1Neuroscience Training Program and 2Department of Physiology, University of Wisconsin, Madison Wisconsin 53706
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ABSTRACT |
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Populin, Luis C. and Tom C. T. Yin. Kinematics of Eye Movements of Cats to Broadband Acoustic Targets. J. Neurophysiol. 82: 955-962, 1999. Operant conditioning was used to train cats with their heads immobilized to localize sound by directing their eyes to the location of the sources. The kinematics of those eye movements were studied and compared with eye movements to visual targets at the same locations. The main finding of this study is that eye movements to broadband long-duration acoustic targets have two components: an initial slow phase of variable duration and a fast, normal saccade. The slow component is characterized by a persistent, shallow velocity ramp, while the saccadic component of the response falls on the main sequence computed from eye movements to visual targets. The slow component was shorter before saccades to long-duration stimuli performed under the delayed-saccade task and practically absent before saccades to transient acoustic stimuli. The results suggest that the initial slow component is used by cats to deal with uncertainty associated with the location of long-duration broadband targets and that the input to the saccade integrator(s) is similar under both visual and acoustic conditions.
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INTRODUCTION |
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Eye movements of cats to visual targets are
characterized by a sharp accelerating initial segment of roughly
constant duration (Evinger and Fuchs 1978), typical of
saccadic responses in other species (Baloh et al. 1975
;
Fuchs 1967
; Hyde 1959
). The larger the
angular distance moved, the higher the maximal velocity achieved (Bahill et al. 1975
; Boghen et al. 1974
).
This relation between maximal eye velocity and movement amplitude is
roughly linear in cats (Evinger and Fuchs 1978
), but in
primates the function saturates for saccades larger than ~20°
(Bahill et al. 1975
; Fuchs 1967
). A plot
of this relationship, known as the main sequence (Bahill et al.
1975
; Boghen et al. 1974
), is a standard tool
for determining if an eye movement falls in the category of saccades.
When the triggering signal for a saccade is nonvisual, such as an
acoustic target, a direct effect on the dynamics has been reported in
the form of a slower peak velocity (Engelken and Stevens 1989; Russo and Bruce 1994
; Zahn et al.
1978
; Zambarbieri et al. 1982
). However, the
data are not in full agreement as Whittington et al.
(1981)
reported no differences between the kinematics of saccades to visual and auditory targets in monkeys.
Anticipatory eye movements have been observed before smooth pursuit of
a moving target (Becker and Fuchs 1985; Boman and
Hotson 1988
; Kowler and Steinman 1979a
) and
before saccades evoked by target steps of predictable direction
(Kowler and Steinman 1979b
; Moschner et al.
1996
). Eye movements of this type required a retinal signal,
did not result from attention shifts or practice, and could not be
suppressed voluntarily. Although with lower frequency, such movements
also were observed under conditions in which the amplitude and time of
onset of the step were randomized (Kowler and Steinman
1979b
).
Here we report an unusual type of eye movement in cats characterized by
a slow velocity ramp that consistently preceded saccades to the
location of long-duration, broadband noise targets. This eye movement
is observed consistently under the standard-saccade conditions used in
our sound localization studies (Populin and Yin 1998),
unaffected by practice, shortened by delaying the execution of the
response, and absent in responses to transient auditory stimuli. When
the slow velocity ramp is removed from the eye movement records, the
remaining quick component resembles a normal saccadic eye movement. The
slopes of the regression lines fit to the main sequences of saccades to
acoustic targets are similar to that of the saccades to visual targets.
These results suggest that the initial slow component reflects the
uncertainty associated with the location of long-duration broadband targets.
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METHODS |
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General
A detailed description of the methods and training procedures is
found in Populin and Yin (1998). Briefly, under sterile
surgery we implanted cats with a small stainless steel head post
modified from May et al. (1991)
and eye coils
(Judge et al. 1980
) to measure eye position with the
magnetic search coil technique (Robinson 1963
). During
experimental sessions, the cats were placed in a canvas bag and their
heads restrained with a bar, modified from McHaffie and Stein
(1983)
, attached to the head post from behind. The experiments
were conducted in a dimly illuminated, sound-attenuated chamber with
sound-absorbent foam covering the inner walls and major pieces of equipment.
