PartII
ThreeTypesofMechanoproprioceptorsintheSwimmerets
Summary
1.
3.
4.
5.
6.
Three types of mechanoproprioceptors were found in the swimmeret of
Bathynommus doederleini. These were a stretch receptor I (StR I), a stretch receptor II (StR II) and a root cell mechanoreceptor (RCMR).
StR I and StR II terminated on elastic strands at the bases of swimmerets.
RCMR extended its dendrites to various regions and organs in the abdominal segments along major nerves of the swimmerets. A set of three mechanoproprioceptors was found in every swimmeret.
Cell bodies of StR I and StR II were identified in the abdominal ganglia. The StR I cell body was located at the anterior half of the ipsilateral hemiganglion, and the StR II cell body was located at the posterior half of the contralateral hemiganglion. The cell body of RCMR was located on the 1st root of each abdominal ganglion.
Intracellular recording from the cell bodies showed that StR I was retraction—
sensitive non—spiking stretch receptor of the swimmeret.
StR II showed the characteristics of a protraction—sensitive non—spiking stretch receptor, and of a velocity—sensitive spiking stretch receptor.
RCMR responded to movements of the swimmeret muscles and to deformation of a variety of regions of swimmerets and their vicinities.
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-Introduction
Crustacean mechanoproprioceptors are classified in three types, according to
the strategies used to propagate their signals to the central nervous system (CNS).
The first category is the spike—generating type, such as the muscle receptor organ (MRO) and chordotonal organ. The second is the analogue—signaling (non—
spiking) type, such as the thoracic—coxal muscle receptor organ (TCMRO, reviewed by Bush 1976, 1981), non—spiking stretch receptors in the swimmerets (Heftier 1982; Macmillan and Deller 1989; Pasztor and Macmillan 1990) and uropod mechanoreceptors (Paul 1972). The third category contains both spike—
generating and analogue—signaling types, such as are found in the scaphognathite (oval organ) (Pasztor 1969; Pasztor and Bush 1982). A variety of motor neurons for somatic movements receive reflex control at the CNS from the mechanoproprioceptors. Besides the somatic reflexes, some recent studies of mechanoproprioceptors in decapods have been focused on the reflex control of the circulatory system (Greco et al. 1986; Burggren et al. 1990; Taylor and Taylor 1991; Rajashekhar and Wilkens 1991; Wilkens and Young 1992). However, the anatomy of mechanoproprioceptors responsible for reflexes of the circulatory systems has not been described at a cellular level. I previously reported the presence of three types of mechanoproprioceptors in the swimmerets of Bathynorus doederleini (see Part I, 1). Two of them were anatomicaIly identified as stretch receptor—like terminal processes (StR I and StR II) at the base of swimmerets, the other was identified electrophysiologically as a mechanosensitive neuron in the nerve to the retractor muscles (RMN) of the swimmerets. Since
these receptors induced reflexes in pathways leading to motor neurons of the cardioarterial valves, it was concluded that they play an important role in control
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-of distribution -of hacmolymph flow among arteries (see Part I, 1).
In this part, I report an investigation of three types of swimmeret mechanoproprioceptors by means of neuroanatomical and electrophysiological techniques. Intracellular recording from the cell bodies of StRs in the abdominal ganglia revealed that StR I was a non—spiking stretch receptor, and that StR II was
an analogue—signaling and spiking stretch receptor. The mechanosensitive fiber in the RMN was shown to be a branch of a mechanoreceptor, whose cell body was situated on the 1st root of an abdominal ganglion. I tentatively refer to the receptor as root cell mechanoreceptor (RCMR). Dendrites from the cell body of RCMR ran along major nerves of abdominal segments, and spread all over the swimmeret. The receptor was sensitive to deformation of various tissues, such as muscles, connective tissues and cuticles, in the abdominal segments.
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-Materials and Methods
Animals
Bathynonnus doederleini, 9-15 cm in body length, were collected and kept as described in Part I.
