow. Rods were identified by their outer segment. The slices were continuously bathed with control Ringer solution containing (mM): 111 NaCl, 2.5 KCl, 1.8 CaCl2, 1 MgCl2, 10 dextrose, and 5 Hepes, buffered to pH 7.8. The recording pipette contained (mM): 100 potassium gluconate, 5 NaCl, 2 MgCl2, 5 EGTA, 5 Hepes and 0.1% Lucifer Yellow, buffered to pH 7.4 with KOH. In perforated patch recordings, 5 mg of gramicidin was dissolved in 1 ml DMSO and 2.5 µl of it was added to 1 ml of pipette solution. The pipette solution containing gramicidin was sonicated before use. In whole-cell ruptured patch recordings, the solution also contained an ‘ATP regenerating cocktail’ consisting of 4 mM ATP, 20 mM phosphocreatine and 50 units ml–1 creatine phosphokinase.
Electrophysiological data were collected with a List EPC-9 amplifier, HEKA Pulse software and a Macintosh G3 computer and analysed with Igor Pro software. The analog signals were filtered at 5 kHz. Data are expressed as means ±S.E.M. Access resistance was 8–15 M
for whole-cell rupture recordings and 8–30 M for perforated patch recordings and generally was not compensated. Liquid junction potential for whole-cell rupture recording was measured to be around –10 mV and this value adjustment was applied to all the data. No liquid junction potential adjustment was made for perforated patch recordings.
Light responses were generated by either a green (wavelength 500 nm) or a red (wavelength 650 nm) LED. The light intensity units used in the text only apply to the green light stimuli and defined such that 1 unit of light is equivalent to an intensity 
103 photons µm–2 s–1.
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Results |
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During the offset of a larger negative current (–35 pA), an inflection appeared in the depolarizing voltage response, followed by a spike. The membrane voltage rose rapidly to a voltage more positive than –20 mV. Increasing the current injection to –40 pA resulted in a faster depolarization at current offset. The spike was of similar amplitude, although it reached peak earlier. After the peak of the spike, the membrane potential decayed gradually for about 50 ms. Then the voltage decline became more rapid and eventually led to an undershoot. The undershoot was not present in traces without spikes. The undershoot was probably caused by the activation of calcium-dependent K+ and Cl– currents, because these two ions had reversal potentials more negative than the rod membrane potential under our experimental conditions.
These experiments indicate that voltage-gated ion channels in the inner segment and terminal of the rod can, under certain conditions, produce regenerative depolarizations. Regenerative currents have been reported in salamander and lizard cones (Maricq & Korenbrot, 1988; Barnes & Deschenes, 1992), produced by the combination of calcium current and calcium-activated chloride current (the chloride reversal potential was set to 0 mV in the cited experiments). However, the chloride reversal potential was set at –65 mV in our experiments and did not contribute to the generation or maintenance of the regenerative response shown in Fig. 1. On the contrary, it may contribute to the decline and collapse of the overshoot. The only significant depolarizing current in our experiments was the calcium current. It is likely that the calcium current is regenerative due to its high density at the synaptic terminal of rods (Xu & Slaughter, 2005).
Action potentials can also be produced by bright light. Dark-adapted rods were recorded in current clamp mode. Of the rods examined, about a fourth (18 out of 78) exhibited spike activity during the recovery phase of the light response (Fig. 2). The spike occurred several seconds after the offset of a 1 s light stimulus (Fig. 2A). The spikes had different shapes in different cells, as exemplified in Fig. 2. The depolarization reached approximately the same voltage, with a mean peak potential of –25.7 ± 2.7 mV (n= 18). The timing of the start of the regenerative potential ranged from 8 to 12 s after the light stimulus, with a mean of 10.1 ± 1.5 s at a light intensity of 1.3 log units (see Methods). We show below that the delay depends on the incident light intensity.
