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The Journal of Neuroscience, September 15, 1998, 18(18):7519-7534
Modulation of Neuronal Activity in Superior Colliculus by Changes
in Target Probability
Michele A.
Basso and
Robert H.
Wurtz
Laboratory of Sensorimotor Research, National Eye Institute,
Bethesda, Maryland 20892
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ABSTRACT |
Complex visual scenes require that a target for an impending
saccadic eye movement be selected from a larger number of possible targets. We investigated whether changing the probability that a visual
stimulus would be selected as the target for a saccade altered activity
of monkey superior colliculus (SC) neurons in two experiments. First,
we changed the number of possible targets on each trial. Second, we
kept the visual display constant and presented a single saccade target
repeatedly so that target probability was established over time.
Buildup neurons in the SC, those with delay period activity, showed a
consistent reduction in activity as the probability of the saccade
decreased, independent of the visual stimulus configuration. Other SC
neurons, fixation and burst, were largely unaffected by the changes in
saccade target probability. Because we had monkeys making saccades to
many locations within the visual field, we could examine activity
associated with saccades outside of the movement field of neurons. We
found the activity of buildup neurons to be similar across the SC,
before the target was identified, and reduced when the number of
possible targets increased. The results of our experiments are
consistent with a role for this activity in establishing a motor set.
We found, consistent with this interpretation, that the activity of
these neurons was predictive of the latency of a saccadic eye movement
and not other saccade parameters such as end point or peak
velocity.
Key words:
monkey; saccade; motor set; target selection; decision; buildup neurons
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INTRODUCTION |
Saccadic eye movements rapidly shift
the line of sight from one region of the visual field to another,
typically to direct the fovea toward objects of interest. Experiments
probing the neurophysiology of visually guided saccades traditionally
involved brief presentations of visual stimuli cueing when and where a saccade should be made. Combining these tasks with single neuron recordings identified many areas with neuronal activity linked to the
visual stimulus presentation as well as to saccade generation. More
recently, tasks in which delays are imposed between the visual stimulus
and the saccade reveal that neurons in many areas of the brain related
to saccades also have activity in the delay period (for summaries, see
Hikosaka and Wurtz, 1989 ; Andersen et al., 1997; Schall, 1997). In
cortical skeletal motor areas, the delay period activity is frequently
interpreted as reflecting aspects of motor set, a behavioral state
related to the preparedness to make a particular movement (Evarts et
al., 1984). Motor set may in turn consist of events including
attention, target and response selection, and movement preparation
(Wise, 1985).
Delay period activity is prominent in many superior colliculus (SC)
neurons, a critical structure relaying cortical signals to the
brainstem. Previous experiments identified at least three aspects of
motor set reflected by the delay activity of SC intermediate layer
neurons that discharge before saccades. First, Glimcher and Sparks
(1992) recorded from neurons they referred to as prelude burst neurons
and concluded that the long lead activity represented the selection of
a saccade, required information about the metrics of the impending
saccade, but was not involved in the initiation of the saccade per se
(see also Glimcher and Sparks, 1993). Second, Kustov and Robinson
(1996) showed that buildup neurons, which also have a long lead
activity, also increased their activity after the target was
identified, and they suggested this increase was related to attention
(see also Kojima et al., 1996). Third, Munoz and Wurtz (1995) found
that the buildup neurons changed their long lead activity before one of
two targets was identified and suggested that the activity reflected
saccade preparation. Most recently, Basso and Wurtz (1997) demonstrated
that the activity before a saccade target was identified was greatly
reduced if multiple possible saccade targets were presented.
Specifically, if the monkeys could be certain about which saccade was
to be made, the delay activity was high; if not, the activity was much reduced.
Our recent findings are consistent with interpreting the delay period
activity of SC buildup neurons as related to motor set, but a number of
key questions remain that we address in the present report. We reported
previously only changes in activity for saccades to targets in the
movement field of the neurons, but because saccades were made to
targets located adjacent and opposite the movement field in our task,
we could compare the magnitude of activity associated with saccades
throughout the visual field. We found that the delay period activity
was similar across the SC until the saccade target was identified and
that this activity was then systematically reduced as the number of
possible targets increased. Examination of the activity of other SC
neuronal elements, the fixation and burst neurons, showed that their
activity was relatively unaffected by changes in target probability.
Finally, because we hypothesized that the change in neuronal activity
was related to a change in motor set, we predicted that a change in
neuronal activity should be accompanied by a concomitant change in
saccade latency. Thus, we compared changes in saccade latency with the activity of buildup neurons and found that significantly shorter saccadic latencies occurred during periods in which there was significantly higher buildup neuron activity.
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MATERIALS AND METHODS |
Physiological procedures. Two monkeys were prepared
for chronic electrophysiological recording of single neurons and eye
movements. Anesthesia was induced initially with an intramuscular
injection of Ketamine (10.0 mg/kg), valium (1.0 mg/kg), and
glycopyrrolate (0.01 mg/kg). Monkeys were intubated and maintained at a
general anesthetic level with isofluorane. A subconjunctival eye coil was implanted (Judge et al., 1980). A plastic head holder for restraint
and a chamber for microelectrode recording were secured to the top of
the exposed skull with titanium screws and dental acrylic. This
hardware allowed subsequent magnetic resonance images to be obtained.
The 20 mm trephine hole and overlying recording chamber were placed
stereotaxically on the midline and angled 38° back so that the
electrode penetrations were directed caudorostral, toward the SC. At
the end of surgery and 1 d after surgery, animals were given
Banamine at 2.0 mg/kg for analgesia. An antibiotic (polyflex) was given
1 d before surgery and every other day for 14 d after
surgery. Monkeys recovered for 1 week before behavioral and
physiological recording commenced. All protocols were approved by the
Institute Animal Care and Use Committee and complied with the Public
Health Service policy on the humane care and use of laboratory
animals.
Single neurons were recorded with tungsten microelectrodes (Frederick
Haer) with impedances between 0.7 and 1.5 M measured at 1 kHz.
Electrodes were aimed toward the SC through stainless steel guide tubes
held in place by a delrin grid that was secured to the recording
chamber (Crist et al., 1988). Action potential waveforms from
individual neurons were identified with a window discriminator that
returned a pulse for each waveform that met both time and amplitude
criteria. The time of occurrence of each action potential was stored
with 1 msec resolution.
