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REPORT
bas 
iburkusDepartment of Cell Biology and Anatomy, Louisiana State Health Sciences Center, New Orleans, Louisiana
Submitted 21 December 2004; accepted in final form 1 August 2006
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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subunit indicated an age-related recession in uncrossed retinal projections. Between P2 and P5 uncrossed projections occupied as much as 50% of the LGN and overlapped substantially with crossed projections. Between the first and second postnatal week uncrossed projections receded, so by P14 they assumed an adultlike profile occupying 15–20% of LGN and showed little or no overlap with crossed projections. The postsynaptic responses of LGN cells evoked by the separate stimulation of each optic nerve indicated that before P14, many relay cells were binocularly innervated and received at least four to six inputs from each eye. However, these features of retinogeniculate connectivity were transient and their attrition occurred in concert with a retraction of retinal arbors into nonoverlapping, eye-specific regions. By P18 cells were monocularly innervated and received input from one to three retinal ganglion cells. These results provide a better understanding of the underlying changes in synaptic circuitry that occur during the anatomical segregation of retinal inputs into eye-specific territories. |
INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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). During perinatal life retinal axons from the two eyes share common terminal space in the dorsal lateral geniculate nucleus (LGN) but then segregate to form well-defined eye-specific territories (Godement et al. 1984; Jaubert-Miazza et al. 2005; Jeffery 1984; Linden et al. 1981; Naska et al. 2004; Shatz 1983). Although the anatomical rearrangement of retinogeniculate projections has been well documented, the functional changes that accompany this remodeling have not been fully realized. For example, at perinatal ages in the cat, the majority of LGN cells receive input from the two eyes (Shatz and Kirkwood 1984). Because these experiments involved extracellular recordings, the actual pattern of retinal convergence was not assessed quantitatively. More recently, in vitro intracellular recordings in postnatal rodents show an age-related reduction in retinal convergence (Chen and Regehr 2000; Lo et al. 2002). However, these studies did not examine the extent to which the projections from each eye contribute to changes in retinal convergence or how such changes correlate with the anatomical segregation of retinal projections into eye-specific territories of LGN.
To address these unresolved issues, we examined the changes in synaptic transmission that occur in the LGN of the rat during the period of retinogeniculate axon segregation. Developing retinogeniculate projections were visualized by labeling axons and their terminal fields with the anterograde tracer cholera toxin subunit (CTB) (Angelucci et al. 1996; Jaubert-Miazza et al. 2005; Naska et al. 2004; Torborg and Feller 2004). To study synaptic responses we used an in vitro isolated brain stem preparation in which large segments of each optic nerve are spared and the intrinsic circuitry of the LGN is left intact (iburkus et al. 2003). This preparation proved especially useful because it allowed us to record the intracellular postsynaptic responses of LGN cells evoked by the separate and independent stimulation of each optic nerve. We found that the retraction of retinal terminal fields into eye-specific domains was accompanied by a loss of binocular responsiveness and a reduction in retinal convergence.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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We made intravitreal eye injections of the subunit cholera toxin (CTB) in 24 Long–Evans hooded rat pups at the following postnatal (P) ages: P2 (n = 1), P3 (n = 1), P5 (n = 2), P7 (n = 2), P8 (n = 1), P9 (n = 1), P10 (n = 1), P11 (n = 1), P13 (n = 1), P14 (n = 2), P15 (n = 1), P17 (n = 3), P18 (n = 3), P19 (n = 1), P21 (n = 2), and P23 (n = 1). CTB has proved to be a reliable and sensitive anterograde tracer of retinal projections, labeling even the thinnest terminal branches in great detail (Angelucci et al. 1996; Torborg and Feller 2004). In 10 animals, CTB was visualized using peroxidase-based immunocytochemistry, whereas in 14 others, we used CTB conjugated to fluorescent Alexa dyes. Both tracers yielded similar results (Fig. 1).
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For peroxidase-based reactions, the brains were removed from the skull, immersion-fixed overnight, and then cryoprotected in 30% sucrose solution for 24–72 h at 4°C. Brains were then blocked and sectioned at 60 µm in the coronal plane using a freezing microtome. Free-floating sections of tissue were treated overnight in a solution containing goat anti-CTB antibody (1:4,000; List Biological Labs). The binding of the primary antibody was visualized first by incubating tissue in biotinylated rabbit anti-goat IgG (1:200; Vector Labs) for 1 h and then reacting with an avidin–biotin–peroxidase complex (ABC Elite Kit; 1:100; Vector Labs) processed with 3,3'-diaminobenzidine tetrachloride (DAB). Labeled projections were viewed using bright-field microscopy (Nikon Labophot 2) and photographed digitally (Kodak CD-290).