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Fain et al. (1980) concluded that the regenerative potentials recorded in toad rods in the presence of TEA represented calcium currents, which only became regenerative after the potassium conductance was blocked. The regenerative potentials we observed under normal physiological conditions were also calcium currents because they were blocked by 100 µM Cd2+, a blocker of voltage-gated calcium channels, or 30 µM nifedipine, an L-type calcium channel blocker (Fig. 2B). They cannot be calcium-dependent potassium or chloride currents, since both have more negative equilibrium potentials. Rod spikes were detected without blockade of potassium channels in our experiments.
Nevertheless, both voltage-dependent and calcium-dependent (BK) potassium channels limited the amplitude and duration of rod spikes. Rods exhibit a large BK current (Bader & Bertrand, 1984; Moriondo et al. 2001; Xu & Slaughter, 2004). When the BK channel was blocked by 1 mM TEA, the regenerative potential reached a mean peak amplitude of –15.4 ± 3.7 mV (n= 5), compared with –25.7 ± 2.7 mV under control conditions (Fig. 3A). Similar results were obtained using 100 nM charybdotoxin, another BK channel blocker. In two cells, the oscillatory potentials became fewer and broader (Fig. 3A upper panel). However, in other cells the spike amplitude increased without a notable broadening (e.g. Fig. 3A lower panel). Thus, in rods as in other neurones the BK channels produce a negative feedback that limits the size of the calcium spike (Hille, 2001).
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The calcium current can be observed in the I–V responses of rods under normal conditions, without the need to block potassium channels (Fig. 4). The I–V curve was obtained by a voltage ramp from –70 mV to 0 mV at 0.5 mV ms–1, recorded in control Ringer solution. The I–V curve was linear from –70 mV to about –35 mV, at which point an inward current was activated. It peaked at around –25 mV. This current could be blocked by 50 µM Cd2+, indicative of a calcium-dependent inward current. It can only be calcium current, because calcium-activated K+ and Cl– currents are both outward in this voltage range. This result is consistent with the previous experiments showing that the calcium current is regenerative, even in the presence of outward currents.
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It can be inferred from the model that if the rod depolarizes to threshold (point C in Fig. 4), then the depolarization will become regenerative. What is the source of the inward current that brings the rod to threshold?Figure 1 suggests that anodal break excitation contributes to it, indicating the contribution of voltage-gated channels. To examine if any voltage-independent mechanism might contribute to it, we recorded the light response of a rod in voltage clamp mode. Light onset produced an outward current. At light offset, the rod produced an inward current undershoot (Fig. 5A, Vhold was –40 mV). As the light intensity increased, the undershoot increased in amplitude and peaked later. If the light intensity is big enough, it may produce enough inward current to bring the rod to spike threshold. To test this, we compared the light-evoked current in a rod with spike generation in the same rod (Fig. 5B). The time course of the light-evoked inward current (below baseline, dotted line) corresponded with the rod depolarization (above resting potential). The spike in the rod occurred near the peak of the inward current. Thus, the undershoot is the spike generator. It is likely to be augmented by voltage-gated channels such as Ih. This inward current was also seen when gap junctions were blocked by carbenoxolone (n= 3), so it is not the result of gap junction currents from neighbouring rods.
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In the rod depicted in Fig. 5A, the recovery phase of the rod current had a slight undershoot when the incident light intensity was low. At higher light intensities, the undershoot became bigger. The amplitude and timing of the undershoot correlated with light intensity. The stronger the light signal, the later the peak of the undershoot. This indicates that the undershoot can carry information encoding light intensity when the initial rod light response has saturated.
