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Previous Article | Next Article
The Journal of Neuroscience, April 15, 2001, 21(8):2759-2767
Patterns of Neural Circuit Activation and Behavior during Dominance Hierarchy Formation in Freely Behaving Crayfish
Jens Herberholz, Fadi A. Issa, and Donald H. Edwards Department of Biology, Georgia State University, Atlanta, Georgia 30302-4010
ABSTRACT
TOP
ABSTRACT
INTRODUCTION
Creation of a dominance hierarchy within a population of animals typically involves a period of agonistic activity in which winning and losing decide relative positions in the hierarchy. Among crayfish, fighting between size-matched animals leads to an abrupt change of behavior as the new subordinate retreats and escapes from the attacks and approaches of the dominant (Issa et al., 1999
). We used high-speed videography and electrical recordings of aquarium field potentials to monitor the release of aggressive and defensive behavior, including the activation of neural circuits for four different tail-flip behaviors. We found that the sequence of tail-flip circuit excitation traced the development of their dominance hierarchy. Offensive tail flipping, attacks, and approaches by both animals were followed by a sharp rise in the frequency of nongiant and medial giant escape tail flips and a fall in the frequency of offensive tail flips of the new subordinate. These changes suggest that sudden, coordinated changes in the excitability of a set of neural circuits in one animal produce the changes in behavior that mark its transition to subordinate status.
Key words: crayfish; fighting; agonistic interaction; dominance hierarchy; social behavior; field potential; escape; command neuron; tail flip; neural circuit activation
INTRODUCTION
Social dominance hierarchies are an organizing mechanism for most animal societies (Wilson, 1975
Decapod crustaceans, especially lobsters and crayfish, provide a useful model for the study of the neural mechanisms of hierarchy formation (Kravitz, 1988
The often sudden change in the behavior of one animal from fighting to escaping marks the decision point at which the social hierarchy is determined. The neural mechanisms in crayfish and lobsters that underlie this decision are unknown but may involve changes in the threshold of neural circuits that mediate discrete behavior patterns displayed during agonistic interactions. Three well known circuits for tail-flip escape are obvious candidates. The lateral giant (LG) and medial giant (MG) circuits are each organized around a set of giant interneurons that function as command neurons to trigger stereotyped tail-flip escapes in response to massive phasic sensory stimulation of the abdomen or cephalothorax, respectively (Edwards et al., 1999
Changes in LG threshold can occur via the imposition or removal of "tonic inhibition" or by application of the neuromodulator serotonin (Glanzman and Krasne, 1983
It is not known whether tonic inhibition is removed or serotonin is released in crayfish during fighting. If they are, the excitability of the LG circuit (and perhaps that of the MG and NG circuits as well) might be increased in isolates, in new dominants, and in new subordinates as they fight to determine a dominance hierarchy. Here we determine whether changes in the excitability of these circuits occur by recording their patterns of activation in freely behaving pairs of juvenile crayfish (Procambarus clarkii) as they interact to form a dominance hierarchy. By tracking the occurrence of each tail-flip behavior in two crayfish as one becomes dominant and the other subordinate, we can gain insight into how shifts in the thresholds of an ensemble of circuits can produce coherent new patterns of social behavior.