For animals injected with fluorescent conjugates of CTB, the brains were postfixed overnight and sectioned at 60 µm in the coronal plane using a vibratome. Sections containing the LGN were mounted in ProLong (Molecular Probes) and imaged with epifluorescence microscopy. Images of LGN were acquired with a Photometrix Coolsnap camera attached to a fluorescence microscope (Nikon Eclipse). Fluorescent images of labeled sections were acquired and digitized separately using the following filter settings: Alexa 488: Exciter 465–495, DM 505, BA 515–555; Alexa 594: Exciter 528–553, DM 565, BA 600–660.
In all labeled material the boundaries of LGN were delineated so as not to include the optic tract, intrageniculate leaflet, and ventral geniculate nucleus. Labeled axons of passage, which tended to be located in more caudal sections of LGN, were also excluded from the analysis. To determine the spatial extent of labeled retinal projections in the LGN, gray-scale images were converted into binary high-contrast black and white images. Background signal was subtracted and images were normalized (0–255) using Metamorph or Photoshop software. A threshold procedure was used that allowed for the specification of a level that corresponded to a location in the gray-scale histogram where there was a clear distinction between signal and residual background (Angelucci et al. 1996; Jaubert-Miazza et al. 2005; Muir-Robinson et al. 2002; Torborg and Feller 2004). Typically threshold levels corresponded to a value of 30–50 on the gray-scale–normalized range of 0–255.
To measure the spatial extent of crossed and uncrossed retinal projections, the total number of pixels corresponding to each defined area of LGN was measured. In fluorescent material in which both uncrossed and crossed projections were labeled, the degree of overlap between the two was also assessed. For this the separate fluorescent images representing crossed and uncrossed terminal fields were superimposed and the pixels that contained both red and green signals (represented as yellow in Fig. 1) were counted.
In all cases, the spatial extent of uncrossed, crossed, and overlapping projections were computed by summing their area across five successive sections through the middle of LGN and then expressing the labeled regions as a percentage of the total area of LGN.
Surgical preparation of the isolated brain stem and in vitro recording
A detailed surgical account and illustration of the isolated brain stem was previously published (Lo et al. 2002; see Fig. 1 of iburkus et al. 2003). Long–Evans hooded rat pups from P3 to P21 were anesthetized with halothane and killed by decapitation. The brain was removed and placed in a solution of artificial cerebrospinal fluid (ACSF, in mM: 124 NaCl, 2.5 KCl, 1.25 NaH2PO4, 1.0 MgSO4, 26 NaHCO3, 10 dextrose, 2 CaCl2, saturated with 95% O2-5% CO2, pH = 7.4). During the excision, the optic nerves were cut just behind the disk and dissected from the base of the skull, sparing at least 4–6 mm of each nerve. Using a ventral approach, the brain was cut in half along the midline axis, while taking precautions to leave the optic chiasm intact. The hemisected brain was glued to a silver plate and placed into the well of a temperature-controlled recording chamber. The lateral surface of the thalamus and midbrain were exposed by removing the forebrain. The isolated brain stem was kept submerged and perfused continuously (4–5 ml/min) with warmed (31–33°C) ACSF. Recordings began 1–3 h after incubation. Electrode penetrations were made along the dorsolateral surface of the LGN and restricted to depths 
150 µm (Fig. 2).
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. All intracellular recordings were done in bridge mode with an Axoclamp 2B amplifier using techniques described previously (Guido et al. 1997; Lo et al. 2002; iburkus et al. 2003). Neuronal activity was displayed on a storage oscilloscope, digitized at 10 kHz, and stored directly on a computer using Heka Pulse software.
During intracellular recording, some LGN cells were filled with biocytin (Fig. 2) by passing alternating positive and negative current pulses (±1 nA, 30 ms, 100–300 pulses) through the recording electrode. Tissue containing biocytin-filled cells was placed in a fixative solution of 4% paraformaldehyde dissolved in 0.1 M phosphate buffer for 72 h. The LGN was sectioned at 400 µm in the coronal plane and processed using a standard avidin–biotin–horseradish peroxidase reaction processed with DAB (Guido et al. 1997; Horikawa and Armstrong 1988). Labeled cells were photographed and drawn using camera lucida.
