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The Journal of Neurophysiology Vol. 87 No. 3 March 2002, pp. 1244-1251
Copyright ©2002 by the American Physiological Society
Centre for Research in Neuroscience, Montreal General Hospital Research Institute; and Department of Neurology and Neurosurgery and Department of Biology, McGill University, Montreal, Quebec H3G 1A4, Canada
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ABSTRACT |
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 TOP
 ABSTRACT
 INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Buss, Robert R. and Pierre Drapeau. Activation of Embryonic Red and White Muscle Fibers During Fictive Swimming in the Developing Zebrafish. J. Neurophysiol. 87: 1244-1251, 2002. Sub-threshold, motoneuron-evoked synaptic activity was observed in zebrafish embryonic red (ER) and white (EW) muscle fibers paralyzed with a dose of D-tubocurarine insufficient to abolish synaptic activity to determine whether muscle activation was coordinated to produce the undulating body movements required for locomotion. Paired whole-cell recordings revealed a synaptic drive that alternated between ipsilateral and contralateral myotomes and exhibited a rostral-caudal delay in timing appropriate for swimming. Both ER and EW muscle were activated during fictive swimming. However, at the fastest fictive swimming rates, ER fibers were de-recruited, whereas they could be active in isolation of EW fibers at the slowest fictive swimming rates. Prior to hatching, fictive swimming was preceded by a lower frequency, more robust and rhythmic synaptic drive resembling the "coiling" behavior of fish embryos. The motor activity observed in paralyzed zebrafish closely resembled the swimming and coiling behaviors observed in these developing fishes. At the early developmental stages examined in this study, myotomal muscle recruitment and coordination were similar to that observed in adult fishes during swimming. Our results indicate that the patterned activation of myotomal muscle is set from the onset of development.
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INTRODUCTION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Studies on the
locomotor behaviors of larval zebrafish have largely focused on the
startle response (Eaton and DiDomenico 1986
;
Kimmel et al. 1974; Liu and Fetcho 1999;
and references therein), while swimming behaviors have received less
attention (Budick and O'Malley 2000; Buss and
Drapeau 2001a; Fuiman 1986; Fuiman and
Webb 1988; Muller et al. 2000;
Saint-Amant and Drapeau 1998). Knowledge of the neural
control of larval zebrafish swimming is restricted to motoneuron
activity patterns and the synaptic drive to motoneurons in paralyzed
zebrafish during fictive swimming (Buss and Drapeau
2001a). Whether the activity of myotomal motoneurons is
coordinated to produce the undulating body movements required for
locomotion, and whether both forms of myotomal muscle, embryonic red
(ER) and embryonic white (EW), are activated during fictive swimming is unknown.
The activity of zebrafish motoneurons is fundamentally similar to the
motoneuron activity observed in lampreys and amphibian tadpoles during
fictive swimming. This is not unexpected considering similarities in
locomotion and spinal cord neuroanatomy (Grillner et al.
1998; Roberts 2000; Roberts et al.
1998). Furthermore, similarities in synaptic drive to
motoneurons during fictive locomotion extend to mammalian (feline)
preparations (see DISCUSSION in Buss and Drapeau
2001a). Accordingly, studies of zebrafish spinal cord physiology and locomotor control provide a framework for genetic and
molecular investigations (Granato et al. 1996) into
locomotor control in this vertebrate model which has the advantages of
a simpler nervous system with identifiable components.
In the present study, paired whole-cell recordings of the rhythmic
activation of larval zebrafish (day 3) muscle fibers, paralyzed with a
dose of D-tubocurarine insufficient to abolish synaptic activity, were used to test whether or not the circuitry of embryos is
sufficient to generate swimming with the attributes of the adult motor
pattern. The recordings revealed a synaptic drive that alternated
between ipsilateral and contralateral sides and exhibited a
rostral-caudal delay in timing. Both ER and EW muscle fibers were
active during fictive swimming and at this early developmental period
their recruitment was similar to that of adult fish. Prior to hatching
(day 1), fictive swimming was preceded by a lower frequency (1-13 Hz),
more robust rhythmic synaptic drive resembling the "coiling"
behavior of fish embryos (Herrick 1949; Hooker
1952; Whiting 1955). The characteristics of
fictive swimming are compared with the swimming patterns observed in
fishes and amphibian tadpoles. This work has been presented previously
in abstract form (Buss and Drapeau 2001b).