We have recorded the activation of each escape circuit in freely behaving juvenile crayfish by recording the tail-flip behavior and the associated change in the electric field around the animal. Activation of each tail-flip circuit creates a distinct electrical field potential pattern in the water surrounding the animal (Fricke, 1984
MATERIALS AND METHODS
Sixteen juvenile crayfish (P. clarkii; 2.2-3.0 cm) of both sexes that had been raised individually in isolation since becoming free-swimming (>4 months) were used throughout this study. Extracellular nerve and muscle potentials were recorded with a bipolar pair of electrodes implanted on the abdominal ventral nerve cord. Wire leads from the ventral cord electrodes were fixed to the carapace by superglue and connected to a differential amplifier (A-M Systems). Amplified (1000×) signals were displayed on an oscilloscope, digitized at 6.7 kHz, and recorded in a personal computer with Axoscope (Axon Instruments). Field potentials from the aquarium bath were recorded with a second pair of copper wire electrodes (1 mm outer diameter, insulated except at the tips) placed at either end of the 9.5 cm (length) by 1.5 cm (width) by 5.5 cm (height) aquarium (Fig. 1A). These potentials were similarly amplified, displayed, and recorded. The recorded signals from the implanted and bath electrodes were similar in amplitude in part because the small aquarium size limited spread of the electric field away from the animal. The aquarium was filled with deionized water to a depth of 5.5 cm, and the bottom was covered with gravel to facilitate walking. Sharp taps delivered by a handheld probe to the abdomen evoked an escape tail flip mediated by the LG interneurons, whereas taps delivered to the cephalothorax evoked a tail flip triggered by the MG interneurons (Wine and Krasne, 1972
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Figure 1. Experimental arrangement and the escape circuitry of crayfish. A, Experimental setup. Neural and muscular activity of one (control) or two (fighting) juvenile crayfish placed in a small test aquarium was recorded with implanted and bath electrodes or with bath electrodes alone. The reflected oscilloscope image of the signals was recorded in the top half of a high-speed video that also captured the tail-flip behavior of the animal(s) at 5 msec/frame. B, Escape tail-flip circuitry of the crayfish. Primary mechanosensory afferents on the abdomen (top row of red circles) excite the LG neurons directly and through an intervening layer of mechanosensory interneurons (second row of red circles). The LG neurons in anterior segments excite motor giant motor neurons in the anterior part of the abdomen but not in the posterior part. The LGs also excite the segmental giant interneurons (green circles) in each segment, and the segmental giants then excite premotor interneurons and the set of fast flexor motor neurons in the anterior abdominal segments. These two sets of motor neurons excite fast flexor muscle in the anterior abdomen. Their contraction produces a rapid flexion around the thoracic-abdominal joint, which pitches the animal up and forward (bottom right). The MG neurons (blue circles) are excited by phasic visual and mechanosensory input to the cephalothorax and produce a rearward tail flip (blue; below left) by exciting motor giant and fast flexor motor neurons in all the abdominal segments. The NG neurons (box labeled non-G) are excited by less phasic stimuli delivered anywhere on the body surface. At much longer latency, they excite fast flexor motor neurons in several segments to produce a pattern of abdominal flexion that will carry the animal away from the stimulus source. SG, segmental giant; MoG, motor giant motor neurons; FF, fast flexor motor neurons. MoG and FF are shown for abdominal segments 2-5 only. The asterisks refer to the FF muscles in abdominal segments 2-5 that are excited by the LG (red) and MG (blue) neurons. VCR, videocassette recorder. Reprinted from Edwards et al. (1999)
Video recordings were used alone to identify three behavior patterns (attack, approach, and retreat) (Issa et al., 1999
RESULTS
Comparison of recordings from the aquarium electrodes and implanted electrodes
Comparison of the amplified signals from the aquarium electrodes and the implanted electrodes revealed very similar electrical potential waveforms (Beall et al., 1990
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Figure 2. Digitized recordings from the implanted (top traces) and bath (bottom traces) electrodes with simultaneously recorded video frames of the tail-flip behavior of the animal. Each video frame also displays the reflected oscilloscope trace of the bath recording (at the top of each frame; the frames are each left-right reversed so that increasing time of the oscilloscope trace is from left to right), the animal, and the stimulus probe (white diagonal line). The bracketed periods of each trace correspond to the period of the frame displayed below. A, MG tail-flip response caused by a phasic probe stimulus to the front of the animal. The field potential includes the MG giant spike potential (* and magnified in the dashed box inset to the left of the trace), the large, phasic MoG potential, and the lower-amplitude potentials produced by the FF motor neurons and FF muscles. B, LG tail-flip response caused by a phasic probe stimulus to the abdomen. As for MG, the LG field potential includes the LG spike potential (* and magnified in the dashed box inset), the MoG potential, and the FF motor neuron and FF muscle responses. C, NG tail-flip response to a nonphasic probe stimulus to the thorax. The field potential consists only of FF motor neuron and FF muscle potentials. No giant spike potential was recorded.
To determine whether the field potentials recorded from unimplanted, freely behaving animals were the same as those recorded from implanted animals, potentials evoked during each of the three types of tail flip were recorded five times in each of 16 unimplanted crayfish. There were no qualitative differences between the field potentials recorded from unimplanted animals and the corresponding potentials from implanted animals.