To evoke synaptic activity in LGN, single square-wave pulses (0.1–0.3 ms, 0.1–5.0 mA) were delivered at a rate of 0.20–1.0 Hz through a pair of low-impedance (0.2–0.5 M), thin-gauged Ir wires whose exposed tips (0.1 mm) were placed on each optic nerve. The stimulating electrodes were placed at least 3–6 mm from the optic chiasm and the two nerves were separated by about 5 mm. In previously documented control experiments, this arrangement eliminated the possibility that current spread, even at maximal levels, inadvertently led to the concurrent stimulation of both optic nerves (Shatz and Kirkwood 1984; iburkus et al. 2003). To examine retinal convergence, we first determined the minimum intensity needed to evoke a postsynaptic response. Minimal stimulation produced responses that ranged in amplitude from 1 to 10 mV. We then adjusted the current intensity in 1, 2, 5, or 10% increments above this initial value until an excitatory postsynaptic potential (EPSP) of maximal amplitude was consistently reached (Lo et al. 2002; iburkus et al. 2003). EPSP amplitude by stimulus intensity plots were constructed and used to estimate the number of retinal inputs converging onto a single LGN cell (Bartlett and Smith 1999; Chen and Regehr 2000; Jaubert-Miazza et al. 2005; Lo et al. 2002; Lu and Constantine-Paton 2004). Trial-to-trial variability is relatively small and individual inputs can be readily distinguished from one another if the amplitude of the evoked response differs by 
1 mV (Bartlett and Smith 1999; Jaubert-Miazza et al. 2005; Lo et al. 2002; Lu and Constantine-Paton 2004). Thus as shown on the amplitude by stimulus-intensity plots of Fig. 4, a change of 1 mV was used to distinguish one step (or input) from the previous one.
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-aminobutyric acid type A (GABAA) antagonist bicuculline (10–25 µM) or the GABAB antagonist 2-hydroxysaclofen (100 µM) were bath applied to block inhibitory activity (Figs. 3 and 4). |
RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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Using peroxidase-based immunocytochemistry or fluorescence to reveal the axonal transport of CTB in LGN, we were able to visualize retinal projections (Fig. 1, A–C) and obtain estimates of the area occupied by their terminal fields (Fig. 1D). Figure 1, A and B shows the labeling pattern in the LGN ipsilateral to the injected eye at different postnatal ages (e.g., P2, P3, P7, P13, and P19) accomplished with the peroxidase-based immunocytochemistry. At P2–P3 projections originating from the ipsilateral retina (uncrossed inputs) were widespread and diffusely organized, occupying as much as 50% of the total area of LGN. The high-power view in Fig. 1A indicates that terminal fields were uniformly distributed and composed of a rich plexus of thinly branched and beaded axons. This diffuse projection pattern receded with age, so by about P10–P14, uncrossed inputs were limited to a small "ipsilateral patch" that resided in the dorsal medial region of the LGN and occupied about 15–20% of the nucleus (Fig. 1D). A similar pattern was observed with fluorescence labeling and representative examples at P7 and P17 are shown in Fig. 1C. In these cases, because each eye was injected with a different fluorescent conjugate, the terminal fields from crossed (contralateral eye) and uncrossed (ipsilateral eye) projections could be visualized simultaneously in a single section of LGN. This allowed us to assess the extent to which inputs from the two eyes share common (overlapping) terminal space in LGN.
Estimates of the spatial extent of retinal terminal fields for crossed and uncrossed projections as well as the degree of overlap between the two projections are shown in Fig. 1D. As shown in the individual data (Fig. 1D, left), crossed projections failed to show significant changes with age. By contrast, uncrossed projections (r = 0.844, P < 0.001) as well as the degree of overlap between crossed and uncrossed projections (r = 0.674, P < 0.046) showed a significant recession with age. To summarize across different ages, we computed the mean values of spatial extent between P2 and P7, P8 and P14, and P15 and P23 (Fig. 1D, right). Pairwise comparisons indicate a significant attrition for uncrossed projections between P2 and P7 (
= 42.5%) and P8 and P14 ( = 20.8%, Kruskal–Wallis, P < 0.001), but only a modest (statistically insignificant) decline thereafter (P15–P23, = 16.7%). Overlapping terminal fields showed significant losses between P2 and P7 ( = 21.9%) and P8 and P14 ( = 4.0%, Kruskal–Wallis, P < 0.001). Overall, these changes are similar to those reported previously for pigmented rodents in which CTB was used as an anterograde tracer (Demas et al. 2006; Jaubert-Miazza et al. 2005; Muir-Robinson et al. 2002; Naska et al. 2004; Torborg and Feller 2004).