Histology
After animals were anesthetized with an isotonic (0.36 M) MgC12 solution, the dorsal carapace of abdomen was removed, and masses involving the base of the swimmerets were isolated. Peripheral nerves of the 1st to 5th abdominal segments involving StR I and StR II were isolated from the base of the swimmerets together with the elastic strands. They were pinned to the Sylgard—
lined bottom of a petri dish. The specimens were pre—fixed for 1 hr with 3 % glutaraldehyde solution (in 0.1 M cacodylate buffer, pH 7.2), and subsequently post—fixed with 1 % osmium tetraoxide solution for 1 hr. After a wash of the specimens with the buffer solution, they were dehydrated with an ethanol series, and embedded in epoxy—resin. n—Butyl glycidyl ether was used in the process of infiltration of the resin. Sections (1 µm thick) were stained with a mixed solution of 1 % methylene blue and 1 % azur II (Richardson et al. 1960), observed under a light microscope and photographed.
Dye injection
In order to reveal central and peripheral morphology of mechanoproprioceptors, fluorescent dyes were injected into their cell bodies (methods for making preparations, see below). The cell bodies of StRs were identified in the abdominal ganglia by means of back—filling from the periphery with a mixed
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-solution of 1 M CoC12 and 1 M NiC12 (Quicke and Brace 1979; and see Part I, 1).
Cell bodies were impaled by microelectrodes filled with 5 % Lucifer Yellow (Sigma) dissolved in 1 M LiC1 or 5,6—carboxyfluorescein (Sigma) dissolved in 0.1 M potassium acetate (tip resistance, 10-40 MQ). The dyes were injected by means of electrophoresis with negative current pulses (1-5 nA, 0.5-1 Hz, and 0.5-1 sec in duration) for 0.5-2 hr. The preparations were incubated in filtered sea water (FSW) or FSW containing 10 mM probenecid (cf. Rosen et al. 1991) over night at 4 °C, fixed with 4 % formaldehyde for 15 min and with 4 % methanolic formaldehyde for 1.5-3 hr. After dehydration with an ethanol series, specimens were cleared with methyl salicylate, and were observed under a fluorescent microscope and photographed.
Electrophysiology
Anesthetized animals were divided the body in two parts at the junction between the thorax and abdomen. For intracellular recordings from StR cell bodies, the abdominal part was pinned to the bottom of an experimental chamber, ventral side up, at the right and left edges of the body. Cuticles of ventral plate right beneath the abdominal ganglia were peeled off, and connective tissue surrounding the ventral nerve cord was carefully removed. The abdominal ganglia (usually the 1st to 3rd) were pinned to a small platform (5 mm in width, 20 mm in length). The platform was equipped with a light guide of glass fibers for transillumination of the ganglion. There are periganglionic sac—like structures of the sheath including several to several tens of cell bodies on the ventral side (cf.
Tanaka and Kuwasawa 1991b; Okada and Kuwasawa 1993). The structures were carefully desheathed with fine forceps to reveal cell bodies.
Isolated abdominal segments were pinned dorsal side up for intracellular
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-recording from RCMR cell bodies. After removal of ventral somatic muscles, protractor and retractor muscles, the cell body was revealed on the 1st root. A small piece of silicone rubber was laid under the cell body for the platform.
Intracellular recording from cell bodies was performed by means of single glass microelectrodes filled with 3 M KC1 (tip resistance, 10-20 M52), which were coupled to a high input impedance preamplifier equipped with a bridge device (Nihon Kohden, MEZ-8201). Activity of an RCMR was recorded extracellularly from the 1st root or RMN with an Ag—AgC1 wired glass capillary suction electrode. Signals were displayed on a pen—writing chart recorder (Nihon Kohden, PMP-3004) and on an oscilloscope (Tektronix, 5110).
Artificial protraction and retraction of the swimmerets were achieved by pulling and releasing a thread tied to the swimmerets (for detail, see Part I, 1). Stretches of the elastic strands attached to StRs were manually applied with a micromanipulator equipped with an isometric transducer (Minebea, UL-2GR) whose probe was connected to the cut end of the elastic strands. Specimens were continuously superfused with FSW at 15-20 °C.