Behavioral procedures. All behavioral paradigms and the
storage of data were presented and acquired on a 486 personal computer running a QNX-based real time experimentation data acquisition system (REX) (Hays et al., 1982). During experiments, monkeys were seated in an adjustable primate chair facing a tangent screen with
their head restrained for the duration of the experiment (3-5 hr). The
visual display on the screen was rear projected by a television (TV)
projector onto a tangent screen that was located 57 cm in front of the
monkeys. An additional light-emitting diode used for a centrally
located fixation point was controlled by a computer that drove
x-y mirror galvanometers (General Scanning). Eye
movements were recorded using the magnetic search coil technique (Fuchs
and Robinson, 1966), and horizontal and vertical eye position signals
were sampled at 1 kHz. An interactive computer program was used to
calculate saccade metrics, dynamics, and latencies. Saccades were
detected using velocity (10-25°/sec) and acceleration (500-800°/sec2) criteria.
Two TV projectors were used, an Electrohome ECP 4000 that used
three cathode ray tubes to project the image and a Sharp 850 that
projected an image using a liquid crystal display. Both were running at
60 Hz frame rates. The projector was synchronized to our computer by
the vertical retrace signal; however, in the liquid crystal display
projector, there was a phase lag in the onset of the projected image
that varied between 0 and 16 msec. There was also a fixed delay of 4 msec. The sum of the mean phase lag and the fixed delay resulted in a
mean stimulus onset delay of 12 msec. Because we were not measuring or
reporting visual latencies, and because the time periods over which we
counted neuronal activity were at least 150 msec long and started in
relation to the earliest time of image onset, this variability did not
affect our quantification. We confirmed this by recomputing some
intervals (see Fig. 4) using the burst onset times determined by a
Poisson algorithm (Hanes et al., 1995). Saccadic latencies were
measured from the offset of the fixation point (light-emitting diode)
and so were unaffected by delays in the TV display.
Neurons were initially studied while monkeys performed a memory-guided
saccade task (Hikosaka and Wurtz, 1983). In this task, a centrally
located fixation point appeared, and the monkeys were required to
maintain fixation of this spot within an electronic window of 2°. A
peripherally located spot was presented for 200 msec while the monkeys
maintained fixation. After a delay of 200-800 msec, the fixation point
was removed, and the monkeys made a saccade to the location of the
previously flashed target spot. We determined the general
characteristics of the neuronal activity and an estimate of the center
of the movement field by requiring monkeys to make saccades to
different locations in the visual field. During all experiments,
monkeys were rewarded with a drop of fruit juice or water. Monkeys
worked daily until satiated and were given supplemental fluid as
required. The monkeys' weight was monitored daily, and they remained
under the supervision of the institute veterinarian.
Target probability tasks. Two tasks were used to determine
the effect of target probability on the activity of SC neuronal activity, a multi-target task and a blocked-mixed task.
In the multi-target task (Fig.
1A), our goal was to
separate the sequence of events leading up to saccade generation, while varying the probability that a given stimulus would become a saccade target. First, a centrally located fixation point (light-emitting diode) came on, and the monkeys were required to look at it for 1 sec
to initiate the trial. Second, one, two, four, or eight spots of light
came on (TV projector) for a randomized time ranging from 800-1200
msec, and these trial types were randomly interleaved. This was the
period of pre-selection because which of the spots would become the
target was unknown to the monkeys. One of these possible targets was
always located at the position in the visual field that yielded the
maximal saccade-related activity of the neuron. All other possible
targets were placed equally eccentric but in different directions (in
the four cardinal and four oblique directions). The eccentricities
ranged from 3 to 25°, with most being ~10°. Third, one of the
possible targets dimmed for 800-1200 msec. This was the period of
selection because the dimming indicated which of the spots was the
target for the saccade. The final period of saccade initiation began
when the fixation point went off (go signal), which required the
monkeys to make a saccade within 500 msec to the dimmed target. Monkeys
were required to maintain their eye position at the target for 300-500
msec to obtain liquid reward. The task had a clear target change so
that it was essentially a pop-out task (Bravo and Nakayama, 1992),
requiring only target detection and not discrimination (Treisman and
Gelade, 1980).
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Figure 1.
A, Multi-target task. Along
the top, the bars labeled "fixation,"
"array on," and "target dim" depict the temporal sequence of
the multi-target task. The line below labeled "Eye"
is a schematic of a representative eye position trace in
this task. The lower portion of the figure depicts the spatial
arrangement of the trial types. The large boxes are a schematic of the tangent screen. The
cross represents the fixation point, and the surrounding
box represents the criterion window for the monkeys to
maintain eye position for correct task performance. Each of these trial
types was randomly interleaved. As the number of possible targets
(filled circles) increased, the probability that
any one of them would be identified as the saccade target decreased.
The fixation period began with the onset of a fixation point, followed
by the pre-selection period when the array of possible stimuli came on.
The selection period was the time when the target dimmed, and the
initiation period was the time when the monkeys were given a cue to
initiate the saccade, in this case, when the fixation point was
removed. The temporal separation of events allowed the neuronal
activity associated with each event to be dissociated.
B, The blocked-mixed task. Along the top,
the labeled bars indicate the temporal sequence of
events in the task. Mixed target trials were those in which the saccade
target was selected randomly on each trial from the eight stimuli. The
blocked target trials were those in which the saccade target was always
the one located in the movement field of the recorded neuron. Note that
the time the target dimmed and the time the fixation point was removed
occurred simultaneously, allowing the saccade to be initiated as soon
as the target was selected.
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In the first 32 neurons studied, we used a version of the task that had
periods randomized among 200 and 400 msec rather than the longer
800-1200 msec periods and included only two, four, or eight possible
targets. For most of these neurons, the single-target condition was
performed separately in blocks. Qualitatively, there were no
differences between the behavior of the neurons in the versions of the
task with the short or long periods, but because of the different
times, we analyzed the data separately.
The multi-target task provided an overt change in target probability by
varying the number of possible targets, but the change in number also
changed the visual stimulus to which a neuron was exposed. Therefore,
we designed a second task, the blocked-mixed task, to change the target
probability while keeping the visual display constant. In this task, we
recorded 32 additional neurons, and for 19 of these, we also recorded
them in the multi-target task.