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METHODS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Experiments were performed on zebrafish (Danio rerio)
larvae and embryos of the Longfin strain raised at 28.5°C and
obtained from a breeding colony maintained according to
Westerfield (1995). All procedures were carried out in
compliance with the guidelines stipulated by the Canadian Council for
Animal Care and McGill University. The experimental methodology has
been described (Buss and Drapeau 2000). Results are
taken from 25 paired and 28 single whole-cell patch-clamp recordings
from ER and EW muscle fibers of zebrafish embryos aged 1.3-1.6 (day 1, length approximately 2.5 mm) and larvae aged 3.0-3.3 (day 3, length
approximately 3.5 mm) days postfertilization. Fictive swimming and
coiling occurred spontaneously or was evoked (day 3) by changes in
illumination. The swimming style of larval zebrafish changes from a
sustained burst swimming pattern to a beat-and-glide pattern between
day 2 (hatching) and day 4. Day 3 is a transition period where a
beat-and-glide-like swimming pattern emerges yet burst swimming is
still observed (Buss and Drapeau 2001a).
Beat-and-glide-like fictive swimming was observed in all day 3 larvae
examined (n = 32) and burst swimming was additionally
observed in 10 preparations.
Experiments were performed at room temperature (approximately 22°C).
The Evan's fish saline recording solution (Buss and Drapeau 2001a; Drapeau et al. 1999) contained the
following (in mM): 134 NaCl, 2.9 KCl, 2.1 CaCl2,
1.2 MgCl2, 10 HEPES, 5-10 glucose, 3 (day 3) or
15 (day 1) µM D-tubocurarine, osmolarity adjusted (with glucose) to 290 mOsm and pH 7.8. Patch-clamp electrodes (1.5-4 M
)
contained a K-gluconate solution consisting of the following (in mM): 2 MgCl2, 10 HEPES, 10 EGTA, 10 D-gluconic acid sodium salt, and 6 KCl added to sufficient
D-gluconic acid potassium salt to reach a final osmolarity
of 290 mOsm, pH 7.2. All chemicals were purchased from Sigma Chemical
(St. Louis, MO). A liquid junction potential of 
12 mV was
experimentally determined according to Barry and Lynch
(1991) and Neher (1992) and records were
corrected for this potential.
Recordings were performed with an Axoclamp-2A (0.1 headstage) and an
Axopatch-1D (CV-4 headstage) amplifier. Data were low-pass filtered at
10 kHz and digitized at 1 kHz (day 1) or 10 kHz (day 3). Analyses were
performed using pClamp 8 software (Axon Instruments). ER fibers were
distinguished by their superficial distribution and longitudinal
orientation, whereas EW fibers were deeper and had an oblique
orientation (Buss and Drapeau 2000). Measurements of
fictive swimming and coiling duration, rhythmic end plate potential (EPP) frequency, and rostral-caudal delay were made by eye (cursor measurement). Measurements on 50 consecutive EPPs were used to calculate mean fictive swimming and coiling EPP frequencies and rostral-caudal delay. Rostral-caudal delay was determined by measuring the fictive swimming rhythmic EPP delay (from EPP onset) between 9 and
12 segments centered on the anal segment. Rostral-caudal delay
per segment was calculated by dividing the mean time delay by the number of separating segments. Percentage phase lag was calculated by dividing the rostral-caudal delay per segment by the mean
cycle period (Wallen and Williams 1984). Paired
recordings between ER and EW fibers located within a segment revealed
differences in recruitment at day 3. When fictive swimming rhythmic
EPPs were observed in EW fibers, synchronous activity was observed in
ER fibers. However, ER fibers were often active in the absence of EW
fiber activity. Instantaneous fictive swimming rhythmic EPP frequencies
were measured during ER-EW fiber co-activity and ER fiber activity.
Results are presented as mean ± SD throughout the text. The term
significant denotes a relationship with P < 0.05 determined using the Student's t-test.
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RESULTS |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Rostral-caudal delay and ipsilateral-contralateral alternation of synaptic drive to myotomal muscle during fictive swimming
The propulsive forces used in undulatory swimming are generated by
an alternating rostral-caudal wave of myotomal muscle contraction, initiated by a synaptic drive originating from myotomal motoneurons, which interacts with the mechanical properties of body tissues (Blight 1977; Grillner and Kashin 1975;
Grillner et al. 1998; Hoff and Wassersug
2000; Lindsey 1978; Roberts 1981;
Roberts et al. 1998; Wardle et al. 1995;
Wassersug 1989). Therefore during a cycle of undulatory
swimming, rostral myotomal muscle fibers receive synaptic drive prior
to caudal fibers and within a segment the synaptic drive alternates
between ipsilateral and contralateral sides of the musculature. To
examine the synaptic drive to myotomal muscle fibers, embryos and
larvae were paralyzed with a low concentration of the neuromuscular
antagonist D-tubocurarine, which reduced, but did not
abolish, neuromuscular synaptic drive. Thus the rhythmic synaptic drive
(i.e., fictive swimming) underlying swimming was examined in
immobilized larvae using the whole-cell patch-clamp technique.