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-Results
Since the swimmerets of Bathynomus are bordered with tufts of branchial filaments, they function as both locomotor and respiratory organs (a review of McLaughlin 1983; Tanaka and Kuwasawa 1991a). In Part I (1), I described the presence of two kinds of stretch receptor—like processes (StR I and StR II) on clastic strands located at the bases of the swimmerets, and a mechanosensitive fiber in the nerve to retractor muscles.
Peripheral and central morphology of StRs
The anatomy of StR I and StR II is shown in Figure 1. StR I and StR II originate from, respectively, the 1st and 2nd roots of the abdominal ganglia, and ramify on elastic strands in the swimmeret sockets. The elastic strand attached to StR I spans from an anterior region of a swimmeret socket to the endopodite. The elastic strand attached to StR II spans between anterior and posterior regions in the swimmeret socket. Both the elastic strands are fused to each other near the anterior end of the strands. In a resting state of the animal, the swimmerets are almost retracted, and the angle of the swimmeret to the ventral plane is about 30 °.
When an individual swimmeret is protracted, the elastic strand of StR I is shortened by the folding of articular membrane between the abdominal sternite and basipodite (see Part I, 1). The elastic strand of StR II is stretched by protraction of the swimmeret since the articular membrane projects into the abdominal cavity (see Part I, 1).
In order to observe details of peripheral structure, 1 µm sections were made from StRs embedded in epoxy—resin. Preparations were sequentially cross—
sectioned from the periphery (Figs. 2 and 3). Axons of StR I and StR II
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-(respectively, 30 and 50 lam in diameter) were the thickest in their own ganglionic root. These characteristics of StRs were similar to non—spiking stretch receptors in decapod appendages (reviewed by Bush and Laverack 1982). The nerve running to the elastic strand of StR I includes several axons (less than 15 µm in diameter) extending to the basipodite and endopodite (Fig. 2). A single giant axon of StR II running from the 2nd root directly extends to the elastic strand, and ramifies in fine branches there (Fig. 3).
Back—filling of Co2+ and Ni2+ ions into StRs revealed their cell bodies in the abdominal ganglion. However, since central processes were obscure in the back—
filled preparation, Lucifer Yellow was injected into the cell bodies of StR I (Fig. 4) and StR II (Fig. 5). The StR I cell body (50 µm in diameter) was located at the anterior half of the ipsilateral hemiganglion to the StR I periphery. Fine intraganglionic processes arising from the axon of StR I were observed at two points, near to the cell body and around the origin of the 1st root. The StR I axon was thin between the cell body and the origin of the 1st root, and gradually got thick in the 1st root to the periphery. The StR II cell body (50 µm in diameter) was located at the posterior half of the contralateral hemiganglion to the StR II periphery. StR II had many more intraganglionic processes than StR I. An axon from the cell body bifurcated at the origin of the 2nd root. One bifurcation extended anteriorly, and ramified in the neuropil of the ipsilateral hemiganglion.
The other ran out of the ganglion in the 2nd root to the periphery. Many fine processes arising from the axon were seen around the origin of the 2nd root.
Peripheral and central morphology of the root cell mechanoreceptor (RCMR)
I pursued pathways of mechanosensitive fibers in the RMN from the periphery to the CNS. Although RMN is one of branches from the 2nd root, the reflex of
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-the nerves innervating -the cardioarterial valves, which was caused by -the afferent stimulation of RMN (see Part I, 1), could be induced even after cutting the 2nd root (data not shown). A single unit of impulses was recorded from the 1st root by the stimulation applied to the RMN, irrespective of the stimulus intensity (data not shown). By means of methylene blue vital staining, the RMN involved one of dendrites from the cell body which was located on the 1st root (Fig. 1). In high Mg2+ saline, intracellular impulses of the cell body, which were caused by depolarizing current injection into the cell body, corresponded to the extracellular impulses of RMN and the 1st root (data not shown). From these observations, the cell body on the 1st root was considered to be mechanoreceptor neuron. I referred to the cell as root cell mechanoreceptor (RCMR). RCMR was stained with intracellular injection of 5,6—carboxyfluorescein (Fig. 6). The cell body (70 pm in diameter) was located at a site near the proximal side of the protractor muscle (Figs. 1 and 6). Dendrites from the cell body ran along major nerves to the swimmeret, and extended to: connective tissues surrounding the ventral nerve cord, lateral body wall, protractor and retractor muscles, the exopodite, hypodermis of the ventral plate, endoskeleton of retractor muscle, and articular membrane of abdomino—basipodite joint. A few fine processes were observed to terminate in the 1st root itself. An afferent process arising from the cell body ran to the abdominal ganglion via the 1st root.