In the blocked-mixed task (Fig. 1B), the acquisition
of the fixation point initiated a trial, and then the same array of
eight visual stimuli appeared. In separate sets of trials, either the same stimulus repeatedly dimmed to indicate that it was the target on
every trial (blocked target trials, maximum probability), or any one of
the eight possible targets dimmed, indicating it was the saccade target
(mixed target trials, minimum probability). This task had an advantage
over the multi-target task because the visual display was identical in
both the mixed and blocked conditions. The only variable that changed
was the probability that the movement field stimulus would serve as the
saccade target. Moreover, the change in probability was based on
experience with the preceding trials. We modified the timing of this
task slightly from the multi-target task in that the go signal and the
identification of the target occurred simultaneously. In this way, we
could measure the latency of the saccade as soon as monkeys selected
the target and initiated the saccade.
Neuronal classification. To compare the effect of the
multi-target task across neurons with similar responses, we classified them as buildup, burst, or fixation neurons. Buildup neurons had a
significant delay period activity between the stimulus onset and the
saccade initiation. We classified a neuron as buildup if there was a
significant difference in activity between a baseline interval
(100-200 msec before the target appeared) and the interval before the
signal to make the saccade [100-200 msec before the fixation point
was removed (see Dorris et al., 1997)]. A significant difference
(Wilcoxon signed-rank test, p < 0.05) was required in
either the single target condition of our task (visually guided saccade) or in the task we used to determine neuronal characteristics (memory-guided saccade task). We also required that neurons discharge at least 30 spikes/sec in the 100 msec interval before the
saccade (Munoz and Wurtz, 1995). Neurons that failed to reach these two criteria were classified as burst neurons. For all but three neurons, the significance criterion alone was sufficient. Neurons that paused
for saccades of at least 10° amplitude were classified as
fixation neurons (Munoz and Wurtz, 1993).
Data analysis. In addition to standard descriptive
statistics, we used two nonparametric statistical procedures. When we
compared more than two levels of a variable, we used ANOVA. When
we compared only two levels of a variable, we used the Wilcoxon
signed-rank test. For multiple group comparisons, such as those in the
multi-target task, we used the Friedman one-way, repeated-measures
ANOVA with Dunnett's method for post hoc pairwise
comparisons. We compared the mean level of discharge for the neurons in
the one, two, four, and eight possible target conditions. We did this
separately for successive time intervals in the task. For example, to
analyze the visual response of neurons in the task, we performed a
one-way ANOVA with four levels, namely, one possible target condition, two possible target condition, four possible target condition, and
eight possible target condition. When a main effect was obtained, we
performed the pairwise comparisons using Dunnett's method to determine
which pair contributed to the significant difference. For those
analyses consisting of only two groups, such as those in the
blocked-mixed task, we performed the Wilcoxon signed-rank test. For
example, using the visual response data from the blocked- and
mixed-target conditions, the Wilcoxon signed-rank test compared the
difference in the activity in these two conditions.
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RESULTS |
We recorded from 141 SC neurons and classified each as a buildup,
burst, or fixation neuron (see Materials and Methods). After classification using the memory-guided saccade task and the
single-target saccade task, we estimated the center of the movement
field by on-line identification of the saccade direction and amplitude that yielded maximal activity from each neuron. We tested a subset of
the neurons on the multi-target task and a subset on the blocked-mixed task.
Multi-target task: buildup neurons
Movement field target
Buildup neurons (n = 72) had a significant delay
period activity and frequently a burst of action potentials associated
with the preferred saccade. When presented with a single possible
saccadic target in the movement field contralateral to the SC in which the neuron was recorded, buildup neurons frequently had an initial phasic response (Fig.
2A, pre-selection).
This was followed by delay period activity that was maintained through
the time when the stimulus dimmed (Fig. 2A,
selection) and until the fixation point was removed indicating that the
saccade should be made. Then, a burst of action potentials preceded the
saccade into the movement field (Fig. 2A, right
column).
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Figure 2.
Decreased target probability reduced buildup
neuron activity. The events of the task are indicated by the labeled
periods across the top, and the spatial arrangement is
indicated by the schematic of the tangent screen as drawn in Figure 1.
The eye position trace is a schematic. This example is
from trials when the stimulus that fell in the movement field of the
neuron was identified as the target. The left column
shows rasters and the average spike density function for five trials
during the pre-selection period when one (A), two
(B), four (C), or eight
(D) possible targets were presented. The
arrowheads and the vertical dashed lines
indicate the alignment of the traces. The left
column is aligned on the onset of the possible targets, and the
middle column is aligned on the beginning of the
selection period, when one of the stimuli dimmed. Both the initial
visual and the delay period responses decreased as the number of
stimuli increased. Activity increased after the stimulus in the
movement field dimmed, indicating it was the target (dashed
vertical line in the middle column). The
right column is aligned on the onset of the saccade, the
initiation period. This neuron had a burst of action potentials
associated with the onset of the saccade that did not differ between
the probability conditions.
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When the number of targets increased, and hence the target probability
decreased, the level of activity in the buildup neuron decreased (Fig.
2B-D). For example, in the four possible target case, both the initial phasic response and the delay period activity in
the pre-selection period decreased compared with that in the one target
case (Fig. 2A,C, pre-selection).
After the stimulus in the movement field dimmed, indicating it was the
target, this neuron had an increase in activity (Fig. 2, selection)
that continued until the go signal was presented. This maintained level
of activity after the target dimmed varied little as the number of
stimuli increased. The saccade-related burst also did not differ in
amplitude between the one, two, four, or eight possible target
conditions (Fig. 2, right column).
The pattern of activity correlating with increasing the number of
possible targets was a decrease in the visual response and the delay
activity in the pre-selection period and no change in the selection and
saccade initiation periods. We saw this pattern of activity to varying
degrees in all 72 buildup neurons recorded even when the amount of
buildup activity varied. To demonstrate the consistency for the sample
of 40 buildup neurons recorded in the task with the long time periods
(800-1200 msec; see Materials and Methods), we averaged the 40 individual neuronal spike density functions in the successive task
periods (Fig. 3). A clear decline in the
visual response and the delay activity is evident as the number of
stimuli increased from one to eight. The sample also reflects the lack
of difference in activity after the target dimmed and at the time of
the saccade, as the number of stimuli increased. Note, however, that
the curves do not overlap until nearly 100 msec after the target is
identified (Fig. 3, vertical line), perhaps reflecting the change related to the time needed for target
selection.
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Figure 3.