Paired recordings revealed a synchronous synaptic drive to muscle fibers within an ipsilateral myotomal segment (Fig. 1; n = 11) and an alternating synaptic drive to contralateral muscle fibers (Fig. 2; n = 6). A rostral-caudal delay was observed in paired recordings from ipsilateral muscle fibers separated by 9-12 myotomal segments (Fig. 3; n = 7). On average, this delay was 0.55 ± 0.20 ms per myotomal segment and there was strong negative relationship (Fig. 5C) between the time delay per segment and the rhythmic EPP frequency (i.e., fictive tail beat frequency). Intersegmental phase lag per segment ranged from 0.8 to 2.7% and averaged 1.8 ± 0.6%. Synchronous activity within ipsilateral myotomal segments, alternation between ipsilateral and contralateral segments, and rostral-caudal delays were similarly observed in paired recordings between ER and ER (Figs. 1 and 3), ER and EW (Figs. 2 and 4), and EW and EW fibers (data not shown).
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Differences in the recruitment of ER and EW muscle fibers during fictive swimming
Fishes that swim by undulatory propulsion generally use red muscle
for slow swimming, recruit white muscle for faster swimming, and
de-recruit red muscle at the fastest speeds of burst swimming (Bone 1978; Coughlin and Rome 1996;
Jayne and Lauder 1996; Johnston 1981,
1983). Whether the embryonic forms of red and white muscle (ER
and EW) found in larval fish are recruited as their adult forms has not
been examined. Comparison of mean fictive swimming rhythmic EPP
frequencies measured in ER (24 fibers, 1200 EPPs) and EW fibers (13 fibers, 650 EPPs) revealed a small but significantly different
(P = 0.03) frequency of rhythmic EPPs in EW versus ER fibers (44 ± 7 vs. 39 ± 7 Hz). Both ER and EW fibers were
recruited during fictive swimming (Figs. 2 and 4). However, within a
swimming episode, there were periods, especially during the end of a
fictive beat period, when ER fibers were active in the absence of EW
fiber activation (Fig. 4). Fictive swimming rhythmic EPP frequencies were lower when ER fibers were active in isolation (Fig. 4D)
of EW fibers. This is graphically illustrated in Fig.
5, A and B, where
intrasegmental paired ER-EW recordings (n = 6) were
used to measure rhythmic EPP frequencies during periods when only ER fibers were active (mean = 32 ± 3 Hz) and when both ER and
EW fibers were active (mean = 44 ± 7 Hz). Furthermore, an
attenuation of synaptic drive to ER fibers was observed during periods
of robust high-frequency synaptic drive to EW fibers (Fig.
4D). The duration of fictive swimming, measured as long
periods of repetitive brief swim episodes, was variable and ranged from
<1 s to 2-3 min (Fig. 5D).
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Fictive coiling and swimming behaviors prior to hatching
The rhythmic EPPs observed during fictive swimming strongly
summated in ER fibers, whereas EPPs quickly decayed to baseline in EW
fibers (Figs. 1-4). However, the time course of larval ER and EW
muscle miniature EPPs are similar (Buss and Drapeau
2000; Nguyen et al. 1999), indicating that the
rhythmic EPP summation was likely due to other factors. EPP summation
could be due to EPPs originating from adjacent electrically coupled ER
muscle fibers as EW fiber coupling is minimal at day 3, whereas ER
fibers are extensively coupled (Buss and Drapeau 2000).
To test whether the summation of rhythmic EPPs in ER but not EW fibers
was due to electrical coupling, recordings were made from day 1 ER and EW muscle fibers which are both extensively electrically coupled at
this age (Buss and Drapeau 2000).
Rhythmic EPPs summated similarly during fictive swimming in both ER and
EW fibers, providing evidence that the summation was due to electrical
coupling and not differences in EPP time course (Fig.
6, A and B).
