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Department of Biomedical Science, Florida Atlantic University, Boca Raton, Florida
Submitted 21 October 2004; accepted in final form 14 June 2005
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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The first synapse in retina is modulated by light stimulation through a long feedback system mediated by interplexiform cells (Dowling 1991
; Knapp and Dowling 1987; Maguire and Werblin 1994; Mangel and Dowling 1987). In some retinas, interplexiform cells release dopamine that can alter the postsynaptic receptor responses to the photoreceptor neurotransmitter: glutamate. In this study, I focus on a much more local and direct regulation of this first synapse. Horizontal cells are depolarized by glutamate released from photoreceptors. However, horizontal cells also possess both GABA and glycine receptors. Activation of either "inhibitory" receptor will also depolarize horizontal cells because of their inherent high internal chloride concentration. Thus all three transmitter systems can work synergistically at the horizontal cell membrane, although thus far, the functional significance of this potential action has not been revealed.
A recent report indicated that glycine receptor function can be regulated by the level of free internal calcium in neurons. In spinal cord neurons and cell expression systems, glycine receptor responses can be up-regulated by raising intracellular calcium (Fucile et al. 2000; Xu et al. 1999). Retinal neurons, which are postsynaptic to photoreceptors, possess glutamate receptors that may be calcium permeable. In addition, there neurons possess voltage-gated calcium channels. In particular, horizontal cells possess L-type calcium channels and calcium-permeable glutamate receptors (Okada et al.1999; Rivera et al. 2001; Schultz et al. 2001). Therefore if these mechanisms and channels are juxtaposed, it raises the possibility that postsynaptic glycine receptors could be regulated by input from photoreceptors. My experiments indicate that this mechanism is operational in horizontal cells. It is relatively quiescent in the dark-adapted retina, but is activated by a brief light stimulation. Because the glycine current in horizontal cells has a reversal potential close to that of glutamate, this mechanism allows for a state-dependent facilitation of photoreceptor action at the horizontal cell membrane.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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Larval tiger salamanders (Ambystoma tigrinum) were purchased from Kons Scientific (Germantown, WI) and Charles Sullivan (Nashville, TN). The animals were kept in a cold room (4°C) with a 12-h dark and light cycle before the experiments. The animals were stunned, decapitated, and double-pithed, and the eyes were enucleated according to National Institute of Health Guide for the Care and Use of Laboratory Animals.
The retinal slices were prepared in a dark room using infrared illumination. Briefly, a retinal tissue was extracted from the eyeball in Ringer solution, and the retina was mounted ganglion cell layer down on microfilter paper (Millipore, Bedford, MA). The filter paper with retinal tissue was vertically cut at 250 µm in a cutting chamber using a tissue slicer (Stoelting Co.). A single retinal slice was moved into a recording chamber, placed on a stage of microscope (BX50W, Olympus) equipped with a x60 water-immersion objective (NA 0.9), and viewed under an infrared intensify CCD camera system. The retinal slice was kept in the dark and perfused with oxygenated Ringer solution that consisted of (in mM) 111 NaCl, 2.5 KCl, 1.8 CaCl2, 1 MgCl2, 5 HEPES, and 10 dextrose (pH 7.8).
Glycine receptors were studied in horizontal cells in the retinal slice preparation under dark conditions, and the retina was briefly light-adapted by a train of light stimuli generated by a combination of a dim red (670 nm) and a dim green (520 nm) LED, with a 3-s ON-OFF duty cycle. The recordings made from horizontal cells in a dark-adapted retinal slice were obtained from animals kept in darkness for at least 6 h.
In the dissociated retinal cell preparation, the retina was digested for 30–45 min in a papain solution that contained DNAse and L-cysteine. The cells were mechanically dissociated in calcium-free Ringer solution after the enzymatic treatment. The isolated cells were seeded on a 12-mm coverslip coated with lectin. After the cells settled for 30 min, the coverslip was moved into a recording chamber and perfused with oxygenated Ringer solution.
All the chemicals were locally applied on isolated horizontal cells through a fast drug exchange system (DAD-12, ALA Scientific Co.). In the tissue slice preparation, drug application was through a gravity-driven perfusion system. All chemicals were purchased from Sigma-Aldrich.