Stimuli and eye-movement recordings
Acoustic stimuli consisted of long-duration (500-1,200 ms),
broadband (0.1-25 kHz) noise bursts and single (100 µs) clicks presented from any one of 15 speakers positioned 62 cm away from the
center of the cat's head, along arcs in the horizontal or median
sagittal plane, within the cat's oculomotor range (±25°) (Guitton et al. 1984). Visual stimuli consisted of red
light-emitting diodes (LEDs) attached to the center of the speakers.
The size of the speakers dictated a minimal separation of 9° between
LEDs, which restricted the spacing and range of saccade amplitudes
studied. In addition, cats rarely made saccades greater than ~15°
to acoustic targets due to undershooting the target (Populin and
Yin 1998
). The speaker/LED assemblies were behind a black
cheesecloth curtain that allowed the LEDs to be seen when lit and
sounds to be heard. The position of the targets was specified with
reference to the primary position (0°, 0°) defined as the point at
eye level on the midline directly in front of the cat, with positive
angles to the right or upward.
The analogue output of the coil system (CNC Engineering, Seattle, WA) was digitally sampled at 500 Hz with a 12-bit A/D converter. The experimental setup, including stimulus presentation and data collection, was controlled with a MicroVAX2 (Digital Equipment, Maynard, MA) computer running custom software.
Experimental sessions and tasks
The cats were trained using operant conditioning to look at the
location of acoustic stimuli with their heads fixed. The experimental sessions consisted of a mixture of various tasks (fixations, standard and delayed-saccades, and sensory probes to visual and auditory stimuli) presented in random order from any of the speaker/LED assemblies so that the cat could not predict the type or the position of the upcoming target (Populin and Yin 1998). The
length of each experimental session was primarily determined by the
cat's willingness to participate. Typically sessions ranged between 3 and 5 h and included ~500 trials per day.
The standard-saccade task was used with two stimuli, the long duration noise and transient click stimuli. It began with a fixation LED presented at the primary position that the cat had to look at for 500-1,500 ms. Coinciding with the offset of the LED, an auditory or visual target was presented at a different location within the cat's oculomotor range. The duration of the long-duration stimuli was measured from the time the eyes entered the acceptance window set around the target.
The delayed-saccade also started with a fixation LED presented at the primary position, but its offset, which signaled the cat to make a saccade to the target, was delayed (300-700 ms) with respect to the presentation of the target. Only long-duration stimuli were used with this task.
Square electronic acceptance windows were set around the targets to
provide a spatial margin of error: 2-5° for visual targets and
6-12° for acoustic targets. Larger windows were used for acoustic targets because the cats made larger errors in looking at these targets. For a discussion of the rationale for selecting the size of
the windows, see Populin and Yin (1998). In both the
standard- and delayed-saccade tasks, the cats were required to make a
saccade to the target within 1,500 ms after the offset of the fixation LED. A food reward was delivered at the end of each trial in which the
temporal and spatial criteria were met.
Data analysescriteria to determine the start and end of the eye
movements
Analyses were conducted off-line with custom graphics software that displayed horizontal and vertical eye position, several time derivatives of eye position, and other parameters used for data analyses. Eye position signals were smoothed digitally with a 5- to 11-point moving window average. Velocity was computed at each point using a first-order least squares fit on successive five-point windows. The procedure was repeated to compute higher-order derivatives. Although we designed the data analysis to be objective, we still found it necessary in <5% of the cases to intervene and override the points chosen by the program, usually due to noise artifacts.
Two events, the end of fixation and return to fixation, were computed
from the time at which eye velocity departed from and returned to,
respectively, within 2 SD of its mean baseline. The mean baseline was
computed from the velocity trace during the time interval comprising
100 ms before to 30 ms after the onset of the stimulus, during which
time the eye was expected to be stationary. The eye position at the
time of these two events defined the start and end of the saccade (Fig.
