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The Journal of Neuroscience, September 1, 2000, 20(17):6570-6577
Coordinated Transitions in Neurotransmitter Systems for the Initiation and Propagation of Spontaneous Retinal Waves
Z. Jimmy Zhou1, 2 and Dichen Zhao1 Departments of 1 Physiology and Biophysics, and 2 Ophthalmology, University of Arkansas for Medical Sciences, Little Rock, Arkansas 72205
ABSTRACT
TOP
ABSTRACT
INTRODUCTION
Spontaneous waves of excitation in the developing mammalian retina are mediated, to a large extent, by neurotransmission. However, it is unclear how the underlying neurotransmitter systems interact with each other to play specific roles in the formation of retinal waves at various developmental stages. In particular, it is puzzling why the waves maintain a similar propagation pattern even after underlying neurotransmitter systems have undergone drastic developmental changes. Using Ca2+ imaging and patch clamp in a whole-mount preparation of the developing rabbit retina, we discovered two dramatic and coordinated transitions in the excitatory drive for retinal waves: one from a nicotinic to a muscarinic system, and the other from a fast cholinergic to a fast glutamatergic input. Retinal waves before the age of postnatal day 1 (P1) were blocked by nicotinic antagonists, but not by muscarinic or glutamatergic antagonists. After P3, however, the spontaneous wave, whose basic spatiotemporal pattern remained similar, was completely inhibited by muscarinic or glutamate antagonists, but not by nicotinic antagonists. We also found that the muscarinic drive, mediated primarily by M1 and M3 receptors, was particularly important for wave propagation, whereas the glutamatergic drive seemed more important for local excitation. Our results suggest (1) a novel mechanism by which a neurotransmitter system changes its functional role via a switch between two completely different classes of receptors for the same transmitter, (2) the cholinergic system plays a critical role in not only early but also late spontaneous waves, and (3) the continued participation of the cholinergic system may provide a network basis for the consistency in the overall propagation pattern of spontaneous retinal waves.
Key words: visual development; spontaneous retinal waves; cholinergic amacrine cells; nicotinic and muscarinic receptors; glutamate receptors; calcium imaging; patch-clamp; rabbit retina
INTRODUCTION
In the developing vertebrate retina, rhythmic excitation occurs spontaneously among ganglion and amacrine cells and propagates laterally in local domains in the form of waves (for review, see Catsicas and Mobbs, 1995
; Katz and Shatz, 1996
We investigated the role of two major excitatory neurotransmitters, ACh and glutamate, in spontaneous waves in the developing rabbit retina. ACh is believed to be a critical neurotransmitter for early retinal waves in ferret (Feller et al., 1996
As bipolar cell synapses begin to develop in the IPL, the balance of excitatory inputs to ganglion and amacrine cells is expected to shift from the cholinergic to the glutamatergic system (Wong et al., 2000
We report here two concomitant transitions in the role of ACh and glutamate in spontaneous retinal waves in rabbits: one from a fast cholinergic to a fast glutamatergic drive, the other from a nicotinic to a muscarinic network. Our data also indicate that the glutamatergic and muscarinic drives play different functional roles in retinal waves.
Preliminary results of this study have been published previously in abstracts (Zhao et al., 1999
MATERIALS AND METHODS
Calcium imaging and patch clamp in the flat-mount rabbit retina. Retinal flat mounts were prepared from pigmented (New Zealand Red) and, occasionally, albino (New Zealand White) rabbits as described previously (Zhou, 1998
To load the calcium indicator dye fura-2 AM (Molecular Probes, Eugene, OR) in ganglion and amacrine cells, pieces of the retina were mounted scleral side up on black filter paper (Type HABP; Millipore, Bedford, MA) and incubated in HEPES-based Ames medium (in which NaHCO3 was replaced with 20 mM HEPES) containing 10 µM fura-2 AM and 0.001% pluronic acid for 1 hr at 30°C. The retinas were then transferred into an incubation chamber containing dye-free, HEPES-based Ames at room temperature until the time of recording. During Ca2+ imaging, the recording chamber was continuously superfused (3-4 ml/min) with Ames medium (Ames and Nesbett, 1981
Whole-cell patch-clamp recordings were made from cells in the ganglion cell layer of the whole-mount rabbit retina as previously described (Zhou, 1998
measured in Ames medium and a pipette solution containing (in mM): 95 K-gluconate, 15 KCl, 5 NaOH, 0.5 CaCl2, 2 MgCl2, 5 EGTA, 2 ATP, 0.5 GTP, 2 ascorbic acid, and 10 HEPES. Series resistance was compensated by 50-80% with the series resistance compensation circuitry in the patch-clamp amplifier (Axopatch 200B; Axon Instruments, Foster City, CA).