The activity across the sample of buildup neurons
showed a reduction of activity with decreased target probability. The
traces show the mean spike density function of the 40 neurons for each target probability condition when the target was in
the center of the movement field of each neuron. The alignments are
identical to that in Figure 2. Black bars indicate a
statistically significant difference between the conditions for the
measurement intervals. Gray bars indicate no significant
difference. The visual interval was the first 150 msec after the
minimal visual latency of SC neurons of 50 msec (Goldberg and Wurtz,
1972a). The early pre-selection interval was 150 msec after the
visual interval. The late pre-selection interval was the 200 msec
before the target dimmed, and the early pre-selection interval
was the 200 msec after the target dimmed. The late selection interval
was the 100 msec before the fixation point was extinguished. The
initiation interval was the 100 msec before the saccade began.
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To compare the activity of the sample of 40 buildup neurons further, we
divided the three periods of the task into six intervals: visual, early
and late pre-selection, early and late selection, and initiation (see
Fig. 3 legend). The ANOVA comparing the neural activity in the
different intervals for the different target conditions across the
sample of 40 neurons revealed significant differences in activity, with
decreases in probability from one possible target to eight possible
targets. We found this for the visual response (p < 0.001), the early pre-selection activity
(p < 0.005), and the late pre-selection
activity (p < 0.001). Changes in the number of
possible targets did not alter the activity in the early selection (p = 0.98), the late selection
(p = 0.90), or the initiation
(p = 0.98) intervals. When we compared the
activity between the two and eight possible target conditions for the
32 neurons recorded in the version of the task with the short periods
(see Materials and Methods), the result was significant and mirrored
the result of the analysis of the data collected in the version of the
task with the long periods (visual, p < 0.001;
pre-selection, p < 0.001; selection, p = 0.06; and initiation, p = 0.52).
To determine whether individual stimulus conditions differed from one
another, we performed post hoc pairwise comparisons of the
data for the 40 neurons. In the pre-selection period, all target
probability conditions, one versus eight, two versus eight, and four
versus eight, differed significantly (p < 0.05). The same trend was found for the 32 neurons; two versus eight
and four versus eight differed significantly (p < 0.05). Because the single target condition was performed in separate
blocks for most of the neurons, those data were not included in the
analysis. We will concentrate further quantification on the data
collected in the version of the task with the long periods.
In sum, reduced levels of target probability reduced the activity of
buildup neurons only during the period of pre-selection, before the
availability of information about the target for selection by the
saccadic system. Neither the activity after the identification of the
target nor the activity associated with the initiation of the saccade
was affected by the change in the number of possible targets.
Pre-selection period activity
In some visual responses, such as those in Figure 2, there were
two phases. It is possible that these two phases of activity are
different kinds of responses and our relatively long 150 msec interval
obscured them. Also, they may be affected differently by the target
probability conditions. We tested to see whether these two phases were
different from each other and whether they had a differential
dependence on the number of possible targets. Because there was some
variability in the onset of the visual response across neurons, we
identified the burst onset using the Poisson spike train analysis
method developed by Hanes et al. (1995) for each individual neuron. We
divided the subsequent 150 msec visual interval into two intervals, a
first 50 msec after the burst onset that always included the initial
peak and a second 100 msec. We did this for each target condition. The
mean firing rate in the first 50 msec and the subsequent 100 msec both
decreased as the number of targets increased (Fig.
4). Both intervals were significantly
different in all of the target probability conditions (p < 0.01). The first 50 msec after the onset
of the burst was also consistently larger than the subsequent 100 msec
interval of activity, and an ANOVA revealed that the two components
were significantly different from one another in all of the target probability conditions (Fig. 4; p < 0.01). Thus,
although there seemed to be two phases of the initial visual response,
both were affected similarly by the changes in the number of possible
targets.
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Figure 4.
The average firing rate for the 40 neurons in each
of the four target probability conditions during the visual interval is
plotted. The visual interval was divided into two intervals, an initial
50 msec (black bars) and a later 100 msec
(gray bars). The initial 50 msec interval was
measured with respect to the onset of the burst for each individual
neuron using a Poisson burst detection algorithm (Hanes et al., 1995).
Both components of the initial response time locked to the onset of the
visual stimulus showed a decrement in activity with increased target
probability.
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Another issue is the cause of the mean decrease of activity in the
pre-selection period with increasing numbers of possible targets. There
are two possibilities. The first is that the neurons had a decreased
level of activity on every trial as the number of possible targets
increased, yielding a reduced mean level of activity. The consistent
reduction in activity as the number of possible targets increased (Fig.
2) is consistent with this alternative, as is our qualitative
evaluation of the response of other neurons. A second possibility,
however, is that with the increasing number of possible targets, the
monkeys shifted resources from one target on one trial to another
target on another trial. The mean would decrease because the amount of
activity on any given trial was less as the number of possible targets
increased.
These two possibilities can be quantitatively distinguished for the
sample of neurons by comparing the measures of dispersion in the
different target conditions. For example, in the eight possible target
condition if the activity is fluctuating between one and the other
seven trials and in the one possible target condition it is not, the
SDs should be very different. To examine this, we first
calculated the SDs for each possible target condition one to eight. To
compare across conditions, we normalized the SDs to z
scores. Using ANOVAs, we compared the z scores for the different target probability conditions and all measurement intervals. Confirming our qualitative impression, no significant differences were
obtained across the target probability conditions in any interval
(visual, p = 1.0; early pre-selection,
p = 0.99; late pre-selection, p = 0.72;
early selection, p = 0.58; late selection, p = 0.98; and initiation, p = 0.89).
Thus, the mean reduction in activity of buildup neurons with decreased
target probability results from decreases across all trials and not
from a sporadic trial-to-trial reduction.
Eight possible target condition
Up to this point we have described buildup neuron activity on
trials when the stimulus that became the target on that trial was in
the movement field of the neuron. For stimulus configurations with two,
four, or eight stimuli, monkeys also made saccades to all of the other
stimuli on trials in which they were the target. To examine the
activity of buildup neurons when saccade targets were located outside
of the movement field of the recorded neuron, we focused on the eight
possible target condition (Fig. 5). The phasic visual response that occurred during the pre-selection period
was identical regardless of which stimulus would later be randomly
identified as the target for the saccade (Fig. 5, leftmost
plot in each of the eight sets of plots).