If the undershoot in the rod current varied with light intensity and was responsible for the generation of the calcium spike, it implies that the spike is intensity dependent. This is indeed the case, as illustrated in Fig. 6. In recordings of rod voltage, dim lights produced a very small voltage overshoot, equivalent to an undershoot in the current recordings. As the light intensity increased, the voltage overshoot became larger and eventually led to a calcium spike. Further increases in light intensity produced spikes of similar amplitudes, but longer latencies. The last four traces represent increasing intensities of supersaturating light stimuli, yielding calcium spikes of increasing latencies. Thus, the rod was able to encode light intensities that exceeded saturation. Similar results were observed in three cells.
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Discussion |
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Generally, first and second order neurones of vertebrate retina are regarded as non-spiking neurones. However, Ca2+ action potentials have been observed in isolated retinal bipolar cells (Zenisek & Matthews, 1998; Ma & Pan, 2003). Additionally, a population of rat cone bipolar cells have a high density of voltage-gated sodium channels (Pan & Hu, 2000) and sodium spikes have also been reported in photoreceptors (Kawai et al. 2001). Light signals can induce calcium spikes in bipolar cells and they are proposed to boost small light signals at the synaptic terminal (Zenisek & Matthews, 1998; Protti et al. 2000; Ma & Pan, 2003).
The rod calcium spike functions at the other extreme of light stimulation. The timing of regenerative potentials encodes light information when the intensity is strong enough to saturate the peak response of rods. The prolonged undershoot after an intense light stimulus can produce a positive afterimage (Sakitt, 1976). This is because the rods exposed to the strongest lights are hyperpolarized longer and release less transmitter. These rods encode a ‘light’ signal while rods exposed to less light have recovered and transmit a ‘dark’ signal.
The depolarizing overshoot and spike can produce a negative afterimage, since these rods are releasing more transmitter and therefore encoding a ‘darker’ signal. This suggests the following model. If rods are stimulated by a saturating test stimulus that is brighter than a background stimulus to adjacent rods, then the test rods are initially more hyperpolarized than adjacent rods, release less transmitter, and therefore encode a ‘brighter’ signal than background rods. Correspondingly, the background rods depolarize earlier and therefore may have an earlier spike, which again would represent a positive afterimage in the test rods. These signals produce the positive afterimage. However, after a further delay the test rods depolarize and produce a voltage overshoot and spike, they release more transmitter than the background rods, and therefore now the test stimulus is encoded as ‘darker’, the opposite of the original signal and therefore a negative afterimage. If no overshoot occurs during the recovery phase of rod light response, then only a positive afterimage occurs. When there is a voltage overshoot and regenerative depolarization, a negative afterimage could occur after the positive image (Fig. 9).
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Detection of rod action potentials
In this study, we show for the first time that regenerative potentials can be observed in rods during the recovery phase of the light response under normal physiological conditions. However, regenerative potentials were only observed in about 25% of rods, although calcium spikes could be induced in all rods by blocking potassium channels with 40 mM TEA. Perhaps the state of individual retinas determined whether we would observe rod spiking. Though we dark-adapted the animals before all experiments, the process of making the retinal slice may have exposed the retina to a small amount of light. Therefore it is possible that retinas were in different adaptational states. This might explain why we consistently observed rod spikes in some retinas and not in others.
Although rod calcium spikes have not been reported before under normal physiological conditions, it is not likely to be an artifact of our procedures. We obtained the same results when using the less invasive gramicidin perforated patch method and we observed transynaptic events that corresponded to rod spikes. There have been other reports of delayed light responses, appearing from 2 to 10 s after offset of a light stimulus, in turtle and frog retina (Chino & Sturr, 1975a,b; Zeise & Hamdorf, 1983; Protti et al. 2000). These signals were proposed to originate in the rod. In addition, field potential recordings have detected an e-wave that has the same temporal properties and intensity sensitivity as the rod spike (Newman & Lettvin, 1978). It is likely that the whole-cell recording technique, as compared with previous sharp electrode recordings, allowed for the detection of calcium spikes by reducing leak. Blocking potassium channels, which decreases membrane conductance and increases rod excitability, always induces spontaneous calcium spikes (Fain et al. 1980) (also see Fig. 3). This indicates that all rods are capable of spike formation.