Data acquisition and analysis. Fluorescence images were collected with Axon Imaging Workbench (AIW) software (Axon Instruments) and analyzed with AIW and Scion Image (Scion Corporation, Frederick, MD). To monitor the excitability of individual cells in the retina, oval zones were drawn around dye-loaded cells using AIW software. The average fluorescence intensity in each zone was plotted as a function of time F(t) with AIW. The relative change in the emission fluorescence intensity (
F/F) was defined as [F(t)
Fo(t)]/Fo(t), where Fo(t) was the baseline intensity, which varied slowly with time as a result of dye bleaching and slow drift of samples out of focus during long periods of recording. Because the duration of spontaneous waves was very brief (~2-3 sec) compared to the interburst interval (~20-300 sec), the baseline fluorescence intensity, Fo(t), could be approximated by fitting F(t) to a polynomial function (or, sometimes, by smoothing with adjacent averaging) using the Origin software (Microcal, Northampton, MA). The result of the fit, Ffit(t), appeared similar to that obtained with a low-pass filter and closely resembled the slowly varying baseline fluorescence intensity (Fo) without rhythmic bursts. Thus,
The propagation of waves was imaged with a low magnification (10 or 4×) objective lens. The wavefront speed (v) was defined as the rate at which the wavefront passed from one point to another along the direction of wave propagation (see Fig. 3). The radial dimension (d) of the wavefront was defined as the radial distance within which |
Patch-clamp data were acquired with pClamp8 software (Axon Instruments) and analyzed with Origin (Microcal). Synchronous acquisition of patch-clamp and imaging data were accomplished by running pClamp8 and AIW programs simultaneously on a Pentium 600 MHz computer through an analog-to-digital converter (Digidata 1320; Axon Instruments).
RESULTS
Spontaneous waves in the developing rabbit retina
Isolated retinas from E26 to P6 (E31 = day of birth = P0) rabbits were loaded with fura-2 AM and imaged with 380 nm illumination. Most of the dye-loaded cells in the ganglion cell layer (GCL) (Fig. 1A) showed rhythmic increases in the intracellular free Ca2+ concentration, indicated by transient decreases in the emission fluorescence intensity of the dye at 500 nm (Grynkiewicz et al., 1985
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Figure 1. Spontaneous waves of rhythmic activity in a P0 retina. A, Fluorescence image of fura-2 AM-loaded cells in the ganglion cell layer taken with a 40× objective lens. B, Relative (%) changes in fluorescence intensity from 16 cells randomly selected from the field of view shown in A. Downward deflections in each trace indicate transient increases in intracellular free Ca2+ concentration. C, Sequential difference images (
The spontaneous activity in the GCL propagated in the form of waves, which could be detected with a low magnification (10 or 4×) objective lens (Fig. 1D). These waves usually passed across the field of view in random directions. The wavefront was 300-600 µm in radial dimension (d) (see definition in Materials and Methods) and propagated at a speed of ~150-300 µm/sec, thus moving past a point in the retina in ~2-4 sec. We also observed waves that originated in the field of view. Some of these waves propagated as two-dimensional plane waves with a nearly circular wavefront and some propagated in a circular or spiral direction. Other waves propagated in irregular shapes at a similar speed. Spontaneous retinal waves with similar overall propagation patterns were detected throughout the developmental period (E26-P6) examined in the study.
Dramatic transitions in the cholinergic and glutamatergic systems during postnatal development
To understand how excitatory drives for retinal waves changed during development, we investigated the effect of antagonists to nicotinic, muscarinic, and glutamate receptors at different stages of development. Application of D-tubocurare (curare; 25-100 µM), a nicotinic receptor antagonist, effectively and reversibly blocked the wave in the newborn (P0) rabbit retina (Fig. 2A). In contrast, the broad-spectrum muscarinic antagonist atropine (1-3 µM) had no significant effect on spontaneous waves at this age (Fig. 2A); neither did ionotropic glutamate receptor antagonists CNQX and D-AP-7 (applied singly or in combination) abolish the wave (Fig. 2A). These results suggest a critical role of the nicotinic, but not the muscarinic or glutamatergic system in early spontaneous waves in the developing rabbit retina.