Similarly, the buildup activity was the same during the rest of the
pre-selection period (Fig. 5, first
one-half of middle plots). It
was not until the target was identified that the activity dramatically
increased when the target was in the movement field (Fig. 5,
second one-half of the middle
plot, 0° target location) and frequently did not change
when the target was outside the movement field (Fig. 5, second
one-half of middle plots). And
finally, the burst of activity before a saccade depended on the
selection of the saccade target in the movement field of the neuron
(Fig. 5, rightmost plots, around the 0°
location).
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Figure 5.
Activity of a buildup neuron during the
presentation of all eight targets. Each trace in each of
the eight sets of three plots is aligned on the same
events described in the Figure 2 legend. The leftmost
plots are aligned on stimulus onset, the middle
plots are aligned on target dimming, and the rightmost
plots are aligned on saccade onset. Each set of three
plots is in the location where the target appeared on
the screen. The movement field is rotated so that the center is in the
0° location.
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For our sample of 40 neurons, we compared the selectivity of three
different intervals of activity. The three intervals we quantified
included the visual response, the activity around the time the target
dimmed, and the activity before the saccade for the different target
directions (Fig. 6). We computed a simple index for each interval. We calculated a visual index by taking the
difference between the visual response and the baseline and dividing it
by the sum of the two (Fig. 6A). Activity during the visual interval differed neither for the two individual neurons shown
nor across the sample for any of the target locations.
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Figure 6.
Selectivity indices for the sample of 40 buildup
neurons. Neural activity is plotted as a function of target direction.
The center of the movement field is normalized to the 0° location for
all the neurons. A, The visual index shows the neural
activity during the visual interval (150 msec after a visual latency of
50 msec) minus 200 msec of baseline neural activity (during the
fixation interval before the stimuli appeared) divided by the sum of
the two activities. B, The selection index is the neural
activity 400 msec after the target dimmed minus the neural activity 400 msec before the target dimmed divided by the sum of both activities.
C, The initiation index is the neural activity 100 msec
before the onset of the saccade (initiation interval) minus the 200 msec of baseline activity divided by the sum of the two activities.
Shown are the results from two example neurons ( and  ) as well as
the result for the mean ( ). The neuron indicated by the () shows
an inhibition of activity for adjacent targets after the target dimmed
as well as just before the saccade.
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We calculated a selectivity index around the time of presumed target
selection by taking the difference between the activity after the
target dimmed and the activity before the target dimmed and dividing it
by the sum of the two (Fig. 6B). Some neurons showed
a dramatic decrease in activity when a target adjacent to the one
centered on the movement field was identified for selection (Fig.
6B, ); others did not (Fig. 6B,
). Across the sample (Fig. 6B, ), there was
very little decline in activity for nontarget locations but rather an
increase at the target location.
We calculated a presaccadic neuronal activity index by taking the
difference between the baseline activity and the activity before the
saccade onset and dividing it by the sum of the two (Fig.
6C). Some neurons were tuned only for the target located at
the 0° location (Fig. 6C, ). Others had broader tuning
with activity before saccades made 45° in either direction from the center of the movement field (Fig. 6C, ). Moreover, the
activity of this neuron with broad tuning was inhibited by targets
located opposite the movement field. The activity of this neuron is
reminiscent of the flanking inhibition reported for the presaccadic
activity of frontal eye field neurons (Schall and Hanes, 1993; Schall
et al., 1995). Neurons with this broad tuning were the most common as
revealed by the mean directional tuning of the sample of 40 neurons
(Fig. 6C, ).
Thus, when we looked at the buildup activity related to all possible
targets, we saw a consistent pattern related to the demands of the
task. With eight possible targets, buildup neuron activity was present
but low, consistent with the reduced probability of a saccade into the
movement field. When the probability became high, when the target
dimmed, the activity increased. Although some neurons decreased
activity for targets outside of their movement fields, across the
sample, buildup neuron activity typically was maintained when targets
outside the movement field were indicated.
Contralateral and ipsilateral targets
Among the eight target positions used in each experiment, two are
particularly interesting. One is the target falling in the contralateral visual field (in the movement field of the neuron). The
second is the target in the ipsilateral field that is symmetrical, across the vertical meridian, to that in the movement field. Activity associated with saccades made to the symmetrically located target can
be used to infer what SC activity there is on the other side of the
brain. This inference is valid if we assume that the activity of
buildup neurons on the two sides of the SC is the same; that is, both
SCs are activated with saccades to their contralateral field (their
preferred direction) but not with saccades to their ipsilateral field
(their null direction). Thus, when a saccade is made in the preferred
direction of a neuron being recorded, the neurons in the other SC are
discharging with that same saccade in their null direction. We
therefore used the activity of neurons for trials in which the saccades
were away from the movement field as indicative of activity in the SC
we were not recording. This assumption is similar to that of
"anti-neurons" in other analyses, (eg., Britten et al., 1992;
Thompson et al., 1996). We compared this with the activity of the same
neuron before saccades made toward the movement field as the measure of
activity in the SC from which we were recording. We made these
comparisons for the two and eight target conditions. Doing so allowed
us to estimate the activity in the SC on both sides of the brain but
was limited to the two symmetrical locations.
Our comparison was made by plotting the mean and SE of the
firing rate across our sample of 40 neurons for all the trials either
toward the movement field or away from the movement field when two
stimuli were presented on each trial (Fig.
7A). During the pre-selection
period, the neuronal activity was the same regardless of which stimulus
would later become the target (Fig. 7A, pre-selection). This
indicated that the activity in the SC on both sides of the brain was
relatively high. At the time the target dimmed, the mean neuronal
activity increased for the SC neurons with the target in the movement
field. The mean activity remained largely unchanged for the neuron in
the other SC. Some individual neurons, however, did change after the
target dimmed (data not shown). A few (5/40) reduced activity
immediately when the stimulus opposite the movement field became the
target. Others (9/40) did not decline at all until after the saccade
ended. Most neurons (25/40) behaved somewhere in between the extremes,
not declining immediately after the identification of the target but,
rather, declining perisaccadically as indicated by the mean response.
Thus, the activity inferred to occur in the two sides of the SC was a
high level of activity throughout both SCs before target identification
and an increase at the time of target identification in the movement
field.
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Figure 7.