However, in addition to a rhythmic motor output expected for swimming,
a slower and more robust rhythmic motor pattern, resembling the coiling
behavior of embryonic fishes (Armstrong and Higgins
1971; Gideiri 1966, 1968a,b; Harris
1962; Richards and Pollack 1987; Whiting
et al. 1992), was observed either alone or following fictive
swimming (Fig. 6, A and B). A fictive coiling episode contained 1-13 rhythmic EPPs, occurring at a mean frequency of
5.1 ± 3 Hz (n = 21) (Fig. 6D), and was
often (11/21) followed by rhythmic EPPs occurring at a faster frequency
(Fig. 6C; mean = 24 ± 12 Hz) that resembled
fictive swimming. A faster frequency of rhythmic EPPs (mean = 60 ± 3 Hz), characteristic of day 2 burst swimming (Buss
and Drapeau 2001a), was observed in one EW fiber (Fig.
6C). When this value was excluded from the average, no
significant difference in fictive swimming rhythmic EPP frequency was
observed in ER (mean = 20 ± 2 Hz) and EW (mean = 22 ± 2 Hz) fibers. Fictive coiling/swimming episodes lasted from
0.3 to 10 s (mean = 2.2 ± 2 s) and occurred every
10-420 s (mean = 140 ± 80 s). At this age, changes in
illumination were not effective at initiating fictive coiling or
swimming behaviors.
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DISCUSSION |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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Coordinated synaptic drive to myotomal muscle during fictive swimming
Requirements for fictive undulatory swimming are appropriate cycle
periods, alternating ipsilateral-contralateral motoneuron activity, a
rostral-caudal delay in motoneuron activity, and a relationship between
rostral-caudal delay and cycle period. By recording sub-threshold
motoneuron-evoked EPP activity in myotomal muscle fibers, a coordinated
motor output appropriate for swimming was revealed in paralyzed larval
zebrafish (Figs. 1-5). An appropriate motor coordination for swimming
has previously been reported in paralyzed or isolated spinal cord
preparations of lamprey (Cohen and Wallen 1980;
Poon 1980; Wallen and Williams 1984),
dogfish (Grillner et al. 1976), goldfish (Fetcho
and Svoboda 1993), and amphibian tadpoles (Kahn and
Roberts 1982; Kahn et al. 1982; Soffe and
Perrins 1997; Soffe et al. 1983; however, see
Blight 1977; Stehouwer and Farel 1980).
Phase lag per segment averaged 1.8 ± 0.6%, a value similar to
the 2.1% reported in a related cyprinid (goldfish; Fetcho and Svoboda 1993) but considerably larger than the value (1%)
reported in the lamprey (Wallen and Williams 1984).
Therefore a larval zebrafish with 30-34 myotomal segments will have
approximately 58% of a full wave of undulatory activity along its body
at any point in time. This compares with 63% in goldfish (29-30
segments) and a full wave (100%) in lamprey (approximately 100 segments). A full wave of activity is a characteristic of anguilliform
swimming, while the briefer wave of activity observed in zebrafish and
goldfish is a characteristic of subcarangiform swimming (Lindsey
1978). Thus although visual inspection of swimming larval
zebrafish revealed an eel-like (anguilliform) style of swimming
(Buss and Drapeau 2001a), examination of phase lag
values reveal the subcarangiform style used by the adult. During
carangiform swimming, anterior myotomes are active for a longer
duration than caudal myotomes; i.e., some ipsilateral and contralateral
muscle is synchronously active (Altringham and Ellerby
1999; Wardle et al. 1995). Whether a
rostral-caudal variation in muscle activation exists in larval zebrafish was not determined. One prediction of this pattern of muscle
recruitment would be different motoneuron output in the rostral and
caudal spinal cord during fictive swimming.
Larval locomotor muscle recruitment
ER and EW muscle fibers were recruited for both burst and
beat-and-glide swimming. At the highest rates of fictive undulatory swimming, ER fiber activity was reduced but not abolished, whereas at
the slowest fictive swimming rates ER fibers could be active in
isolation. These swimming rates were comparable to those observed in
free swimming zebrafish (Budick and O'Malley 2000;
Buss and Drapeau 2001a) as well as those previously
observed during fictive swimming (Buss and Drapeau
2001a). Thus the pattern of muscle recruitment in larval
zebrafish was organized as in adult fishes, where red muscle is
recruited during slow undulatory swimming (Bone 1978;
Coughlin and Rome 1996) and de-recruited at the fastest unsteady burst speeds when white muscle is recruited (Jayne and Lauder 1996). The neural basis for this muscle recruitment is unknown. However, the present findings and those of Bone
(1966), Jayne and Lauder (1994), and Mos
et al. (1990) indicate that two unique populations of
motoneurons, that can be activated or inactivated independently of each
other, innervate ER and EW muscle fibers.