Whole cell and perforated patch-clamp recording
Whole cell and perforated patch recordings were made from horizontal cells in dissociated and retinal slice preparations using low resistance electrodes (3–5 M
). Whole cell recording electrodes were filled with a solution containing (in mM) 65 K-gluconate, 40 KCl, 1 MgCl2, 5 EGTA, and 10 HEPES, with "ATP regenerating cocktails" consisting of (in mM) 20 ATP, 40 phosphocreatine, and 2 creatine phosphatase. In some experiments, 10 mM BAPTA was added to the electrode solution and introduced into horizontal cells through whole cell recording electrodes.
The gramicidin perforated patch technique was used for maintaining intracellular chloride concentration, because gramicidin forms pores that are only permeable to monovalent cations. Gramicidin was dissolved in DMSO at a concentration of 500 mg/ml as a stock and was diluted 1,000 times in the electrode solution and sonicated before the experiments. Whole cell recording electrodes were filled with the gramicidin solution. Chloride reversal potential in horizontal cells was measured in the gramicidin perforated patch experiments.
Cobalt staining
The cobalt staining technique was used to identify calcium-permeable glutamate receptors (Pruss et al. 1991). In general, the retinas were treated with 25 µM kainate, an ionotropic glutamate receptor agonist, in calcium-free cobalt uptake solution containing 3 mM CoCl2 and 100 µM AP-7 to block N-methyl-D-aspartate (NMDA) receptors. After a 30-min incubation, the cobalt-stained retinas were precipitated in 1.2% (NH4)2S. Formaldehyde (4%) fixation followed the precipitation solution. Cobalt precipitation was enhanced with 0.2% AgNO3. The cobalt stained retinas were vertically cut at 200 µm, and cobalt-positive horizontal cells were observed under the Olympus microscope.
Calcium imaging
Calcium fluorescence-imaging measurements were performed using an intensified CCD camera (Video Scope International) and a calcium-sensitive fluorescence dye. The imaging system was controlled by an Axon Workbench imaging program (Axon Instruments) installed in a Dell computer. Fluo-4 potassium (5 µM), a fluorescence calcium indicator, was introduced into horizontal cells through a recording electrode. The calcium indicator was excited by 480-nm excitation light. The emission fluorescence was passed through a dichroic filter with a 520-nm barrier filter. Intracellular calcium levels were measured by monitoring the changes of fluorescence intensity. The fluorescence measurements were collected in horizontal cell soma with acquisition rate of one sample every 6 s. The data were analyzed by the Axon imaging program.
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RESULTS |
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Glycine responses were studied on isolated horizontal cells in voltage clamp experiments. Horizontal cells were stepped to a series of potentials between –90 and +10 mV from a holding voltage of –55 mV using gramicidin perforated patch technique. Horizontal cells were clamped at each voltage for 1 s, followed by a 1-s application of 50 µM glycine at each potential. Results from a representative cell and a summary of glycine current-voltage (I-V) plot from eight horizontal cells are shown in Fig. 1, A and B. In control conditions, the glycine current was linear from –90 to –40 mV, which is the normal operational range of horizontal cells. The glycine current began to rectify at about –40 mV, and the rectification became steeper at or above –20 mV. Rectification of glycine currents has been reported in several studies from different neurons (Harty and Manis 1996; Melnick and Baev 1993). In this study, glycine current rectification occurs at a voltage where voltage-dependent calcium channels are activated in horizontal cells (Linn and Gafka 2001; Ueda et al. 1992). It is possible that the glycine current rectification might be induced by activation of voltage-dependent calcium channels. To test this possibility, 50 µM cadmium was used to block calcium influx through voltage-dependent calcium channels in the horizontal cells. The glycine currents at each voltage step were measured in the presence of cadmium. The cadmium completely blocked the outward rectification of glycine currents, and the glycine I-V plot calculated from six horizontal cells showed linear properties in the presence of cadmium (Fig. 1C). This result indicates that activation of voltage-dependent calcium channels increases intracellular calcium, leading to a potentiated glycine response in the horizontal cells. If the glycine response is calcium sensitive, BAPTA, a fast calcium buffer, should reduce or remove the effect of calcium on glycine receptors. BAPTA (10 mM) was added in the electrode solution and introduced into the horizontal cells during whole cell recordings. Again, the amplitudes of glycine currents were measured at different voltage steps from –70 to +30 mV, with 20-mV step increments. The glycine I-V plot was generated from five isolated horizontal cells in the presence of 10 mM BAPTA. Figure 1D shows that, in the presence of BAPTA, the glycine I-V plot is linear. These experiments indicate that outward rectification of the glycine current is associated with elevated intracellular calcium. It also indicates that factors that depolarize horizontal cells and activate voltage-gated calcium channels can induce glycine receptor plasticity in horizontal cells.