3 in Populin and Yin 1998).
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RESULTS |
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The kinematic analyses that follow were carried out to quantify
differences in cat eye movements to acoustic and visual targets. Most
of the data presented in this report were recorded during the sound
localization experiments presented previously and were selected from
experimental sessions that had a large number of trials in the
conditions of interest (Populin and Yin 1998). Because we did not screen these data in any other way, they are representative but only a small fraction of the entire set. Only trials that met the
temporal and spatial criteria for success were analyzed. The percent of
successes ranged between 65 and 88% for the standard-saccade task
with long-duration stimuli, between 60 and 68% with transient stimuli,
and between 35 and 80% for the delayed-saccade task. Most errors in
the delayed-saccade task were early saccades due to anticipation,
whereas most errors in the transient condition were due to a lack of response.
The difference between eye movements to long-duration visual and
acoustic targets is illustrated in Fig.
1. Horizontal eye position signals (Fig.
1, A and B) and their corresponding velocities (Fig. 1, C and D) are plotted as a function of
time. These data are a subset from Fig. 4 in Populin and Yin
(1998), but here plotted synchronized to the end of fixation as
defined in the methods section.
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The initial segment of the eye movements was different in the two conditions. Visual trials (Fig. 1, A and C) were highly stereotyped: the eye started to move immediately in the direction of the target after the end of fixation with a high acceleration phase of uniform duration. In acoustic trials, on the other hand, the eye started to move in the direction of the target with a slow velocity ramp of irregular duration that preceded the fast saccadic component of the response (Fig. 1D). The presence of the slow velocity ramp in acoustic trials is illustrated more clearly in the insets of Fig. 1, C and D, which show magnified views of the velocity traces. Thus in visual trials the saccade coincides with the end of fixation criterion, but in acoustic trials it is preceded by a slow velocity ramp.
Saccade onset
The presence of the slow component in the initial part of the response to long-duration acoustic targets led us to seek an additional criterion that could objectively distinguish between the end of fixation and saccade onset in those eye movements with the slow velocity ramp. When applied to visual trials, which appeared to lack the slow ramp, the new criterion should mark saccade onset nearly coincident with the end of fixation. The irregular profile and the variable duration of the slow velocity ramp (Fig. 1D) precluded us from using a criterion based on a predetermined velocity threshold.
Empirically we determined that the first and fourth prominent peaks in
the fourth derivative of position could be used as markers for the
onset and offset of a saccadic eye movement. Figure 2 compares this criterion to the end of
fixation applied to both visual (top) and acoustic
(bottom) trials. Both examples are saccades from the primary
position to targets located at (18°,0°). If we define the start
and the end of the saccade as the time of the first and fourth
prominent peaks, respectively, in the fourth derivative (vertical
dashed lines), then in the visual trial (Fig. 2, top) the
end of fixation (vertical dotted line) and the saccade onset (vertical
dashed line) occur nearly simultaneously, although saccade offset and
the return to fixation do not. In the acoustic trial, on the other
hand, saccade onset occurred almost 100 ms after the end of fixation
(Fig. 2, bottom). Thus in this visual trial saccade onset is
essentially equivalent to the end of fixation, and we used it as an
objective criterion for marking saccade onset in both visual and
auditory trials.
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Duration of the slow velocity ramp
We defined the duration of the slow component as the time elapsed
between the end of fixation and saccade onset. Representative distributions of this measure for acoustic and visual trials to horizontal and vertical targets are illustrated in Fig.