Each type of field potential in the unimplanted animals had a distinct amplitude and duration. The mean peak-to-peak amplitude of the MoG potential (3.4 ± 1.2 mV, mean ± SD) evoked by an MG spike was significantly greater (p < 0.05, Friedman test of repeated measurements on ranks) than the MoG potential evoked by LG (2.3 ± 0.8 mV) or the largest potential evoked by NG (1.4 ± 0.7 mV). However, the duration of the MoG potential evoked by LG (1.9 ± 0.4 msec, mean ± SD) was significantly longer than that evoked by MG (1.4 ± 0.1 msec). The duration of the largest biphasic NG potential (2.6 ± 0.5 msec) was significantly longer than either of the MoG potentials (p < 0.01, Friedman test of repeated measurements on ranks). The mean durations (± SD) of the entire LG- and MG-related field potentials were similar (18.1 ± 1.8 and 15.0 ± 1.0 msec, respectively), and both were shorter than the entire NG field potential (23.8 ± 2.4 msec). Although the mean values of each measurement of the different potentials were significantly different, their ranges overlapped.
Categorization of tail flips during interactions between crayfish
Categorization of a tail flip depends on the correlation between the high-speed video recording of the tail flip and the simultaneously recorded field potential. The field potentials were evoked only by tail flips, and animals were never seen to tail flip simultaneously, so that attribution of the field potential to a tail-flipping animal is unambiguous.
NG tail flips can take any behavioral form, including those typical of LG and MG tail flips, but they have a much longer response latency than do LG or MG tail flips in response to an applied mechanical stimulus (Wine and Krasne, 1972
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Figure 3. Recordings from the bath electrodes and tail-flip behavior during fighting. A, NG tail-flip field potential. The field potential lacks the giant spike potential and the large MoG potential characteristic of a giant neuron response and consists only of FF muscle potentials in response to the FF motor neurons. B, MG circuit activation and tail-flip field potential. The MG spike potential (*) and the large, biphasic MoG potential can be seen, followed by the lower-amplitude response of the FF muscle to the FF motor neurons. C, Offensive tail-flip field potential (top) and behavior (bottom). The signal is identified by its small amplitude and extremely long signal duration and results from a prolonged activation of the FF muscle by the FF motor neurons. No giant spike potential is recorded. Bracketed periods of the trace correspond in time with the sequence of frames.
Although both LG and MG tail flips produce an initial MoG field potential, their tail-flip trajectories are readily distinguishable. Crayfish bend only the first three abdominal segments during LG tail flips, but bend all abdominal segments during MG tail flips, and so produce distinct trajectory angles for each type of giant tail flip (Wine and Krasne, 1972
Field potentials and tail-flip behaviors during agonistic interactions
After a 1 d period of rest, the 16 juvenile crayfish used in the control experiments were paired for 30 min with another animal from the group of the same size and opposite sex. The two animals began a series of mutual agonistic encounters that soon resulted in one animal escaping and retreating in response to the attacks and approaches of the other.
The LG, MG, and NG tail flips that occurred during fighting were readily recognizable. They and the accompanying voltage records (Fig. 3A,B) were indistinguishable from the corresponding records obtained previously from the same animals when isolated and from the implanted animals (Fig. 2). The peak-to-peak amplitudes and durations of the electrical field potentials were measured before and after pairing. There were no differences in the measurements of each tail flip between dominant and subordinate animals or within one animal before and after pairing. NG tail flips occurred both as the initial response to an attack (NG tail flips) and during swimming movements that followed each of the three types of escape (Swim tail flips).
A fourth, previously undescribed form of tail flip (offensive) occurred only when the tail-flipping animal had a secure grip on its opponent (Fig. 3C). These OTs began with an abdominal extension followed by several (2.9 ± 1.4, mean ± SD) abdominal flexions and reextensions. The duration of the entire offensive potential (74.1 ± 5.3 msec) exceeded all other tail-flip potentials and correlated with a longer-duration abdominal movement (Fig. 3C). These characteristics make OTs readily distinguishable from NGs and giant neuron-evoked tail flips. The abdominal extensions were accompanied by a spread of the tailfan that was maintained during the abdominal flexion, which occurred primarily around the anterior abdominal segmental joints, while the posterior segments remained extended. This configuration helped to throw the animal up into the water column, above the opponent held in the grasp of the tail-flipping animal.