Comparison of neuronal activity related to a
target in the movement field and in the opposite visual field. The
plot shows the mean (black lines) and the
unidirectional SE (gray shading) of the neuronal
activity for the sample of 40 neurons. The arrangement and alignments
are the same as in Figure 3. A, The
traces from the two possible target condition trials in
which the stimulus in the movement field was identified as the saccade
target and in which the stimulus in the ipsilateral visual field was
the saccade target are superimposed. B, The same
conditions described in A apply except the trials are
from the eight possible target condition. The black bars
under the plots indicate statistically significant
differences in the intervals of activity between the movement field and
opposite target trials. The gray bars indicate a lack of
statistical significance. The horizontal dotted reference
line in A and B indicates the
mean activity in the late pre-selection interval in the two possible
target condition (27 sp/sec). The reference line shows
that the activity after the target dimmed in the movement field was
virtually identical in the two and eight possible target conditions and
that the neurons did not reduce their activity after the opposite
target was identified for selection.
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We saw the same sequence of changes when one of eight possible stimuli
became the saccade target, but with two prominent differences (Fig.
7B). First, in the pre-selection period, the activity was lower in both sides of the SC than when only two targets were present.
Second, after the target dimmed, the increase in activity was greater
for the neuron in whose movement field the target fell than was
the case with two targets. This was not because the peak activity after
the target dimmed was higher but, rather, because the activity before
the selection was lower (Fig. 7).
For the two possible target condition, the difference between the
activity when the target was in the movement field and that when the
target was opposite the movement field was not statistically significant in the visual (p = 0.75), early
pre-selection (p = 0.22), or late pre-selection
(p = 0.49) intervals (Fig. 7, gray bars). The visual (p = 0.11), early
pre-selection (p = 0.23), and late pre-selection
(p = 0.88) intervals in the eight possible target condition also failed to reach significance. Differences between
the neuronal activity for trials in the two possible target condition
were found for the early selection (p < 0.001),
late selection (p < 0.001), and initiation
(p < 0.001) intervals (Fig. 7, black
bars). Similarly, in the eight possible target condition, the intervals early selection (p < 0.001), late
selection (p < 0.001), and initiation
(p < 0.001) were significantly different.
In sum, this analysis revealed differences in the two SCs that were a
result of the probability of a given stimulus becoming the target for
the next saccade. Before the identification of the saccade target,
activity was lower in both SCs when there were many stimuli rather than
just a few. As a consequence of this difference, the change in activity
after the target was identified in the movement field was greater in
the SC when the target was identified from among many stimuli rather
than from among only a few.
Burst and fixation neurons
In contrast to buildup neurons, burst neurons had no significant
activity during the delay period of the memory or visually guided
saccade tasks but had a robust and discrete burst of action potentials
associated with the onset of the preferred saccade. We recorded from 12 burst neurons in the task with the long-time periods. We plotted the
mean spike density function for the sample of burst neurons in the
different target probability conditions and superimposed them (Fig.
8). To the extent that burst neurons had
some activity other than the presaccadic burst, that activity was
modulated by the change in target probability. For example, frequently
there was a phasic visual response to the stimulus onset that decreased
in the low probability condition (Fig. 8, pre-selection). Likewise,
there was a phasic response of some burst neurons after the target
dimmed that was reduced in the eight possible target condition (Fig. 8,
selection). There were no differences in the presaccadic burst across
probability conditions (Fig. 8, right column). Thus,
if burst neurons had activity in the pre-selection period, it was
decreased with decreased probability.
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Figure 8.
Burst neurons and saccade target probability.
A, The arrangement and alignment of this figure are the
same as in Figure 3. The mean spike density function of the 12 burst neurons in each target condition is plotted. Black
bars indicate a statistically significant difference between
the conditions for the different intervals. Gray bars
indicate no significant difference. The quantification intervals are
the same as in Figure 3.
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We quantified the activity of the burst neurons in the intervals of the
task. The visual interval activity was significantly different between
the target conditions (p < 0.001), as were all the pairwise comparisons of one versus eight (p < 0.05), two versus eight (p < 0.05), and four
versus eight (p < 0.05) target conditions. There was a statistically significant difference in the activity during
the late pre-selection interval (p < 0.001) and
for the early selection interval (p < 0.03).
Differences in activity in the other intervals failed to reach
significance (early pre-selection, p = 0.25; late
selection, p = 0.95). Like the saccade-related burst of
buildup neurons, the saccade-related burst of burst neurons did not
differ between the different possible target conditions (p = 0.67). Because burst neurons only had
activity for saccades made to their preferred location in the visual
field, the response (or lack thereof) when targets presented in the
opposite hemifield is not shown.
Fixation neurons in the rostral pole of the SC (n = 25)
showed discharge during fixation and paused for saccades of 10°
amplitude. In the 25 fixation neurons from which we recorded, there
were no statistically significant differences between the one and eight possible target conditions in any of the intervals (visual,
p = 0.67; early pre-selection, p = 0.16; late pre-selection, p = 0.65; early selection,
p = 0.06; late selection, p = 0.63; and initiation, p = 0.65; data not shown). This was true
for the trials in which either the target ipsilateral or contralateral
to the recording SC was identified as the target for the upcoming
saccade.
In 9 of the 25 fixation neurons, we tested whether they increased their
activity in a trial type that required the suppression of a saccadic
eye movement or maintenance of fixation. To do so, we modified our task
to include interleaved catch trials in the two, four, or eight possible
target conditions. In these trials, the fixation point rather than one
of the peripheral targets dimmed. This signal required the monkeys to
maintain fixation rather than prepare a saccade, and we reasoned that
this signal might be accompanied by an increase in fixation cell
activity. We found no significant differences between the activity
measured during the late pre-selection interval and the early selection
interval (two possible targets, p = 0.06; four possible
targets, p = 0.21; and eight possible targets,
p = 0.11), consistent with a lack of selectivity for the dimmed fixation point. We did not test the fixation neurons with
targets very close to the fixation point, which subsequent experiments
(Krauzlis et al., 1997) have shown modulates the activity of these
neurons.
Blocked-mixed target task: buildup neurons
We have described changes in the activity of SC neurons that
resulted from changing target probability overtly, by altering the
number of possible targets from which saccade selection occurred. However, this design also changed the visual stimulus configuration, which may have contributed to the change in neuronal activity. Therefore, we tested the effect of target probability by manipulating it covertly. We did not change the visual stimulus configuration but
rather changed the monkeys' trial-by-trial experience with the
identified target. In one condition of this experiment, there were
still eight possible targets, but only one of them dimmed on every
trial (blocked target trials). The probability that one stimulus would
be the target was 100%. In the other condition, we presented the
identical eight stimulus array, but any one of them could be the
target, yielding a probability of 12.5% (mixed target trials).