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Figure 2. Transitions in neurotransmitter systems. A, Early spontaneous waves in P0 retinas were reversibly blocked by D-tubocurare (curare, 25 µM), but not by atropine (2 µM), CNQX (4 µM), or CNQX (4 µM) + D-AP-7 (200 µM). B, The late spontaneous activity in P4 retinas was no longer sensitive to curare (100 µM) but could be blocked by atropine (0.5 µM) and CNQX (4 µM). Scale bars, 20%.
As development proceeded, however, the pharmacology of spontaneous waves changed drastically. The inhibitory effect of nicotinic antagonists started to diminish quickly after P2, such that at P3-P4 even saturating concentrations of the antagonists (e.g., 400 µM curare) usually only reduced, but did not completely block the wave. By P5, the nicotinic antagonists hexamethonium (HEX) (100 µM; Fig. 2A) and curare (400 µM, data not shown) no longer had a significant effect on the wave. On the other hand, waves in rabbits >P2 became surprisingly sensitive to muscarinic antagonists. Atropine (0.5-1 µM), which had no significant effect on retinal waves in rabbits <P2 (Fig. 2A), completely abolished the late (>P2) retinal wave (Fig. 2B). Thus, starting at P2, there was a dramatic transition from a nicotinic to a muscarinic drive for the wave.
Interestingly, we also discovered that the above transition within the cholinergic system was correlated with another profound transition in the fast excitatory drive for the wave
a transition from a nicotinic receptor-mediated to an ionotropic glutamate receptor-mediated drive. Spontaneous retinal waves in rabbits older, but not younger, than P0-P1 could be blocked by specific non-NMDA receptor antagonists CNQX and DNQX (4-20 µM; Fig. 2B), indicating an emergence of an AMPA/KA receptor-mediated input that eventually replaced the nicotinic system as the primary fast excitatory drive for the wave. The NMDA receptor antagonist D-AP-7 (100-200 µM) also had an inhibitory, but much weaker effect, often reducing the wave frequency without completely abolishing the wave (data not shown).
Figure 3 summarizes the effect of nicotinic, muscarinic, and glutamatergic antagonists on the frequency of spontaneous waves between E26 and P6. As shown in the figure, the emergence of muscarinic and glutamatergic inputs occurred during a similar developmental period (P1-P3), with the glutamatergic drive appearing first at ~P0-P1, followed by a muscarinic drive starting at ~P1-P2. The decline of the nicotinic drive also began at ~P2 but had a slightly slower time course, so that the complete withdraw of the nicotinic drive occurred at ~P4-P5, after the muscarinic and glutamatergic inputs were securely established (Fig. 3). Thus, the transitions in the cholinergic and glutamatergic systems were well coordinated, strongly suggesting a dramatic and interrelated change in the role of these neurotransmitter systems in spontaneous retinal waves.
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Figure 3. Summary of the effect (expressed in percentage of control wave frequency) of nicotinic (A), muscarinic (B), and glutamate (C) receptor antagonists between ages E26 and P6. Data were pooled from experiments with various nicotinic, muscarinic, and glutamatergic antagonists. The nicotinic antagonists included D-tubocurare (25-400 µM), HEX (25-100 µM), and mecamylamine (300 µM). The muscarinic antagonists used were atropine (0.5-2 µM) and pirenzepine (0.6-10 µM). Glutamate receptor antagonists included CNQX (2-20 µM) and DNQX (2-10 µM), which were applied either singly or in combination with D-AP-7 (100-200 µM). Data from P6 retinas were obtained in the presence of picrotoxin (30-100 µM) or gabazine (SR95531, 25-50 µM) in both the control and test solutions. Error bars indicate SE. Numbers in parentheses indicate the total number of experiments pooled at each age.