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; Sullivan and Lasater 1992). To study potential interactions between glycine currents and L-type voltage-dependent calcium channels, 25 µM nifedipine was used to block the L-type channels. The same experimental protocol was used as in Fig. 2, A and B. In controls, after the cell was depolarized to –10 mV, glycine generated a larger response at the 6-s time-point compared with the 1-s time-point. When nifedipine was applied, glycine responses were slightly affected by the different time course after step to –10 mV. The amplitudes of glycine currents at these two time-points were almost equal (Fig. 2C). Compared with nifedipine, which blocks L-type calcium channels, cadmium is a wide spectrum blocker of voltage-dependent calcium channels. The action of 25 µM cadmium duplicated the effect of nifedipine in the same cells (Fig. 2D), suggesting that L-type calcium channels are the predominant voltage-gated calcium channels that are capable of enhancing glycine currents in horizontal cells. The control and drug effects were compared by calculating the percentage change of normalized peak outward currents at the 6-s with respect to the 1-s time-point. The results are shown in Fig. 2E. The statistics show that, under control conditions, the average current increase at the 6-s time-point was 22.8 ± 13.9% (SD; n = 4; range, 8.9–58%). However, there was no significant change in the current amplitude at these two time-points if BAPTA, nifedipine, or cadmium was applied (Fig. 2E). The changes in glycine current between these two time-points were 1.2 ± 1 (n = 7), –0.5 ± 1.1 (n = 5), and –0.5 ± 1% (n = 5) in the presence of BAPTA, nifedipine, and cadmium, respectively. These results indicate that an increase of intracellular calcium leads to an enhancement of glycine responses in horizontal cells. L-type voltage-dependent calcium channels and glycine receptors are close to each other. Thus calcium influx through L-type voltage-dependent calcium channels is a source that triggers glycine receptor plasticity in horizontal cells.
Calcium permeable glutamate receptors potentiate glycine response in horizontal cells
Another potential way to increase internal calcium in horizontal cells is through ligand-activated, calcium-permeable channels. Glutamate released by photoreceptors may activate ionotropic or metabotropic receptors on horizontal cells, potentially leading to a change of internal calcium level. Glutamate depolarizes horizontal cells by activating ionotropic kainate and AMPA receptors (Shen et al. 2004). However, there is no evidence that NMDA receptors are expressed in amphibian retinal horizontal cells (Slaughter and Miller 1983; Yang and Wu 1990). Based on our previous studies in human horizontal cells (Shen et al. 2004), 5 µM kainate was used as the ionotopic glutamate receptor agonist to mimic the effect of glutamate in horizontal cells.
Experiments were performed on acutely dissociated retinal horizontal cells. Dissociated horizontal cells were identified by the morphological and electrophysiological properties (Gilbertson et al.1991; Han et al. 2000; Miller and Dacheux 1983; Picaud et al. 1998; Stockton and Slaughter 1991). The horizontal cells were voltage clamped at –55 mV, below the glycine reversal potential that is approximately –30mV (see Fig. 1). Glycine currents were studied with or without pretreatment of 5 µM kainate. When 50 µM glycine alone was rapidly puffed onto the horizontal cells at the holding potential, it elicited an inward current (Fig. 3 A, black trace). After removal and recovery from glycine application, 5 µM kainate was applied to the horizontal cell. A small inward current was observed under the low dose of kainate (Fig. 3A, gray trace). In the presence of kainate, the peak glycine currents were enhanced (Fig. 3A, gray trace), suggesting that glycine receptor sensitivity was increased by the glutamate analog. Overall, pretreatment with the kainate enhanced the glycine currents by 79.5 ± 13.3% (n = 5; range, 51.2–94.6%; Fig. 3, right).