A de-recruitment of slow (i.e., red muscle) muscle fibers during
locomotion is not unique to fishes. In crabs, tonic firing of the
common inhibitor neuron abolishes residual tension in slow tonic (but
not fast phasic) muscle fibers during rapid walking and swimming
(Bevengut and Clarac 1990; Rathmayer
1990; Wiens 1989).
The facilitation of fictive swimming EPPs in larval ER muscle
fibers was likely due to summation of filtered and attenuated EPPs from
adjacent electrically coupled ER fibers (Buss and Drapeau 2000). ER fibers have a low-contraction threshold
(approximately 40 mV) and many similarities to vertebrate slow tonic
muscle (i.e., outward rectification, a depolarized resting potential, and a low-chloride permeability; unpublished observations). During swimming, EPPs from neighboring ER fibers may summate to contraction threshold and provide a tonic level of muscle contraction, on which is
superimposed the rhythmic swimming contractions. The locomotor function
of tonic ER activation might include body stiffening, maintenance of
posture, or steering, but its true function or existence remains to be
determined. EW fibers have a high contraction threshold, which is
likely reached in an all-or-none fashion via a regenerative
voltage-activated current. Thus tonic muscle activation would not be
expected in EW fibers which have characteristics more similar to
vertebrate twitch muscle (i.e., a nearly linear I-V near the
resting potential, a hyperpolarized resting potential, and a
high-chloride permeability; unpublished observations). Recently Ono et al. (2001) observed action potentials in
dissociated larval zebrafish muscle, a property not observed by
Buss and Drapeau (2000). This was attributed to a
combination of weak, undeveloped voltage-gated conductances and the
inability to charge the membrane fast enough from a point source of
current due to fiber cable properties. However, reexamination in vivo
has revealed the presence of a TTX-sensitive action potential in some
EW fibers (but not ER fibers) dialyzed with a low-chloride
patch-pipette solution and with resting potentials < 85 mV
(unpublished observations), thus revealing further similarities between
EW fibers and vertebrate twitch muscle. Thus although ER and EW fibers
have many similar electrophysiological properties (i.e., input
resistance, miniature EPP time course, and amplitude), they are
functionally unique and receive different recruitment during swimming,
and due to differences in electrical coupling, different degrees of
synaptic facilitation.
Embryonic fictive swimming and coiling
Embryonic (day 1) ER and EW fibers both have extensive
electrical coupling and were examined to provide evidence that the summated fictive swimming EPPs were due to electrical coupling and not
EPP kinetics. As predicted, EPPs summated in both day 1 ER and EW
fibers during fictive swimming. In contrast to larval fictive swimming
(day 3), ER and EW fibers were recruited similarly in embryos (day 1).
Rhythmic EPPs assumed to underlie fictive swimming occurred at a lower
frequency in embryos than in larvae as observed by Buss and
Drapeau (2001a) and Saint-Amant and Drapeau (1998) in behaving zebrafish. A second, slower and more robust fictive motor pattern that had the characteristics of the coiling behavior of embryonic fishes was also observed in embryos. However, the
coiling observed in this study is not identical to the coiling and
fictive coiling behavior described in younger embryos (Myers et
al. 1997; Saint-Amant and Drapeau 1998, 2000)
where single coils are observed. Rather they are more similar to the
bursts of coils observed in zebrafish embryos >24 hpf
(Saint-Amant and Drapeau 1998) and in the angelfish
(Yoshida et al. 1996).
In conclusion, the motor output observed in paralyzed larval zebrafish is coordinated appropriately for generating undulatory swimming. Furthermore, at the early developmental stages examined in this study, muscle recruitment and swimming style (subcarangiform) were similar to that of adult fishes. Thus there is a considerable degree of sophistication in the organization of the locomotor circuitry at the onset of development of locomotion in the zebrafish.
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ACKNOWLEDGMENTS |
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R. R. Buss holds a Canadian Institutes of Health Research (CIHR) Doctoral Research Award.
This work was funded by the CIHR and the Natural Sciences and Engineering Research Council of Canada.
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FOOTNOTES |
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Address for reprint requests: P. Drapeau, Dept. of Neurology, Montreal General Hospital, 1650 Cedar Ave., Montreal, Quebec H3G 1A4, Canada (E-mail: pierre.drapeau{at}mcgill.ca).
Received 9 August 2001; accepted in final form 12 November 2001.
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REFERENCES |
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TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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a lamprey perspective.
Ann NY Acad Sci
860:
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