The source of the current undershoot was not determined. Torre and colleagues found that the current response of a rod to light had a prominent undershoot when a high concentration of Ca2+ buffer (10 mM BAPTA) was present in the cytoplasm, but not in control conditions (Torre et al. 1986). A conclusion from their work was that a slowing of calcium changes in the outer segment of isolated rods could produce a current undershoot. Our results show that when using perforated patch method, which presumably maintained the internal Ca2+ buffers of the cell, the undershoot was still observed (Fig. 5). The reason for this discrepancy is not clear. One piece of evidence showing that the rod's internal content was conserved during the perforated patch recording was that the time to peak of the current response to increasing intensities of light decreased (dashed line in Fig. 5A) (Baylor & Hodgkin, 1974; Baylor et al. 1979). This was also seen in Torre's study in the control responses (Torre et al. 1986, Lamb et al. 1986). The undershoot they observed was much larger than the one seen in our experiments, but it did show a light intensity-dependent delay. It is possible that rods in situ do not have the same transmembrane calcium flux and that slows calcium changes in the outer segment, accounting for the current undershoot in our experiments. Alternatively, a voltage-independent process in the inner segment may be responsible for the current undershoot.
Repolarization after the calcium spike
What accounts for the repolarization of the calcium spike? Large conductance Ca2+-activated potassium channels contribute to the shape of spikes (Fig. 3). However, blocking the BK channels had no consistent effect on the length of the action potentials (Fig. 3). It is possible that other potassium channels turn off the Ca2+ action potentials. However, when almost all the potassium currents in rods are blocked, Ca2+ action potentials are spontaneous and oscillatory (Fig. 2B). Therefore K+ channels are not necessary for repolarization of Ca2+ action potentials. Calcium-activated chloride current is not necessary for repolarization either because the oscillatory spikes are also observed in gramicidin perforated patch recordings that preserve the Cl– concentration inside the cell. In salamander rods, the Cl– reversal potential is about –20 mV (Thoreson et al. 2002) and hence not hyperpolarizing. Fain and coauthors also found that the Cl– conductance had no effect on the Ca2+ spike oscillation (Fain et al. 1980). Therefore the most likely candidate is the Ca2+ channel itself. The L-type Ca2+ channels in retinal photoreceptors are traditionally regarded as having little or no voltage-dependent inactivation (Corey et al. 1984; von Gersdorff & Matthews, 1996). However, in a recent study, Rabl and Thoreson found that rod Ca2+ channels inactivate substantially during depolarization (Rabl & Thoreson, 2002). A 5 s depolarization to –20 mV inactivated more than 70% of the Ca2+ current in isolated rods. They also showed that local depletion of Ca2+ ions in the synaptic cleft contributes to a transient decrease of Ca2+ current. These two factors may account for, or contribute to, the repolarization of the Ca2+ action potentials. They may also create a refractory period for the generation of another Ca2+ action potential.
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References |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
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Akopian A, McReynolds J & Weiler R (1991). Short-term potentiation of off-responses in turtle horizontal cells. Brain Res 546, 132–138.[CrossRef][Medline]
Armstrong-Gold CE & Rieke F (2003). Bandpass filtering at the rod to second-order cell synapse in salamander (Ambystoma tigrinum) retina. J Neurosci 23, 3796–3806.
Attwell D & Wilson M (1980). Behaviour of the rod network in the tiger salamander retina mediated by membrane properties of individual rods. J Physiol 309, 287–315.
Awatramani GS & Slaughter MM (2002). Origin of transient and sustained responses in ganglion cells of the retina. J Neurosci 20, 7087–95.
Bader CR & Bertrand D (1984). Effect of changes in intra- and extracellular sodium on the inward (anomalous) rectification in salamander photoreceptors. J Physiol 347, 611–631.