The cholinergic and glutamatergic drives had different functional roles in wave production
To understand the functional role of muscarinic and glutamatergic inputs, we examined the spatiotemporal properties of spontaneous waves after they were partially blocked by submaximal concentrations of pirenzepine (PZ) (a relatively selective antagonist for M1 receptors, see below) and CNQX, which blocks non-NMDA receptors. Because the boundary of the waves often lay outside the field of view and were difficult to quantify, we examined the effect of the above two reversible antagonists on the speed (v) and the radial dimension (d) of the wavefront. Both v and d could be definitively measured under a 10× objective lens (see Materials and Methods). In some experiments, we also included 25-100 µM picrotoxin in the control and the test solution to enhance waves in P3-P6 retinas, so that the waves were more robust and less likely to "run down" during long recording periods (>2 hr) and partial blockade of waves by pirenzepine and CNQX was more easily attainable. Picrotoxin significantly increased the speed, size, and frequency of the wave at this age (Zhao et al., 1999
As shown in Figure 4, low concentrations of pirenzepine consistently reduced v and d by 30 ± 5% (mean ± SE; n = 21; p < 0.0001; t test) and 36 ± 5% (mean ± SE; n = 21; p < 0.0001; t test), respectively. On the other hand, low concentrations of CNQX significantly reduced the frequency and the amplitude (peak
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Figure 4. Effects of nicotinic, muscarinic, and glutamate receptor antagonists on the speed v and the radial dimension d of the wavefront. A, Relative (percentage of control) v and d of the wavefront under partial blockade by subsaturating concentrations of HEX (0.1-2 µM), PZ (0.1-0.3 µM, or 1-2 µM in 100 µM picrotoxin), and CNQX (0.2 µM). Numbers in parentheses indicate the number of waves included in the analysis. Error bars indicate SE. B, Representative waves recorded from a P3 control retina and with 0.3 µM PZ. Images were collected at 2 Hz with an integration time of 300 msec under a 10× objective lens. Arrows indicate the direction of wave propagation. Scale bar, 500 µm. C, Relative changes in the average fluorescence intensity from the circles in B marked with 1 and 2, respectively. The distance between each pair of circles is 932 µm. The speed v, calculated from the time delay between the two peaks in traces 1 and 2, is 167 µm/sec in control and 93 µm/sec in PZ. The radial dimension d, calculated from the product of v and the mean half-amplitude width of the peaks, is 474 µm under control and 233 µm with PZ.
We also tested low concentrations of HEX in the P1 rabbit retina. HEX reduced v and d by 29 ± 8% (mean ± SE; n = 12; p = 0.006; t test) and 34 ± 8% (mean ± SE; n = 12; p = 0.002; t test), respectively (Fig. 4A).
Pharmacological and physiological properties of the cholinergic system
The action of ACh in both the early (<P1) and late (>P2) spontaneous wave was further investigated by perturbing the level of ACh in the retina. Application of ACh (30 µM) reversibly blocked both the early and late wave after a transient increase in Ca2+ concentration in ganglion and displaced amacrine cells (data not shown), suggesting that constant activation and, most likely, desensitization of cholinergic receptors interfered with wave formation. The blocking effect of ACh on the early wave could be mimicked by the nicotinic agonist 1,1-dimethyl-4-phenylpiperazinium (DMPP) (30-50 µM; Fig. 5A; n = 3) but not by muscarine (2.5 µM; n = 3; Fig. 5B), suggesting that activation of muscarinic receptors had little influence on the early wave. Because most cells in the ventricular zone of the rabbit retina are strongly excited by muscarinic activation at this age (Wong, 1995
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Figure 5. Effects of nicotinic and muscarinic agonists. Application of 50 µM DMPP reversibly blocked the wave after a brief excitation in both P0 (A) and P2 (C) retinas. Muscarine (2.5 µM) reversibly blocked waves in P2 (D) but not in P0 (B) retinas.