3. In all five cats studied, the
distributions of the duration of the slow component from visual trials
are narrow (Fig. 3) with a mean near zero (Table
1), although the vertical trials had a
broader distribution and correspondingly larger means, especially for cat 09, which confirms that for visual targets there was
essentially no slow component. On the contrary, the distributions from
acoustic trials to both horizontal and vertical targets are broader
(Fig, 3) and have significantly larger positive means and larger
standard deviations (2-tailed t-test, P < 0.01) (Snedecor and Cochran 1980), reflecting the
presence of the slow velocity ramp. Thus saccades to acoustic targets
are preceded by a slow velocity ramp that is generally not present in
saccades to visual targets.
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Saccade dynamics
Having established the presence of a slow eye movement before saccades to noise stimuli in the standard-saccade task, we tested whether the saccadic components of the responses to visual and acoustic stimuli are different. Figure 4 illustrates the same velocity data plotted in Fig. 1, but synchronized to saccade onset, which effectively removes the slow velocity ramp. The traces corresponding to the visual trials remain essentially unchanged (cf. Figs. 1C and 4A), but those from acoustic trials are now better aligned in time showing a more typical saccadic profile (cf. Figs. 1D and 4B). Thus the velocity profiles of eye movements to visual and acoustic targets, when synchronized to saccade onset, are now very similar. The maximal velocity of the saccades to the acoustic target is smaller due to the smaller amplitude of the undershooting movements to acoustic targets.
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To assess quantitatively whether the saccadic component of eye
movements to long-duration acoustic targets is similar to saccades to
visual targets, we compared the slopes of the main sequences, i.e., the
relationship between peak saccade velocity and amplitude. Because of
the symmetry of the data, the main sequences from leftward and
rightward saccades (Fig. 5, A
and B), as well as upward and downward (Fig. 5, C
and D), were collapsed and plotted with a positive slope.
The results were consistent across all five subjects studied (Table
2): the slopes of the regression lines
fitted to the main sequence of saccades to acoustic and visual targets were not significantly different for horizontal or vertical targets (P > 0.05; test for significance of the difference
between independent s) (Cohen and Cohen 1975
) in any
cat.
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Although there were no significant differences between the slopes
of main sequences of upward and downward saccades, there was
nonetheless a trend for shallower slopes in downward saccades. This
trend is consistent with the presence of a prolonged deceleration in
downward eye movements, a "dynamic undershoot" as defined by Bahill et al. (1975). This dynamic undershoot is
illustrated in Fig. 6, which shows the
velocity of leftward eye movements to a target at (
18°, 0°)
( · · · ) and downward eye movements to a target
at (0°,
23°) (
), all plotted synchronized to the point of
maximal velocity. Notice that while the eyes stopped moving horizontally within ~100 ms after peak velocity, the eyes continued to move vertically >100 ms after peak velocity. In all subjects, downward eye movements displayed a deceleration tail that was significantly longer than that observed in horizontal eye movements (P < 0.05).
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Effects of time of exposure to the target before behavioral response
In the data presented in the preceding text, the cat was expected to make a saccade to the location of a long-duration visual or acoustic target, the presentation of which coincided with the offset of the fixation LED. To examine the effects of time of exposure to the target on the kinematics of the responses, we used both longer and shorter exposure times. Longer times were achieved using the delayed-saccade task, which forced the cat to listen to the stimulus for the duration of the delay before allowing a response. Shorter times were implemented using the standard-saccade task with transient stimuli, which were much shorter than the saccade reaction time and, therefore, required the cat to respond from memory.
EYE MOVEMENTS IN THE DELAYED-SACCADE TASK. In this condition, the offset of the fixation light, which was the signal for the cat to respond, occurred 300-700 ms after target onset; different delays were used to prevent the cats from anticipating. The velocity profiles of delayed saccades from the 500-ms delay condition from cat 06 are presented in Fig. 7A with corresponding distributions of the duration of slow component in Fig. 7B. Similar results were obtained from cat 15. The longer exposure to the targets affected the kinematics of eye movements to acoustic but not visual targets. Inspection of these velocity data reveals that eye movements to long duration acoustic targets in the delayed-saccade task are much more similar to eye movements directed to visual targets (Fig. 1C) than those directed to identical broadband noise targets in the standard-saccade task (Fig. 1D). Although the slow velocity ramp was still present (Fig. 7B), its duration was shorter than in the standard-saccade task (Fig. 3A). The slopes of the regression lines fit to the main sequences from delayed saccades to acoustic and visual targets (Table 2) were not significantly different from those obtained from standard saccades for each stimulus condition and each subject separately (P > 0.05).