Details of the central projection of RCMR are shown in Figure 7. An axon from the root cell arborized in a neuropil region of the ipsilateral hemiganglion.
The thickest axon ran to the center of the ganglionic neuropil, and turned to a rostral direction there to become an ascending process. The ascending process was observed to pass through neighboring ganglion anterior to the ganglion where the cell body was located.
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-Responses of StRs to the swimnzeret movement
Intracellular records were obtained from cell bodies of StR I and StR II. It was characteristic that cell bodies of StRs never discharged spikes at the time of impalement with microelectrodes. When the animal is in a resting state, the swimmerets show slow and narrow—range beating in a retracted position for respiration. The respiratory movement of the swimmerets changes into rapid and wide—range heating during walking or swimming locomotion. In the locomotor heating, the maximum angle of the swimmeret to the ventral plane reaches more than 90 °, and the beating frequency ranges from 2 to 5 Hz (Tanaka and Kuwasawa 1991a).
Figure 8 shows responses of StR I and StR II to the stretching of their elastic strands. Stretching of the elastic strands generated sustained depolarizing potentials in the cell bodies of StR I and StR II. Figure 9 shows the responses of StR I to artificially—produced protraction of the swimmerets. In the resting state of the swimmerets, the swimmeret angle was about 30 ° to the ventral plane, and the resting membrane potential was —39 mV. StR I showed sustained hyperpolarizing potentials in response to the continuous protraction of the swimmerets. The amplitude of the hyperpolarizing potentials was dependent on the angle of the swimmerets to the ventral plane. Membrane potential changes in response to repetitive protraction also corresponded to protraction, in an analogue manner. No spike discharge was observed in the cell body of StR I. When the angle of the swimmeret was at about 120 °, the maximum hyperpolarizing potential (about 15 mV) was recorded. Since StR I was depolarized by the stretching of the clastic strand (see Fig. 8A), it was confirmed that protraction of the swimmeret causes shortening of the elastic strand of StR I, and generates hyperpolarizing potentials (cf. Part I, 1). In the initial phase of protraction
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-movement, a large hyperpolarization was observed (Fig. 9). This potential was followed by steady membrane potential. On the other hand, a rebound depolarizing potentials were observed in the retraction phase (Fig. 9).
Figure 10 shows the responses of StR II to continuous (A) and repetitive (B) protractions of the swimmerets. Resting membrane potential was —55 mV in the resting state (swimmeret angle, about 30 °). StR II showed sustained depolarizing potentials in parallel with displacement of the swimmerets. Amplitude of the sustained depolarization depended on the angle of the swimmerets, as in StR I.
When the swimmerets were at about 150 °, the maximum depolarizing potential (about 18 mV in amplitude) was recorded. Since StR Il was depolarized by the stretching of the elastic strand (Fig. 8B), it was shown that protraction of the
swimmerets stretches the elastic strand of StR II. StR II often showed a large
phasic depolarization at the initial phase of protraction (Fig. 10). Similar potentials were observed as "dynamic component" in the thoracic—coxal muscle receptor organ of the crab (reviewed by Bush 1981) and as "transient large depolarization" of the swimmeret non—spiking stretch receptors of the crayfish (Heitler 1982). The sustained potentials were followed by afterhyperpolarization at the cessation of protraction (Fig. 10).
StR II generated the sustained depolarization and even spike potentials.