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). Cobalt can pass through ionotropic glutamate receptors but not through voltage-dependent calcium channels. In the cobalt precipitating experiments, 10 µM kainate was used to activate calcium permeable glutamate receptors in intact retinas. Figure 3B is an example of vertical cross-sections of cobalt-stained retinas treated with or without 10 µM kainate. In the control slice, light cobalt-positive staining, could be observed only in the inner plexiform layer and the outer plexiform layer where horizontal cell dendrites are located. Very light staining was observed in the horizontal cell somatic layer. After the retina was treated with kainate, a strong cobalt-positive staining pattern was observed in the retinal slices. Cobalt-positive horizontal cells were identified in the retinal slice (Fig. 3B, white arrows). Because cobalt blocks chemical synaptic transmission, this result is direct evidence that kainate activates calcium permeable ionotropic glutamate receptors in the horizontal cells. The effects of glutamate were similar to the effects of kainate on isolated horizontal cells. The horizontal cells were voltage clamped at –55 mV. Glycine currents were studied with or without pretreatment of 20 µM glutamate using the same protocol described previously in kainate experiment. Glycine (50 µM) alone elicited an inward current that was enhanced in the presence of 20 µM glutamate (Fig. 4 A), a low concentration of glutamate that produced a small inward current. To verify that the effect of glutamate was on chloride permeable glycine receptors, 1 µM strychnine, a glycine receptor antagonist, was added to the bath solution. Strychnine fully blocked glycine currents in both control and in glutamate-pretreated conditions, leaving a small glutamate current (Fig. 4B, gray trace). This indicates that strychnine-sensitive glycine receptors are modulated by glutamate. The effects of glutamate and strychnine were robust and seen on all of the tested horizontal cells.
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Repetitive light stimulation enhances horizontal cell response to glycine
The physiological significance of glycine receptor modulation was studied in the dark adapted retinal slice. The salamanders were kept in the dark for several hours before the experiments, and all procedures were performed under infrared light. Initial experiments measured internal free calcium. Fluo-4 (10 µM), a membrane-impermeable fluorescent calcium indicator, was introduced into a horizontal cell in the retinal slice through a recording electrode. The calcium indicator was excited by a very brief (50 ms) excitation stimulus of 480 nm. The intracellular free calcium change was monitored every 6 s in dark. After the baseline calcium signal was established, the retinal slice was exposed to a repetitive light stimulation paradigm consisting of the green and red stimuli (see METHODS). The repetitive light stimulation resulted in an increase in basal free calcium in the horizontal cell (Fig. 5 A).
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The repetitive light stimuli paradigm led to an increase in the horizontal cells response to 50 µM glycine. To study the behavior of glycine receptors during this experiment, glycine responses were recorded from horizontal cells in the retinal slice under gramicidin perforated patch configuration. The horizontal cells were voltage clamped at –50 mV. When 50 µM glycine was applied to a fully dark-adapted retinal slice, it generated an inward current in horizontal cells (Fig. 5C, dark trace). The inward glycine current was caused by chloride efflux through glycine receptors in horizontal cells (Miller and Dacheux 1983). The glycine was removed, and the cell was allowed to recover while remaining in the dark. Then the retinal slice was stimulated by the repetitive light stimuli. A small postsynaptic inward current was generated at the holding voltage after 3- to 5-min exposure to the light stimuli (Fig. 5C, *). This inward current corresponded to the depolarization described in Fig. 5B. The average postsynaptic inward current was 42.9 ± 31.8 pA (n = 10; range, 22–107 pA). Then 50 µM glycine was reapplied. The glycine current was larger in amplitude, and the current response was faster than that observed before the light stimuli (Fig. 5C, gray trace). The potentiation was observed in 7 of 10 horizontal cells that responded to the glycine application. The average current increase was 50.1 ± 32.6% (n = 7; range, 18.3–102%). The other three cells had no significant change in glycine current after the brief light adaptation.