Barnes S (1994). After transduction: response shaping and control of transmission by ion channels of the photoreceptor inner segments. Neuroscience 58, 447–459.[CrossRef][Medline]
Barnes S & Deschenes MC (1992). Contribution of Ca and Ca-activated Cl channels to regenerative depolarization and membrane bistability of cone photoreceptors. J Neurophysiol 68, 745–755.
Barnes S & Hille B (1989). Ionic channels of the inner segment of tiger salamander cone photoreceptors. J Gen Physiol 94, 719–743.
Baylor DA & Fuortes MG (1970). Electrical responses of single cones in the retina of the turtle. J Physiol 207, 77–92.
Baylor DA & Hodgkin AL (1974). Changes in time scale and sensitivity in turtle photoreceptors. J Physiol 242, 729–758.
Baylor DA, Lamb TD & Yau KW (1979). The membrane current of single rod outer segments. J Physiol 288, 589–611.
Burkhardt DA, Zhang SQ & Gottesman J (1991). Prolonged depolarization in rods in situ. Vis Neurosci 6, 607–614.[Medline]
Chino YM & Sturr JF (1975a). The time course of inhibition during the delayed response of the on-off ganglion cell in the frog. Vision Res 15, 185–191.[CrossRef][Medline]
Chino YM & Sturr JF (1975b). Rod and cone contributions to the delayed response of the on-off ganglion cell in the frog. Vision Res 15, 193–202.[CrossRef][Medline]
Corey DP, Dubinsky JM & Schwartz EA (1984). The calcium current in inner segments of rods from the salamander (Ambystoma tigrinum) retina. J Physiol 354, 557–575.
Fain GL, Gerschenfeld HM & Quandt FN (1980). Calcium spikes in toad rods. J Physiol 303, 495–513.
Fain GL & Quandt FN (1980b). The effects of tetraethylammonium and cobalt ions on responses to extrinsic current in toad rods. J Physiol 303, 515–533.
Hille B (2001). Ionic Channels of Excitable Membranes, 3rd edn. Sinauer Associates, Sunderland, MA, USA.
Kawai F, Horiguchi M, Suzuki H & Miyachi E (2001). Na+ action potentials in human photoreceptors. Neuron 30, 451–458.[CrossRef][Medline]
Kyrozis A & Reichling DB (1995). Perforated-patch recording with gramicidin avoids artifactual changes in intracellular chloride concentration. J Neurosci Meth 57, 27–35.[CrossRef][Medline]
Lamb TD, Matthews HR & Torre V (1986). Incorporation of calcium buffers into salamander retinal rods: a rejection of the calcium hypothesis of phototransduction. J Physiol 372, 315–349.
Ma YP & Pan ZH (2003). Spontaneous regenerative activity in mammalian retinal bipolar cells: roles of multiple subtypes of voltage-dependent Ca2+ channels. Vis Neurosci 20, 131–139.[CrossRef][Medline]
McNaughton PA (1990). Light response of vertebrate photoreceptors. Physiol Rev 70, 847–883.
Maricq AV & Korenbrot JI (1988). Calcium and calcium-dependent chloride currents generate action potentials in solitary cone photoreceptors. Neuron 1, 503–515.[CrossRef][Medline]
Miyachi E, Takahashi K & Murakami M (1984). Electrically evoked calcium responses in rods of the frog retina. Jpn J Physiol 34, 307–318.[Medline]
Moriondo A, Pelucchi B & Rispoli G (2001). Calcium-activated potassium current clamps the dark potential of vertebrate rods. Eur J Neurosci 14, 19–26.[CrossRef][Medline]
Newman EA & Lettvin JY (1978). Relation of the epsilon-wave to ganglion cell activity and rod responses in the frog. Vision Res 18, 1181–1188.[CrossRef][Medline]
Normann RA & Werblin FS (1974). Control of retinal sensitivity. I. Light and dark adaptation of vertebrate rods and cones. J Generalphysiol 63, 37–61.