Figure 11A shows two kinds of responses of StR II to different velocities of the swimmeret movement. The maximum angle between the swimmeret and ventral plane was fixed at 120 °. StR II showed only sustained potentials in response to slow movements (at about 0.5 Hz, Fig. 11A1). On the other hand, when the swimmerets were moved at a faster rate (at about 1 Hz), spike potentials arose at the end of the rising phase in each movement (Fig. 11A2). Figure 11B shows responses of StR II to a variety of protraction velocities. The number of spikes
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-increased depending on the velocity of protraction movements. Angle of the swimmerets to the ventral plane was common through three trials at 120 °. The spikes were often followed by damped oscillatory potentials (Fig. 11B, 2 and 3).
These results suggest that the StR II has functions of both displacement and velocity sensors for the swimmeret movements.
Afferent activity of RCMR
Figure 12 shows responses of RCMR to various mechanical stimuli. Afferent activities of RCMR were recorded extracellularly from a distal cut—stump of RMN (Fig. 12A). As described in Part I (1), responses to continuous (A1) and repetitive (A2) protraction of the swimmerets suggest that RCMR functions as the mechanoproprioceptor for the movements of the retractor muscles of the swimmerets.
In the isolated preparation from the CNS, antidromic impulses of RCMR were recorded extracellularly from the proximal cut—stump of RMN. Deformation of cuticles of the gill, exopodite and articular membrane of the abdomino—basipodite joint triggered impulse discharge of RCMR (Fig. 12B). RCMR may be a type of
phasic mechanoreceptor for various regions and organs in the abdominal segment including the swimmeret.
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-Discussion
Physiological role of the switnnieret nechanoproprioceptors in cardiovascular control
StR I, StR II and RCMR were found to be receptors which trigger reflex responses of the valve nerves of the arteries (see Part I, 1). Long—lasting current injection, but not repetitive short pulse stimuli, to StR I or StR II affects two valve nerves in lateral arteries. The reflexes of the valve nerves induced by activation of StRs may result in an increase of haemolymph flow to the swimmerets, and a decrease of flow to the walking—legs and viscera, simultaneously. Repetitive stimuli of the nerve to retractor muscles (RMN), which results in activation of the RCMR, induced two patterns of reflexes in the two valve nerves (see Part I, 1).
One causes decreases of haemolymph flow to the swimmerets, and to walking—
legs and viscera. The other causes an increase of haemolymph flow to the swimmerets, and a decrease of that to the walking—legs and viscera. In Bathynornus, Tanaka and Kuwasawa (1990) showed that artificial movements of the swimmerets evoked EPSPs in identified cardioaccelerator neurons. Thus, afferent inputs from the swimmeret mechanoproprioceptors to the CNS play important functions in neural control of the cardiac outflow to arteries. In Part I (2), I identified some neurons of the valve nerves in the CNS. Identification of the receptors may allow analyzing central mechanisms for reflex control of the circulatory system.
Characterization of StR I and StR II
In this study, using histological and electrophysiological methods, I showed characteristics of StR I and StR II. Swimmeret stretch receptors have been
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-reported in decapod species (Homarus americanus, Davis 1969; Pasztor and Macmillan 1990; Pacifastacus leniusculus, Heitler 1982; Nephrops norvegicus and Homarus gammarus, Miyan and Neil 1986; Cherax destructor, Macmillan and Deller 1989). However, there has been no report on the swimmeret stretch receptors in isopod species.
Histological observations of the periphery of StRs revealed that the axons of StRs were extremely thick (about 30-50 µm in diameter), and were one of the thickest in each abdominal ganglionic root. This is a similar characteristic to the axons of non—spiking stretch receptors in decapods such as thoracic—coxal muscle receptor organ (TCMRO, reviewed by Bush 1976), uropod mechanoreceptors (Paul 1972), non—spiking stretch receptors of the swimmerets (Heftier 1982) and oval organ (Pasztor 1969; Pasztor and Bush 1982). In contrast with the impulse—
coded neurons, the large diameter axon is advantageous for analogue—signaling cables to propagate decremental information over a long distance (reviewed by Bush 1981).