Regulation of glycine response by intracellular calcium during light stimulation
The implication of these experiments is that there is a causal link between the elevated internal calcium produced by light stimulation and the enhanced glycine current. The prediction is that buffering internal calcium would reduce or eliminate the effect of the light stimuli on the glycine current. Experiments in Fig. 4 showed that BAPTA could reduce the exogenous glutamate potential glycine current in isolated horizontal cells. If the effects of light stimulation could be explained by the same mechanism, BAPTA should also block the enhancement of glycine induced by the light stimulation. The experimental protocol described in Fig. 5C was repeated, but with 10 mM BAPTA included in the electrode. Briefly, horizontal cells were voltage clamped at –55 mV and 50 µM glycine was applied for a few seconds (Fig. 5D, black trace). This produced a small, slowly rising glycine current. Then, 50 µM glycine was reapplied after a train of light stimuli was applied. Unlike control experiments, (Fig. 5C), the calcium buffer suppressed enhancement of glycine current. Interestingly, the postsynaptic inward current is evident (*), indicating that the light stimulation still induced an increase of photoreceptor transmitter release. Without BAPTA in the internal solution, the light stimulation increased the average glycine currents by almost 50%. With BAPTA, the average increase was 
10% (Fig. 5E). BAPTA largely reduced enhancement of glycine current by light stimulation. The results indicated that light stimulation induces glycine receptor plasticity by modulation of intracellular calcium in horizontal cells.
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DISCUSSION |
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; Smiley and Basinger 1988; Smiley and Yazullar 1990; Yang and Yazulla 1988). According to my experiments, the glycine feedback signal could be locally amplified in horizontal cells by synergistic regulation from glutamate input during light stimulation.
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Neurotransmitter receptor plasticity has been considered as an underlying mechanism of neural adaptation and modulation in the CNS that has been studied for many years. Most studies were carried out by application of electrical stimulation in neural tissues. In this study, a physiological stimulus, light, was used to induce glycine receptor plasticity in the sensory neurons. Interestingly, light stimulation–induced glycine receptor plasticity in horizontal cells is a network effect involving two inputs: a feedforward glutamatergic pathway and a centrifugal glycinergic feedback pathway. Both effects are positive to horizontal cells. The positive glycinergic feedback signal is locally amplified by reciprocal mechanisms during repetitive light stimulation. In general, glutamate input is a primary source of horizontal cell excitation, whereas the effect of glycine is through neural feedback and complements the effect of glutamate. Hence, a persistent glycine effect facilitated by repetitive stimulation would increase the operational range of horizontal cells to the primary input, glutamate. Yang and Wu (1992) found that voltage gain at the photoreceptor to horizontal cell synapse increases about 10-fold under ambient light conditions. The glycinergic feedback might mediate synaptic gain control in the distal retina.
The repetitive light stimulation promoted a glutamate-mediated depolarization in horizontal cells. This is an interesting phenomenon, indicating that the glutamate level in the distal retina might be increased by the flash stimulation paradigm. This also suggests that the frequent light stimulation may change the state of the retina from the dark-adapted state to the light-adapted state. According to psychophysical and neurophysiological studies, rods are very active in the dark-adapted, scotopic condition. Rods suppress cone release of glutamate in scotopic conditions (Frumkes et al. 1992; Goldberg et al. 1983). This tonic suppression is largely reduced in mesopic conditions when retinas are exposed to a background light or a flicking light stimulation to reduce rod activation (Frumkes and Eysteinsson 1987, 1988). It is possible that, under my experimental condition, rod-cone suppression was significant in the dark-adapted retina. Therefore glutamate input to horizontal cells was suppressed in control conditions. During the frequent light stimulation, rods might be suppressed, which would enhance cone input to horizontal cells. Thus release of rod-cone suppression would cause horizontal cells to depolarize. Indeed Fig. 5B shows that the offset light response of the horizontal cell to the green stimuli (*) became much faster after 5-min exposure to the frequent flash stimulation (top trace) compared with in the dark-adapted state (bottom trace). The fast offset light response is a indication of increase of cone input (Wu 1987). Thus the repetitive light stimulation paradigm may enhance glutamate release from cones by reducing rod suppression. The consequence of the action is to increase network glycine response in the horizontal cells.