Patterns of tail-flip circuit activation and behavior during dominance hierarchy formation
The relative dominant and subordinate status of each pair was determined from counts of the numbers of attacks, approaches, escapes, and retreats that occurred throughout the interaction (Issa et al., 1999
Dominance hierarchy formation between two crayfish began with fighting that differed in intensity and duration among eight pairs of animals, from a pair of one-sided interactions with little fighting to a prolonged, intense fight that lasted almost 4.5 min before it was interrupted by the withdrawal of one animal. In six of eight pairs of animals, initial bouts of fighting included attacks, approaches, and OTs by both animals and few defensive behaviors such as retreats or escapes (Fig. 4). OTs usually occurred in alternating bouts, in which several tail flips made by one animal were followed by a series of OTs by the other. The future dominant animal always displayed the final bout of OTs before dominance status was decided, and it displayed more OTs than did the future subordinate. The status decision was apparent when a sudden change in the behavior of one animal, the future subordinate, occurred. The aggressive behavior of this animal, including attacks, approaches, and offensive tail flips, ceased, and defensive behavior, including a series of escapes, retreats, and swims, began (Fig. 4). The new dominant animal maintained its aggressive behavior after the decision and persisted with attacks and approaches. In three of the pairs the initial fight was decisive and produced a sharp switch from offensive to defensive behavior in one animal, while the other continued to behave offensively. This is illustrated by the ethogram of Figure 4A, in which the different behavioral events are displayed according to their time of occurrence (top) and according to their order of occurrence (bottom). The temporal display shows that for this pair, most of the activity occurred within the first 10 min of interaction. The bottom display shows that the decision of one animal to withdraw and cease offensive behavior was abrupt. The temporal display shows that the level of agonistic activity by both animals declined over the remaining part of the half hour. The ethograms of two other pairs of animals are similar (data not shown): an abrupt change in the behavior of one animal persists throughout the remainder of the 30 min interaction. In four other pairs the initial decision was incomplete: having switched from offensive to defensive behavior once, the new subordinate animal reengaged the new dominant with brief bouts of offensive behavior. An example is seen in Figure 4B, in which after an initial decision after 5 min of interaction, the new subordinate reengaged the new dominant with periodic approaches, offensive tail flips, and attacks. These were isolated events in all the pairs and did not change the balance of behavior between the animals.
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Figure 4. Sequence of tail-flip circuits activated and behavior patterns displayed by two of the eight pairs of animals during the 30 min period of dominance hierarchy formation. Events are presented according to their time of occurrence (top) and in their order of occurrence (bottom). X and O symbols mark the behavior of the new dominant and subordinate animals, respectively. The dashed vertical lines give the approximate time of the dominance decision. OT, MG-evoked, NG-evoked, and Swim nongiant-evoked tail flips are activated. A, A pair in which the initial decision (dashed vertical line) was decisive. B, A pair in which the new subordinate reengaged the new dominant at intervals after the initial decision (dashed vertical line).
The changes in behavior over time can be seen in the plots of Figure 5, where the frequencies of each behavior are expressed as the total number of occurrences in all animals in 5 min periods over the 30 min period of interaction. The period between their introduction and the onset of vigorous fighting differed among the pairs. This onset was marked by the first tail flip, whether an escape or an OT, which enabled the time series of responses from all eight pairs to be compared by aligning them along the time axis with the time of the first tail flip at time 0. Dominant and subordinate animals made similar numbers of attacks, approaches, and retreats during the period before that first tail flip (Fig. 5A). The greatest aggressive activity occurred during the first 5 min after the initial tail flip, when large numbers of attacks (45), approaches (20), and offensive tail flips (85) by the dominant animal evoked correspondingly high frequencies of retreats (21) and escape tail flips of all types (210) by the subordinate, the vast majority of which were NG and Swim tail flips (194). Dominant animals in all pairs produced few retreats (2) or escape (LG, MG, or NG) tail flips (24) within the first 5 min of vigorous interaction, whereas the subordinate produced few attacks (7), approaches (1), or offensive tail flips (36) during this period (Fig. 5). Both types of animals produced a small number of MG tail flips, with the greater number being produced by the subordinates (dominants, 11; subordinates, 16).