Pan ZH & Hu HJ (2000). Voltage-dependent Na+ currents in mammalian retinal cone bipolar cells. J Neurophysiol 84, 2564–2571.
Penn RD & Hagins WA (1972). Kinetics of the photocurrent of retinal rods. Biophys J 12, 1073–1094.
Piccolino M & Gerschenfeld HM (1980). Characteristics and ionic processes involved in feedback spikes of turtle cones. Proc R Soc Lond B 206, 439–463.[Medline]
Protti DA, Flores-Herr N & von Gersdorff H (2000). Light evokes Ca2+ spikes in the axon terminal of a retinal bipolar cell. Neuron 25, 215–227.[CrossRef][Medline]
Rabl K & Thoreson WB (2002). Calcium-dependent inactivation and depletion of synaptic cleft calcium ions combine to regulate rod calcium currents under physiological conditions. Eur J Neurosci 16, 2070–2077.[CrossRef][Medline]
Sakitt B (1975). Locus of short-term visual storage. Science 190, 1318–1319.
Sakitt B (1976). Psychophysical correlates of photoreceptor activity. Vision Res 16, 129–140.[CrossRef][Medline]
Sakitt B & Long GM (1979). Spare the rod and spoil the icon. J Exp Psychol Hum Percept Perform 5, 19–30.[CrossRef][Medline]
Thoreson WB & Burkhardt DA (1991). Ionic influences on the prolonged depolarization of turtle cones in situ. J Neurophysiol 65, 96–110.
Thoreson WB, Stella SL Jr, Bryson EI, Clements J & Witkovsky P (2002). D2-like dopamine receptors promote interactions between calcium and chloride channels that diminish rod synaptic transfer in the salamander retina. Vis Neurosci 19, 235–247.[CrossRef][Medline]
Torre V, Matthews HR & Lamb TD (1986). Role of calcium in regulating the cyclic GMP cascade of phototransduction in retinal rods. Proc Natl Acad Sci U S A 83, 7109–7113.
von Gersdorff H & Matthews G (1996). Calcium-dependent inactivation of calcium current in synaptic terminals of retinal bipolar neurons. J Neurosci 16, 115–122.
Wu SM (1987). Synaptic connections between neurons in living slices of the larval tiger salamander retina. J Neurosci Methods 20, 139–49.[CrossRef][Medline]
Xu JW & Slaughter MM (2005). Large-conductance calcium-activated potassium channels facilitate transmitter release in salamander rod synapse. J Neurosci 25, 7660–7668.
Yang XL & Wu SM (1996). Response sensitivity and voltage gain of the rod- and cone-horizontal cell synapses in dark- and light-adapted tiger salamander retina. J Neurophysiol 76, 3863–3874.
Yang XL & Wu SM (1997). Response sensitivity and voltage gain of the rod- and cone-bipolar cell synapses in dark-adapted tiger salamander retina. J Neurophysiol 78, 2662–2673.
Zeise ML & Hamdorf K (1983). Two late response components in on-off ganglion cells of the frog retina: the delayed response-generated by red rods; the second off-response-generated by green rods. Vision Res 23, 887–893.[CrossRef][Medline]
Zenisek D & Matthews G (1998). Calcium action potentials in retinal bipolar neurons. Vis Neurosci 15, 69–75.[CrossRef][Medline]
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Acknowledgements |
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Author's present address
J. W. Xu: Division of Neurology, Children's Hospital of Philadelphia, 409 D Abramsson, 3615 Civic Center Blvd, Philadelphia, PA 19104, USA.
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) was observed in each of a series of traces. The bar represents light stimuli of 1 s. C, in the dark-adapted wholemount retina, EPSCs were recorded from a ganglion cell clamped to –70 mV and stimulated with a bright, 1 s light. Two delayed EPSCs occurred after the cessation of the light response.