In contrast, bath application of muscarine (2 µM, n = 4) after P2 reversibly blocked the wave (Fig. 5D) consistent with the age dependence of the atropine effect (Fig. 2B). However, unlike curare, DMPP (30 µM) continued to block the wave after P3 (Fig. 5C; n = 2), suggesting that nicotinic receptors remained functional in these cells after the transitions, perhaps to play a role other than directly mediating spontaneous retinal waves. This is also consistent with the fact that ganglion cells in the adult rabbit retina respond to nicotinic agonists with increases in the intracellular free Ca2+ concentration (Baldridge, 1996
Altering the temporal pattern and concentration of endogenously released ACh with the cholinesterase inhibitor neostigmine also had age-dependent effects on spontaneous waves. Waves at E30-P2 (n = 6) were only minimally affected by neostigmaine (4-8 µM), showing a slight and transient reduction in wave frequency (data not shown). However, in three of the five retinas tested at P4-P6, neostigmine (2-4 µM) significantly inhibited the wave (data not shown), suggesting that the rate at which ACh was degraded after the release had a more pronounced effect on the late wave than on the early wave. This is consistent with our conclusion that ACh plays different roles before and after P2-P3.
The identities of nicotinic and muscarinic receptors involved in the wave were further investigated by using more specific antagonists. The action of curare in early waves could be mimicked by hexamethonium (Fig. 6A) and mecamylamine (data not shown), but not by
-bungarotoxin (Fig. 6B; n = 3), an antagonist specific for neuronal nicotinic receptors containing
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Figure 6. Pharmacology of the nicotinic and muscarinic drive for the spontaneous wave. The spontaneous activity in a P0 retina was reversibly blocked by 50 µM HEX (A), but was not blocked by
To understand whether muscarinic antagonists blocked synaptic inputs to ganglion cells during late retinal waves, patch-clamp recordings were made from ganglion cells in conjunction with Ca2+ imaging in the whole-mount retina. Figure 7 shows an example of simultaneous patch-clamp recording and fluorescence imaging from a P4 retina. The retina was first loaded with fura-2 AM and imaged under a 40× objective lens (Fig. 7B) to determine the presence of spontaneous waves and the location of cells participated in the waves (Fig. 7C). A rhythmically bursting ganglion cell (Fig. 7A-C, arrow) was then selected for voltage-clamp recording, while the vicinity of the cell (Fig. 7B, oval area enclosed by the dashed line) was simultaneously imaged for changes in free Ca2+ concentration (Fig. 7D). In general, the bursts of synaptic currents in the ganglion cell closely correlated with the rhythmic appearance of spontaneous waves in the local region of the retina. Application of 2 µM of atropine readily blocked both rhythmic synaptic currents in the ganglion cell and Ca2+ waves (Fig. 7D). The blocking effect of atropine was partially reversible after washing out the drug for >10 min (data not shown). These results suggest that synaptic transmission to ganglion cells during the late wave was critically dependent on muscarinic interactions. The site and nature of the muscarinic action are still under investigation.
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Figure 7. Simultaneous patch-clamp and optical measurement of the atropine effect on late retinal waves and synaptic inputs to ganglion cells. A, A Nomarski image of a P5 rabbit retina showing a ganglion cell (indicated by the arrow, also in B) under whole-cell patch-clamp recording. B, A fluorescence image of the same field as in A, showing fura-2-AM-loaded cells in the ganglion cell layer. Images in A and B were collected with an intensified cooled digital camera under a 40× objective lens. C, Correlated changes in the average fluorescence intensity measured from six randomly selected cells (enclosed by circles in B) immediately before patch-clamp recording. Arrow indicates the trace corresponding to the ganglion cell identified by the arrow in A and B. D, Simultaneous fluorescence measurement (top trace) from the oval area enclosed by the dash line and whole-cell voltage-clamp (bottom trace, Vh =
DISCUSSION
Coordinated transitions in neurotransmitter systems
This study demonstrates that the excitatory drive for spontaneous waves in the rabbit retina undergoes two coordinated transitions during early postnatal development: one from a fast cholinergic to a fast glutamatergic and the other from a nicotinic to a muscarinic system. The finding that the cholinergic system selectively uses two entirely different classes of receptors for the same transmitter to mediate waves at different developmental stages is both surprising and intriguing. It suggests a novel mechanism by which a neurotransmitter system changes its functional role during development. This mechanism is uniquely economical and conservative because it apparently uses the same basic starburst network as a neuronal substrate.