We recorded the activity of 32 buildup neurons in the blocked-mixed
task. As the monkey performed the mixed target trials in which any one
of the eight possible targets could be identified for selection, the
activity was low, consistent with the decreased probability (Fig.
9A, first row).
When the monkey performed the blocked target trials, in which one of
the eight possible targets was repeatedly the target in many trials,
the neuronal activity increased (Fig. 9A, second
row). As the number of trials with the same saccade target
increased, the activity of the neurons increased further. The increase
in activity is indicated by comparing the first and last 20 trials in a
series of 100 trials of the blocked target condition (Fig.
9A, third row). Similar activity changes have
been reported in premotor cortex neurons (di Pellegrino and Wise,
1993).
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Figure 9.
Comparison of the activity of buildup neurons in
the blocked-mixed task (A) and the multi-target
task (B). A, Comparison of the
neuronal activity in the mixed- (first row) and
blocked- (second two rows) target trials. The blocked
target trials are divided into the first and last set of 20 trials in a
series of 100 blocked trials. The spatial arrangement of this task is
depicted to the left of the rasters and spike density
functions. The effect of the changing target probability was evident in
the pre-selection period in both the multi-target task
(B) and the blocked-mixed task (A). Because in both tasks for the
recording of these neurons the target dim and the fixation point offset
occurred simultaneously, monkeys could initiate the saccade as soon as
the target dimmed. Therefore, after the target identification, there
remained some difference in activity between the blocked and mixed
conditions. The activity in the late pre-selection period between the
first 20/100 and the last 20/100 trials in the blocked condition
suggests a reflection of the learning of the saccade goal by the
monkeys. B, The neuronal activity in the multi-target
task with one possible target presented, shown by the first
row of rasters and spike density functions. The figure is
arranged the same as Figure 3. Note that for the experiments comparing
the multi-target and the blocked-mixed tasks, we modified the timing of
the multi-target task so that the fixation point offset and the target
dim occurred simultaneously, as they did in the blocked-mixed task. The
traces are aligned on the array onset
(first column), target dim and fixation point
offset (middle column), and the saccade onset
(last column). The vertical dashed lines
and the arrowheads at the bottom of the figure indicate
the alignment.
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For 19 of our 32 neurons, we were able to maintain isolation long
enough to also record the neurons while the monkeys performed the
multi-target task. In these cases, the target dim and the fixation
point removal also occurred simultaneously similar to that in the
blocked-mixed task, so we could make direct comparisons between the
activity in the two tasks. In the single target case, the neurons were
very active, consistent with the high probability (Fig. 9B,
first row). In the eight target case, buildup neurons decreased their activity relative to the single target case (Fig. 9B, second row).
For the sample of 32 neurons, we compared the activity in the blocked
and mixed trial conditions for the same intervals that we used
previously and again plotted the mean spike density function and
superimposed the means from the two conditions (Fig.
10). Because of the clear differences
between the first series and the last series of blocked target trials,
we plotted and analyzed the data only for the last five blocked target
trials and compared these with the mixed target trials (Fig.
10A). The average firing rate of the sample of
buildup neurons was greater in the last five blocked target trials than
in the mixed target trials. Using the same measurement intervals used
previously in the multi-target task, we quantified the difference in
the two conditions. The differences between the last five blocked
target trials and the mixed target trials were statistically
significant for all pre-selection intervals (visual, p < 0.001; early pre-selection, p < 0.001; and late
preselection, p < 0.001). The
early selection interval was also significantly different (early
selection, p < 0.001), in contrast to the result in
this interval of the multi-target task. We think the significance in
the early selection interval results from the temporal overlap of the
selection and initiation periods in the blocked-mixed task, making the
trials in this task shorter than those in the multi-target task. The
initiation interval failed to reach statistical significance
(initiation, p = 0.54).
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Figure 10.
Comparison of the activity of the buildup neurons
in the blocked-mixed task conditions. A, The mean spike
density function for each of the 32 neurons is plotted in each
condition for the mixed target trials (dotted line) and
the last five blocked target trials (solid line).
B, The mean spike density function for each of the 32 neurons is plotted for the first five trials (dotted
line) and the last five trials (solid line) in
the blocked condition. Consistent with the change in the saccade
latency, the activity of neurons was greater as the monkeys repeated
the same saccade on every trial.
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We also compared the differences between the first and last five
blocked target trials in our sample of 32 neurons (Fig.
10B). Again, the activity of the sample of neurons
was higher later in the series of blocked target trials compared with
that in the initial series of blocked target trials. There were no
statistically significant differences between the first and last five
blocked target trials in the visual interval (p = 0.97) or the early pre-selection interval (p = 0.55). However, during the late pre-selection interval, there was a
statistically significant difference in activity between the first and
last five trials of the blocked trial condition (p < 0.01), as was the early selection response
(p < 0.01) consistent with the increase in
saccade target probability. Interestingly, for the initiation interval,
the neuronal activity was larger in the first five blocked target
trials (median, 127.0 sp/sec) than in the last five blocked target
trials (median, 110.0 sp/sec). The difference was statistically
significant (p < 0.01) and is evident in the
slightly higher rise of the saccade-related burst for the first five
trials (Fig. 10B, dotted line).
Changes in the saccade-related activity have been reported previously
for visuomotor neurons in the SC when monkeys repeatedly made the same
saccade (Ottes et al., 1987).
Thus, buildup neurons showed a decreased level of activity as the
probability of a particular stimulus becoming a saccade target
decreased. The change in activity was present whether the saccade
target probability was manipulated overtly with changes in the number
of possible stimuli or covertly by changing the past experience of the
monkeys with a particular saccade target.
Saccade latency and metrics
In the blocked-mixed task, it is only an inference that the
monkeys are actually using the probability information in the task. A
simple way to assess the validity of this inference is to measure
saccade latency. The prediction generated by a motor set hypothesis is
that when the saccade target is highly probable, saccadic latency is
shorter. Recall that the multi-target task was a simple reaction time
task in that at the time the stimulus dimmed identifying the saccade
target, the monkeys remained fixating until the central fixation point
went off. We imposed this delay to dissociate the neuronal activity
during the selection period from the activity in the initiation period.