Alteration of postsynaptic glycine response was also observed in salamander ganglion cells under light adaptation (Cook et al. 2000). According to their study, light adaptation increases glycine inhibitory postsynaptic currents (IPSCs) on the ganglion cells. It seemed that picrotoxin block of GABAC receptors also up-regulates glycine IPSCs. However, it is unclear the mechanism of the action in the ganglion cells. It is possible that glutamate input might increase in ganglion cells if picrotoxin blocks negative feedback at bipolar cells axon terminals through GABAC receptors. Combined with my experimental results, glycine receptor plasticity may play a role in neural network transduction and adaptation. However, the physiological function of glycine receptor plasticity still needs to be determined.
Co-localization of glycine receptors and glutamate receptors in distal horizontal cells
Glutamate receptors, kainate, and AMPA subtypes exist in horizontal cells (Hack et al. 2001; Okada et al.1999; Vandenbranden et al. 2000). However, there is no evidence that NMDA receptors are present in salamander retinal horizontal cells (Slaughter and Miller 1983; Yang and Wu 1990). However, calcium permeable glutamate receptors have been found to express in horizontal cells (Okada et al. 1999; Rivera et al. 2001). My cobalt-staining experiments indicate that kainate-sensitive glutamate receptors are calcium permeable. Because the regulation of glycine receptors is sensitive to BAPTA, but not EGTA, calcium regulation likely occurs within microdomains near the cytoplasmic membrane. This suggests that glutamate and glycine receptors are co-localized in horizontal cells. Kainate and AMPA receptors express on horizontal cell processes that are postsynaptic to photoreceptors (Hack et al. 2001; Okada et al.1999; Vandenbranden et al. 2000). My studies suggest that glycine receptors are very close to glutamate receptors and therefore are in the synaptic processes of horizontal cells. Possibly calcium entry through glutamate receptors might be the only source for raising internal calcium levels in horizontal cells when the glutamate concentration is insufficient to depolarize the neurons to activate voltage-dependent calcium channels.
Possible intracellular pathways for regulation of glycine receptors
Calcium-permeable glutamate receptors and voltage-dependent calcium channels exist in retinal horizontal cells (Linn and Gafka 2001; Rivera et al. 2001). Calcium influx through these receptors and channels control glycine receptor plasticity in horizontal cells. The calcium regulation by voltage-gated calcium channels and glutamate receptors may be independent because the effects could be generated individually. However, it is unclear whether regulation of glycine receptors is through convergent pathways or through spatially separated pathways.
Glycine receptor apparent affinity can be up-regulated by intracellular calcium, G-proteins, and different cellular protein kinases (Fucile et al. 2000; Wang and Randic 1996; Xu et al. 1996; Yevenes et al. 2003). Among these intracellular pathways, internal calcium seems an essential factor for potentiation of glycine receptors (Fucile et al. 2000; Xu et al. 1999). Studies of cultured spinal cord neurons and transfected human cell line clearly indicate that glycine receptors are modulated by intracellular calcium from glutamate receptors and voltage-dependent calcium channels (Fucile et al. 2000). There are several intracellular transduction pathways found to be related to calcium regulation of glycine receptors, such as protein kinase C, calcium calmodulin-dependent kinase II (CaMKII), or a diffusible cytoplasmic factor (Fucile et al. 2000; Xu et al. 1996, 1999). These intracellular messengers could be candidates for the cellular transduction pathway of light-driven glycine receptor plasticity in horizontal cells. To address this question, further studies are required.
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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FOOTNOTES |
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Address for reprint requests and other correspondence: W. Shen, Dept. of Biomedical Science, Florida Atlantic Univ., Bldg. BC-71, Rm. 229, 777 Glades Rd., Boca Raton, FL 33431 (E-mail: wshen{at}fau.edu)
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REFERENCES |
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