Loss of binocular responsiveness during the period of retinogeniculate axon segregation
To explore this remodeling on a functional level, we examined the synaptic responses of developing LGN cells (n = 285) evoked by the separate stimulation of each optic nerve. All recordings were restricted to the dorsolateral region of LGN, which in the mature rat corresponds to an area that receives a crossed projection (Reese 1988; see also Fig. 1). We confirmed the location of 27 recorded cells by filling them with biocytin during intracellular recording (Fig. 2, A and C). In all cases, labeled cells resided well within the boundaries of LGN representing crossed projections. At all ages, labeled cells had relatively large somata and multipolar dendritic arbors consistent with those of relay cells (Webster and Rowe 1984; iburkus et al. 2003). A comparison of labeled cells in a section prepared from an isolated brain stem preparation at P18, with that of a section in which uncrossed terminal fields were labeled with CTB (Fig. 2, A vs. B), provided further evidence that recordings were done in dorsolateral regions of LGN.
Representative EPSPs evoked by optic nerve stimulation are shown in Fig. 3A. At early postnatal ages, separate and distinct EPSPs were frequently activated by stimulating the contralateral as well as the ipsilateral optic nerve. Between P0 and P7, when uncrossed inputs project diffusely throughout the LGN, the majority of responses (64%) were binocular (Fig. 3B). A high incidence of binocular responses was also evident between P8 and P14 (64.5%). However, between P15 and P21, excitatory binocular responses were encountered far less frequently (17.4%, chi square, P < 0.001). A day-by-day inspection of the encounter rate (Fig. 3B) revealed that after P17, binocular responses were extremely rare (3/43, 6.9%; see also Grieve 2005). Indeed, at P18, P20, and P21 all encountered cells were monocular and responded only to stimulation of the contralateral optic nerve.
Loss of retinal convergence during the period of retinogeniculate axon segregation
Another transient feature in the development of retinogeniculate transmission was the prevalence of synaptic responses that reflected the convergence of multiple retinal ganglion cell inputs onto a single LGN cell. To estimate the number of retinal inputs converging onto a single relay cell, we activated the optic nerves at various levels of stimulus intensity and measured the amplitude of the evoked EPSP. Representative examples of these responses along with their corresponding amplitude by stimulus intensity plots are shown in Fig. 4. Individual inputs were distinguished from each other if the amplitude of the evoked response was 1 mV and this relation was taken to reflect the successive recruitment of active inputs innervating a single LGN cell (Jaubert-Miazza et al. 2005; Lo et al. 2002). At early ages, a progressive increase in stimulus intensity typically produced a multiple stepwise increase in EPSP amplitude (Fig. 4A). However, at late postnatal ages the same stimulus protocol evoked either a single step or just a few steps (Fig. 4B). The summary plot in Fig. 5A reveals that between P0 and P7 LGN cells, on average, received six inputs from the contralateral eye and four from the ipsilateral eye. Between P8 and P14, the number of inputs a cell received decreased, typically to three to four inputs from the contralateral eye and only one to two from the ipsilateral eye. By P15–21, the degree of retinal convergence declined even further so that LGN cells, like their adult counterparts, received far fewer (one to three) and exclusively monocular inputs.
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= 7.46) tended to receive more inputs than monocular cells ( = 3.37, Mann–Whitney U test, P < 0.001), both groups showed a decrease in retinal convergence with age (Fig. 5C; monocular cells: r = 0.466, P < 0.001; binocular cells: r = 0.461, P < 0.001). |
DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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An important aspect of the present findings is that functional changes in connectivity continue after the anatomical segregation of retinal inputs is nearly complete. This apparent discrepancy has been observed in other species. In the cat a high incidence of binocular responses still exists at birth (Shatz and Kirkwood 1984), even though retinal projections have sorted into eye-specific layers of the LGN (Shatz 1983). Similarly in the mouse, a high degree of excitatory retinal convergence is evident at the time (P14) of natural eye opening (Chen and Regehr 2000) when retinal axons have finished segregating into eye-specific territories (Jaubert-Miazza et al. 2005; Muir-Robinson et al. 2002). Interestingly, the continued loss of functional inputs after anatomical segregation seems consistent with the time course of receptive field maturation (Daniels et al. 1978; Tavazoie and Reid 2000). Thus it seems that anterograde labeling techniques that rely on bulk filling of retinal axons fall short in revealing the precise patterns of synaptic connectivity of developing relay cells. Perhaps single axon labeling done in conjunction with an ultrastructural analysis is needed to resolve this issue.