The emergence of the glutamatergic drive began in rabbits at ~P0-P1, a developmental stage (~77% caecal period; Dreher and Robinson, 1988
Whereas the exact developmental role of the above pharmacological transitions in retinal waves is yet to be understood, these transitions almost certainly reflect changes in the retinal circuitry that supports the spontaneous wave and also indicate different functional roles played by the early and late spontaneous waves. A variety of important developmental events, such as ON/OFF segregation in the IPL and the central visual pathway (Bodnarenko and Chalupa, 1993
A possible network basis for the consistency in the overall pattern of wave propagation
Despite drastic pharmacological changes in spontaneous retinal waves at P1-P3, we found the overall characteristics of the wave remained similar (Zhao et al., 1999
On the other hand, it is well known that the cholinergic and glutamatergic circuits in the vertebrate retina differ completely (Dowling, 1987
We believe our finding of the transition from the nicotinic to the muscarinic system may provide an intriguing clue to this puzzle. Because the late retinal wave is critically dependent on muscarinic transmission, it is almost certain that the starburst network remains essential for the late spontaneous wave. Thus, even after the glutamatergic input replaces the nicotinic system as the major fast excitatory drive for the wave, the cholinergic system, through the activation of muscarinic receptors, continues to play a critical role in the propagation of retinal waves, perhaps by working in conjunction with the glutamatergic system and providing a lateral cholinergic network that could ensure a consistent pattern of wave propagation. Indeed, our results showed that a partial blockade of muscarinic receptors led to smaller and slower waves, whereas a partial block of AMPA/KA receptors reduced the wave frequency and amplitude, but not the size or the speed of the wave. This would suggest that glutamate released from bipolar cells might be more suited for strong but more localized excitation in ganglion and amacrine cells, whereas the cholinergic system might be particularly important for lateral propagation of this excitation. Recent results from turtle and chick retinas, in which the spontaneous waves are driven by both glutamatergic and nicotinic inputs at the ages studied, also showed that a partial nicotinic blockade led to spatial shrinkage of waves, whereas a partial blockade of glutamatergic input reduced the overall excitability but not the spatial extent of the propagation pattern (Sernagor and Grzywacz, 1999
Thus, in the early developing mammalian retina, the cholinergic system, through the activation of nicotinic receptors, may provide a major excitatory drive for both the initiation and propagation of spontaneous waves [the wave is also likely to be mediated by an excitatory glycinergic drive (Paul and Zhou, 2000
Involvement of second messenger-mediated interactions in the formation of retina waves
For spontaneous retinal waves to play a role in the refinement of retinal circuitry as previously suggested (Sernagor and Grzyacz, 1996
Potential muscarinic actions in the late wave may include modulation of glutamate release from bipolar cells as well as regulation of cellular excitability and synaptic communication among bipolar, amacrine (including the starburst), and ganglion cells. Activation of M1 and M3 receptors typically leads to protein kinase C activation and the production of IP3, which affects intracellular Ca2+ and may pass through gap junctions. Furthermore, it remains a possibility that muscarinic inhibition of M currents may also provide a form of excitation in the network. The existence of muscarinic receptors in the IPL of the developing ferret retina has been demonstrated immunohistochemically (Hutchins, 1994
Implications on mechanistic models of spontaneous retinal waves
Our finding of a critical dependence of the late spontaneous wave on the cholinergic network does not support implications from previous studies that as development proceeds the cholinergic contribution to the wave is completely replaced by the glutamatergic drive in the mammalian retina. Our data that the glutamatergic and muscarinic systems played different functional roles in wave formation (Fig. 4) are also incompatible with the hypothesis that the synaptic organization of excitatory inputs is not important for the gross pattern of retinal waves. Thus, a homeostatic model, such as that proposed for the developing spinal cord (for review, see O'Donovan et al., 1998
FOOTNOTES Received March 23, 2000; revised June 15, 2000; accepted June 22, 2000.
This study was supported by grants to Z.J.Z. from the National Institutes of Health (RO1 EY01894) and Research to Prevent Blindness, Inc. We thank Dr. Sunil Paul and Ms. Suzanne Bakewell for scientific discussions and Dr. Gordon Fain for helpful comments on this manuscript.
Correspondence should be addressed to Dr. Z. Jimmy Zhou, Department of Physiology and Biophysics, University of Arkansas for Medical Sciences, 4301 West Markham Street, Mail Slot 505, Little Rock, AR 72205-7199. E-mail: zhoujimmy{at}exchange.uams.edu.
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