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EYE MOVEMENTS TO TRANSIENT STIMULI.
We found that shortening the time of exposure to the acoustic target,
which requires the cat to respond to the target from memory,
essentially abolished the slow velocity ramp. Figure 7C shows the velocity profile of cat 06's eye movements to a
single 100-µs click target located at (18°, 0°). Clearly, the
initial stage of these movements does not show the slow velocity ramp that characterizes eye movements to long-duration broadband noise targets. Instead they are similar to saccadic eye movements to visual
targets, as corroborated by the lack of significant differences (P > 0.5) between the distributions plotted in Fig.
7D. The slopes of the main sequences computed from standard
saccades to acoustic and visual transient stimuli were similar, and
they were also similar to those computed from standard saccades to
long-duration targets (Table 2). Comparable results were obtained from
cat 15.
Summary
A summary of the duration of the slow velocity ramp for horizontal eye movements measured in the various experimental conditions from two subjects (cats 06 and 15) is shown in Fig. 8. The mean duration of the velocity ramp was negligible for visual targets in the standard- and delayed-saccade tasks. In acoustic trials, on the other hand, the duration of the slow velocity ramp changed systematically across the three different conditions studied. For both cats, there was an orderly reduction in the mean duration of the velocity ramp from the long-duration stimuli to the transient stimuli, with intermediate duration recorded in delayed saccades. In both cats, all conditions were significantly different, except that for cat 06 the duration for transients was shorter than for delay-saccades but did not reach significance.
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DISCUSSION |
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Methodological considerations: saccade onset criterion
Central to the thesis of this paper is the accurate detection of
saccadic eye movement onset. In visual trials, this was straight forward because the eye movements of our cats showed the typical abrupt
onset that characterizes saccadic eye movements in various species
(Becker and Fuchs 1969; Evinger and Fuchs
1978
; Fuchs 1967
). In acoustic trials, however,
saccadic eye movements were preceded by a slow velocity ramp of
variable duration (Fig. 1) so that the onset of the saccadic component
was delayed. A common criterion used to mark the onset of saccades is
to use some minimum velocity threshold, e.g., Waitzman et al.
(1991)
. However, we found this unsatisfactory because the
different slopes and durations of the slow velocity ramp led to
underestimates of saccade onset in some trials and overestimates in
others and because velocity thresholds that were high enough to
accommodate all acoustic trials did not coincide with saccade onset in
visual trials as selected by the end-of-fixation criterion.
Empirically, we found that the first prominent peak of the fourth
derivative of position was a reliable measure of saccade start for it
produced results consistent with those of the end of fixation criterion
in visual trials (Figs. 3 and 8).
Slow component
The present results show that saccadic eye movements of cats to long-duration broadband noise targets, unlike those to similar visual targets, are preceded by a slow velocity ramp of variable duration. This eye movement is unlikely to be an artifact of our recording system or the result of damage to the eye during surgery because it was not observed in eye movements to visual targets. To our knowledge, this type of eye movement has not been described in the literature.
In the delayed-saccade task, the cat was compelled to listen to the acoustic stimulus for an additional period before responding. This resulted in slow components of much shorter duration than in the standard-saccade condition (Figs. 3, 7, and 8).
The systematic changes in slow component duration observed across the acoustic conditions lead us to hypothesize that its presence in the standard-saccade condition to long-duration signals is due to uncertainty about the actual position of the target. It appears as if the cats were able to determine the general location but not the actual position of the acoustic target at the time of end of fixation. Thus they began to move their eyes slowly in the general direction of the target while waiting for additional information about its actual location and made a saccade only after the uncertainty was resolved.