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Figure 5. Patterns of offensive and defensive behavior during 30 min of interaction between eight pairs of unacquainted crayfish. Total numbers of events are shown for dominant (top) and subordinate (bottom) animals in all eight pairs in sequential 5 min periods. The first tail flip of each pair marks the beginning of the first 5 min period (i.e., time 0) for that pair; the sequence of periods of each pair is aligned with that mark. A, Attacks, approaches, and retreats. Before indicates behavioral events that occurred before the first tail flip. B, Different types of tail-flip behavior. The 5 min periods correspond to the similarly labeled periods in A.
Both dominants and subordinates performed many fewer offensive tail flips (14 and 5, respectively) during the second 5 min period (Fig. 5B), after the decision had been made for most pairs. The drop in OTs reflects the absence of fighting in which the animals grapple each other. The dominant animals persisted in approaching (22) and attacking (27) the subordinates, which responded by retreating (21) and escaping (127). Only 5 of these escapes were of the more forceful MG type, reflecting the reduced level of aggressiveness of the dominant animals.
The level of aggressiveness of the dominant animals fell almost linearly to ~15% of its initial level after 30 min, as reflected in the decline in the numbers of attacks and approaches (Fig. 5). An increase in the number of attacks by the dominant animal in two pairs occurred in the fourth 5 min period (15-20 min) and accounts for the deviation from the downward trend in summed agonistic activity. The dominant member of one of those pairs also produced the increase in the number of OTs reported during that period (Fig. 5). The frequency of retreats and NG escapes (including Swim) by the subordinate fell in parallel with the decline in attacks and approaches by the dominant. MG tail flips occurred primarily during the first period of intense interaction, primarily in the subordinate animal. MG tail flips continued at a low level in both animals throughout their interaction. The only LG tail flip recorded in all pairs occurred when a dominant animal struck a subordinate on the abdomen during the second 5 min period.
The differences in the behavior of dominant and subordinate animals are made clear in Figure 6. Dominant animals made more attacks than did subordinates (p < 0.01, Wilcoxon signed rank test) and more approaches (p < 0.02), more OTs (p < 0.04), fewer retreats (p < 0.02), fewer NG tail flips (p < 0.01), and fewer swim tail flips (p < 0.01) than did subordinate animals. No significant differences occurred in the number of MG tail flips made by dominant and subordinate animals.
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Figure 6. The average numbers of different agonistic behavior patterns (± SD) performed by dominant and subordinate animals in eight pairs during 30 min of interaction (**, significantly different with p < 0.01; *, significantly different with p < 0.05; Wilcoxon signed rank test).
DISCUSSION
Field potential measurements and tail-flip circuit activation
Field potential measurements have provided a means for distinguishing between giant neuron-evoked and NG-mediated tail flips in freely behaving crayfish (Beall et al., 1990
The use of field potential recordings to identify patterns of tail-flip circuit activation takes advantage of the large size of the giant fibers and the specific circuit arrangement via which they trigger a tail flip. The large phasic potential that follows the LG or MG spike (Fig. 2A,B) results from the almost synchronous excitation of the set of abdominal MoG motor neurons and the subsequent almost synchronous excitation of the segmental FF muscles that the MoGs excite (Heitler and Darrig, 1986
No large impulse appears during NG activation in either Procambarus or Cherax (Finley and Macmillan, personal communication) because the NG circuit makes no use of the MoG motor neurons. Instead, the NG circuit excites a set of nongiant FF motor neurons in each abdominal segment according to the needed pattern of abdominal flexion. The FF motor neurons excite subsets of FF muscles, and this pattern of muscle excitation accounts for the longer, lower-amplitude field potentials recorded during an NG tail flip. The similar pattern of low-amplitude field potentials that follows the initial phasic MoG response when LG or MG is activated also results from excitation of the FF motor neurons and their excitation of the FF muscle. Whereas the MoG motor neurons are excited by en passant synapses made directly by the LG and MG axons (Furshpan and Potter, 1959
Offensive tail flips may be a variant of the NG escape tail flip but are more likely to be produced by a circuit that is distinct from the three escape circuits. The hallmark of the OT is the slow abdominal flexion performed as the animal grasps its opponent. The NG tail flip is much faster but might conceivably be slowed if the animal were to perform it while dragging a heavy load. The animal drags its opponent during an OT, but the direction of the tail flip is initially upward and perpendicular to the axis of the connection between the animals. The perpendicular direction of the tail flip relative to the direction of the inertial force of the load (i.e., the opponent) suggests that the force developed by the abdominal flexion should initially be primarily unaffected by the load of the opponent. As a result, one would expect that the initial flexion of an NG tail flip would be rapid until the load slows it down. This is not what happens. An OT begins with an extension that is immediately followed by a slow flexion that throws the animal upward. This result suggests that the OT differs categorically from the NG tail flip.