The cell body of StR I was located in the anterior half of the ipsilateral hemiganglion, and the cell body of StR II was located in the posterior half of the contralateral hemiganglion. Since the cell bodies of StRs were conspicuously
large (50 µm in diameter) among abdominal ganglionic neurons, they were easy to be identified visually. StR I showed sustained hyperpolarizing potentials in response to protraction of the swimmerets (Fig. 9). On the other hand, StR II showed sustained depolarizing potentials upon swimmeret protraction (Fig. 10).
These results indicate that the StR I and StR II are retraction— and protraction—
sensitive stretch receptors, respectively. Therefore, they are stretch receptors of antagonistic signaling for swimmeret movements such as protraction and retraction. Antagonistic signaling—stretch receptors, which have been found in
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-the coxo—basipodite joint of the crab Carcinus raenas, were shown to be a non—
spiking type (Cannone 1987; Cannone and Nijland 1989). In the swimmeret of the lobster, antagonistic signaling—spiking stretch receptors were reported by Miyan and Neil (1986).
In addition to occurrence of sustained depolarizing potentials, StR II also generated spike potentials when rapid and wide—range beating of the swimmerets were elicited (Fig. 11). The faster the swimmeret velocity, the larger the number of spikes that were generated. This suggests that StR II may respond to both displacement and velocity of the swimmeret movements. In intact animals, beat rate of locomotor movements of the swimmerets reaches up to 5 Hz (Tanaka and Kuwasawa 1991a). However, with my present device for artificial movements of the swimmerets, such high frequency movements were not attained. Then, it might be expected that StR II generated more spikes than those observed, in locomotor beating in intact animals. Both the analogue—signaling and impulse—
coded stretch receptors have been shown to be the oval organ in the scaphognathite of decapods (Pasztor 1969; Pasztor and Bush 1982). Three X, Y and Z mechanosensitive fibers comprising the oval organ have basically analogue—signaling features. These fibers have the ability to generate impulses, depending on the velocity of stretching of the elastic strands (Pasztor and Bush 1982). In this study, it was concluded that StR II has characteristics similar to the fibers of the oval organ.
Characterization of RCMR
In the crayfish abdomen, cutaneous mechanoreceptors were described by Pabst and Kennedy (1967). The receptors respond to mechanical stimulation applied to the soft cuticle of the abdomen, and their cell bodies are located on the 1st and 2nd
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-roots of each abdominal ganglion. Activation of the cutaneous mechanoreceptors caused suppressions of motor outputs to the slow flexor muscle and swimmeret muscles, and of afferent interncurons in the abdominal ganglia (Pabst and Kennedy 1967). In the hermit crabs, Pagurus granosinmanus and P. pollicarus , Chapple (1966, 1974) demonstrated that phasic afferent units of the 1st or 2nd root of the abdominal ganglia are sensitive to mechanical stimulation of the abdominal wall. Bush and Laverack (1982) mentioned in their review that the cutaneous
mechanoreceptor of the crayfish and the abdominal mechanoreceptor of the hermit crab are homologous to each other. The morphology of RCMR in Bathynonius is very similar to the cutaneous mechanoreceptor of the crayfish. Methylene blue vital staining and fluorescent dye injection revealed the peripheral and central morphology of RCMR. RCMR has an extensive central projection in the ipsilateral hemiganglion, and an interganglionic ascending process. Dendrites from the RCMR cell body extended not only to the abdominal cuticle, but also to almost all regions of the swimmerets and abdomen. The RCMR may respond to tension on the ventral nerve cord, since there was a single RCMR process extending to connective tissues surrounding the ventral nerve cord. This feature is comparable to the intersegmental tension—sensitive fiber (cord stretch receptor) in the abdominal ganglionic sheath of the crayfish (Hughes and Wiersma 1960;
Grobstein 1973). The sensory modality of RCMR is likely to be more varied than that of the crayfish cutaneous mechanoreceptor. RCMR is characterized as a phasic type of intrasegmental mechanoreceptor signaling deformation of the internal structure of abdomen including the swimmerets.
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