The lack of a slow component before saccades to transient acoustic targets (Fig. 7) also appears to support our hypothesis. In the transient stimulus condition the 100-µs target expired well before the end of fixation, so that there was no additional information to be gained by waiting to make a saccade.
Anticipatory eye movements, qualitatively similar to the slow component
we report here, to visual, but not acoustic, targets have been
previously reported in human subjects: before smooth pursuit
(Becker and Fuchs 1985; Boman and Hotson
1988
; Kowler and Steinman 1979a
) and saccadic
eye movements (Kowler and Steinman 1979b
;
Moschner et al. 1996
) to visual targets moved in a
predictable direction. Eye movements of this type have been attributed
to the subject's expectations for the target to move. Because the acoustic targets used in our experiments did not provide a retinal signal nor could our subjects predict the position of upcoming targets,
the mechanisms underlying these anticipatory eye movements to visual
and acoustic targets are likely to be different.
Saccade dynamics
When the target for a saccade is nonvisual, the dynamics of the
movement are reported to be different, although there is no unanimity.
Slower peak velocities have been observed in human (Engelken and
Stevens 1989; Zahn et al. 1978
;
Zambarbieri et al. 1982
) and monkey (Russo and
Bruce 1994
) saccades to acoustic targets. Whittington et
al. (1981)
, on the other hand, reported no differences in the
kinematics of saccadic eye movements to visual and acoustic targets in
monkeys trained to localize sound. The limited description of the
methods and the lack of representative kinematic data in both
Russo and Bruce (1994)
and Whittington et al.
(1981)
make it difficult to evaluate their results.
The similarity of the slopes of the regression lines fitted to the main sequences of saccades to horizontal and vertical acoustic and visual targets in all five subjects suggests that the saccade burst generator was engaged in a similar manner regardless of the type of target. The different levels of experience of our subjects, which included a novice cat (cat 09), suggests that practice did not play a role in shaping the dynamics of the saccades.
The slopes of the regression lines fit to the main sequence of both
horizontal and vertical saccades were slightly steeper than those
reported by Evinger and Fuchs (1978) for two subjects: 13.5 and 9.0°/s/° for horizontal movements, and 14.1 and
17.6°/s/° for vertical movements. Differences in the experimental
procedures could account for the steeper main sequences obtained in the
present study. Such differences may be subtle and thus difficult to
relate to the data. For instance, Evinger and Fuchs
(1978)
presented a tone that sounded continuously when the eyes
of the cat were within 2° of the target.
Most models of the oculomotor system propose that saccades are executed
by the discharge of burst neurons, which carry the desired velocity
information of the impending saccade (Fuchs et al. 1985;
Robinson 1975
). The velocity, or pulse, then is
integrated by a neural circuit to derive the position, or step, signal
of the saccade. Both the pulse and step then are sent to the oculomotor plant to generate the saccade. The slow eye movement preceding saccades
to acoustic targets is novel, and in this model could be generated by a
small ramp velocity signal to the burst neurons.
Last, the differences in dynamics observed between downward and upward
eye movements are consistent with the results of
André-Deshays and Ron (1992) and Collewijn
et al. (1988)
in humans under both head-fixed and -free
conditions. The origin of the differences is unknown, but asymmetries
in the head-neck musculoskeletal system have been suggested as the
potential source (André-Deshays and Ron 1992
).
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ACKNOWLEDGMENTS |
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We thank R. Kochhar for help in designing and implementing the analysis software used for this work, D. J. Kistler for help with statistics, and A. F. Fuchs and D. A. Robinson for reading an earlier version of this manuscript.
This work was supported by National Institute of Deafness and Other Communication Disorders Grants DC-00116 and DC-02840 to T.C.T. Yin.
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FOOTNOTES |
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Address for reprint requests: L. C. Populin, Dept. of Anatomy, University of Wisconsin, 1300 University Ave., Madison, WI 53706.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 11 December 1998; accepted in final form 10 May 1999.
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REFERENCES |
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