Overall, the synaptic remodeling we observed in the rat is consistent with the refinement of connections reported in other species. At perinatal ages in the cat, LGN cells begin to lose binocular responsiveness (Shatz and Kirkwood 1984) and in postnatal mice, relay cells exhibit a severalfold reduction in excitatory retinal convergence (Chen and Regehr 2000; Jaubert-Miazza et al. 2005). However, it should be noted that our present estimates of convergence in the rat (see also Lo et al. 2002; Lu and Constantine-Paton 2004) seem conservative compared with those previously reported in the mouse LGN (Chen and Regehr 2000). In part, this may reflect a difference in species (but see Jaubert-Miazza et al. 2005), type of in vitro recording preparation (thalamic slice vs. isolated brain stem), recording technique (voltage-clamp vs. current-clamp) or the criterion used to distinguish individual inputs. Nonetheless, our estimates of retinal convergence in the mature LGN (one to three retinal inputs/geniculate cell) are in accord with those reported previously in cat (Mastronarde 1987; Usrey et al. 1999), rodent (Chen and Regehr 2000; Lo et al. 2002), and ferret (Tavazoie and Reid 2000). The functional loss of retinal inputs during retinogeniculate axon segregation may also help explain the postnatal maturation in LGN receptive field structure. Immature fields are large and irregularly shaped and lack distinct ON- and OFF-subregions, whereas mature ones are much smaller and have well-defined concentric center-surround organization (Daniels et al. 1978; Tavazoie and Reid 2000; Tootle and Friedlander 1989).
Finally, it is important to consider the underlying mechanisms responsible for the remodeling of retinogeniculate connections. The establishment of orderly connections in LGN has been attributed to the coordinated firing patterns of spontaneously active retinal ganglion cells (Wong 1999). When early retinal activity is altered or completely eliminated, retinogeniculate projections fail to segregate properly (e.g., Penn et al. 1998; Stellwagen and Shatz 2002; but see Huberman et al. 2003). The spontaneous activity of retinal ganglion cells is also sufficient to generate action potentials in LGN cells (Mooney et al. 1996). A proposed mechanism for activity-dependent remodeling is based on a Hebbian form of synaptic plasticity in which the degree of correlated firing between pre- and postsynaptic elements leads to either a long-term potentiation (LTP) or a depression (LTD) in synaptic strength (Bear and Malenka 1994; Shatz 1996). Long-term modifications in synaptic strength appear to underlie the refinement of sensory connections in the visual cortex (Kirkwood et al. 1996) and may also embody the synaptic rearrangements occurring during retinogeniculate axon segregation (Torborg and Feller 2005). Indeed, we noted a potential bias in retinogeniculate connectivity at early postnatal ages (Fig. 5; P0–P7 and P8–P14) that would seem to favor a Hebbian form of synapse consolidation and elimination. In the dorsolateral regions of LGN, developing cells, although binocular, seemed to receive more inputs from the contralateral rather than the ipsilateral eye. Certainly more definitive estimates would require additional experimentation, particularly at very early ages (e.g., P0–P4). Nonetheless, such a relation would suggest that postsynaptic activity in these regions of LGN is tightly coupled to retinal activity (Mooney et al. 1996) and also dominated by the activity of contralateral eye inputs (Weliky and Katz 1999), thus placing contralateral inputs at a competitive advantage over ipsilateral ones. The synaptic responses in LGN are also subject to long-term modification (Mooney et al. 1993). However, future studies will be needed to elucidate the exact nature and polarity of synaptic plasticity that prevails during early postnatal visual development.
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GRANTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONGRANTSACKNOWLEDGMENTSREFERENCES |
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Present address of J. iburkus: Dept of Engineering Science and Mechanics, The Pennsylvania State University, University Park, PA 16802 (E-mail: jziburku@gmu.edu).
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FOOTNOTES |
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Address for reprint requests and other correspondence: W. Guido, Department of Anatomy and Neurobiology, Virginia Commonwealth University School of Medicine, 1101 E. Marshall St., Richmond, VA 23298-0709 (E-mail: wguido{at}vcu.edu)
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REFERENCES |
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