Sequences of behavior that lead to hierarchy formation
Previous studies have shown how the expression of agonistic behaviors, including approaches, attacks, retreats, and escapes, changes over 2 weeks after the formation of a dominance hierarchy (Issa et al., 1999
Changes in the pattern of tail-flip circuit activation underlie part of the behavioral change that occurs as one animal becomes dominant and the other subordinate. These changes hinge on a decision point when the prospective subordinate switches from offensive tail flipping and fighting to initiating repeated MG and NG escapes. The change in circuit activation appears to result from corresponding changes in the thresholds for excitation of the different circuits (Krasne et al., 1997
The use of tail-flip circuits during hierarchy formation
These experiments have changed our view of the three different escape circuits and the ways in which the animal uses them. The LG and MG have been seen as escape command neurons that trigger rapid, reflexive escapes upward or backward in response to rearward or frontward attacks, respectively (Wiersma, 1947
The current experiments make clear that stimulus conditions necessary for the MG and NG tail flips change significantly in new subordinate animals, whereas the adequate stimulus for LG appears not to change. Both the MG and NG circuits appear to become more excitable after dominance has been decided. Many of these MG tail flips cannot be readily attributed to any stimulus other than the nearby presence of the dominant animal, suggesting that the MG threshold decreases significantly during fighting and may even become "voluntary." Subordinates performed 20 of the 29 voluntary tail flips seen in all eight pairs of animals, and they performed more of them than did dominants in six pairs, suggesting that the threshold for activating an MG tail flip is lower in subordinates than in dominants. The greatest change in apparent threshold was experienced by NG escape behavior, which was a rare event before the status decision was made and quickly became the predominant behavior of the subordinate animal afterward.
Previous studies suggested that serotonin may be released during fighting between crayfish, where it promotes an aggressive posture, reduces the motivation of a subordinate to retreat (Livingstone et al., 1980
Offensive tail flipping has not been described previously but appears to play an important role in dominance hierarchy formation between size-matched crayfish. During initial fighting, crayfish appear to use bouts of repeated OTs to drag their opponent and gain a position above it. The alternation in bouts of OTs between two animals as they grapple suggests that each is trying to demonstrate its size and strength to the other. The slow rate of abdominal flexion relative to escape movements is consistent with this suggestion in that OTs are not used to injure or dismember an opponent. The future dominant displays more OTs in each bout, more bouts, and the last bout before the status decision. The decision often followed the last bout quickly, as the subordinate displayed a series of NG tail flips that signaled its defeat. We conclude that the OTs appear to provide a means for each crayfish to assess its strength relative to its opponent and to reach a status decision without suffering injury.
The neural mechanisms that account for the coordinated changes in circuit thresholds associated with the change in status are unknown but may include the tonic inhibitory mechanisms and serotonergic modulation that have been found previously to affect the LG threshold (Vu and Krasne, 1993
FOOTNOTES Received Sept. 28, 2000; revised Dec. 22, 2000; accepted Jan. 4, 2001.
This work was supported by National Science Foundation Grant IBN 9726819.
J.H. and F.A.I. contributed equally to this work.
Correspondence should be addressed to Dr. Donald H. Edwards at the above address. E-mail: biodhe{at}panther.gsu.edu.
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