In the blocked-mixed task, however, we changed the timing so that the
target was identified and the go signal occurred simultaneously, making
this a choice reaction time task. Because of this, we could measure the
latency of saccades as soon as the monkey selected the target and
initiated the saccade. The differences in activity between the early
and late trials in the blocked target trials prompted us to use the saccade latency in the last five blocked target trials for the comparisons.
In the mixed target trials, the mean latency was 266.21 msec (12.38 msec SE), and in the last five blocked target trials, the mean latency
was 245.00 msec (9.18 msec SE). These differences were statistically
significant (p < 0.01). Moreover, comparing the
saccade latency in the first five blocked trials (mean = 271.73 msec; SE = 14.62 msec) with that in the last five target trials (mean = 245.00 msec; SE = 9.18 msec) yielded statistically
significant differences across the sample (p < 0.01). Thus, consistent with the alterations in neuronal activity with
changes in saccade target probability, changes in saccade latency were
found concomitant with changes in the saccade target probability.
Higher saccade target probability resulted in decreased saccade
latency.
It is important to point out that although the changes in saccade
latency occurred concomitant with changes in neuronal activity, no
significant changes were measured in the metrics of the saccadic eye
movements. For example, the end points of saccades made in the one
possible target and the eight possible target conditions were not
significantly different (p = 0.70). The saccade
end points in the mixed target trials and in the last five blocked
target trials were also not significantly different
(p = 0.98). Likewise, no significant differences
were observed for saccade end points in the first five blocked target
trials and in the last five blocked target trials
(p = 0.88). We compared peak velocities of the
saccades made in the different conditions. The mean peak velocity in
the single target condition was 455.17°/sec (SE = 28.77°/sec),
whereas that in the eight possible target condition was 441.02°/sec
(SE = 29.13°/sec). This difference failed to reach significance
(p = 0.66). The mean peak velocity in the mixed
condition was 524.95°/sec (SE = 30.06°/sec), whereas that in
the last five blocked trials was 514.48°/sec (SE = 33.43°/sec). This difference also failed to reach significance
(p = 0.70). Finally the mean peak velocity of
the first five trials of the blocked condition was 510.80°/sec (SE = 35.01°/sec), and the mean in the last five trials was
514.48°/sec (SE = 33.43°/sec). This difference also was not
statistically significant (p = 0.99).
Thus, we found that the higher probability of a stimulus becoming a
saccadic target, the shorter the latency of a saccadic eye movement.
This result is consistent with the higher activity we recorded in the
buildup neurons. In contrast, the target probability did not result in
other saccade changes such as peak velocity or variation in end
point.
Effect of visual stimulus configuration
Comparison of the neuronal activity in the blocked target trials
and the mixed target trials demonstrated that the effect of target
probability could not have resulted from changes in the visual stimulus
configuration alone. However, this result does not exclude the
possibility that the visual stimulus configuration can contribute to
the activity of buildup neurons. We recorded 19 of the 32 neurons in
both the blocked-mixed task and the multi-target task and therefore
could assess the contribution of the visual stimulus configuration to
changes in the activity of buildup neurons. To do this, we compared the
activity of the buildup neurons in the one target condition of the
multi-target task, in which the probability of the target being
identified was 100%, to that in the blocked condition of the
blocked-mixed task, in which the target probability was also 100%
(Fig. 11). If we assumed that the
monkeys used the information accumulated on previous trials in the
blocked condition, the only difference between these trial types was
the visual stimulus configuration (one stimulus or eight stimuli).
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Figure 11.
Comparison of one and eight stimulus conditions
when target probability was the same. The data from the 19 neurons
recorded in both the multi-target task and the blocked-mixed task are
plotted to compare activity in the single stimulus, single target
condition with that in the eight stimuli, single target condition (see
Results). A, The mean firing rate during the visual
interval in the single target case is plotted against the mean firing
rate in the blocked target. B, The same activity is
plotted for the pre-selection interval data. C, The same
is plotted for the initiation interval. In the visual interval, many
neurons fell above the line, showing greater activity
when only a single stimulus was present and indicating an effect of the
stimulus display. Most neurons fell around the unity
line in both the pre-selection and the initiation intervals.
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We plotted the mean firing rate of the 19 neurons in the single target
condition against the mean firing rate in the blocked target condition
for three intervals: visual, pre-selection, and initiation (Fig. 11).
Points that fell along the unity line in these plots indicated that
there was no difference in the two conditions. Points that fell above
the lines in the plots indicated that neuronal activity in the single
target condition was greater than the activity in the blocked target
condition. During the visual interval, most neurons had activity that
was greater in the single target case than in the blocked target case
(Fig. 11A; p < 0.01). During the
pre-selection interval as well as the initiation interval, fewer
neurons showed this trend (Fig.
11B,C; p = 0.92 and
p = 0.89). Thus, the initial visual response of buildup
neurons was affected by the presence of other stimuli in the visual
field, whereas the later delay period activity was unaffected. The
interaction was one of suppression because the single visual target
always produced a larger response in buildup neurons than did the same stimulus embedded in the pattern of eight stimuli.
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DISCUSSION |
We investigated whether the activity of the SC buildup neurons had
the characteristics we would expect of neurons related to motor set by
using behavioral paradigms that varied the probability that a given
stimulus in an array would become the target for a saccade. We found
that a decrease in the probability that a stimulus would be the target
for a saccade resulted in a decrease in the activity of SC buildup
neurons. The change in activity was evident from the initial visual
response after the stimulus onset until the target was specified. The
changes in neuronal activity did not result simply from changing the
visual stimulus display, because altering the probability that a
particular target would be selected without changing the configuration
of the visual stimuli resulted in similar decreased activity with
decreased target probability. In contrast to the change in the delay
activity, the presaccadic burst of activity of buildup neurons, as well as that of burst neurons, was largely unmodulated by the level of
saccade target probability. Thus, although the burst of activity related to the direction and amplitude of the impending saccade remains
relatively fixed for any given buildup neuron, the earlier delay period
activity varies with the conditions under which saccades are made.
We think the changes in the delay activity of buildup neurons reflect
the changes in the motor set of the monkeys. We will first discuss the
relation of our observations with respect to motor set and then
consider what our observations indicate about the change of activity
across the SC movement map.
Relation of observations to motor set
Visual response
Changing the number of stimuli changed the number of possible
saccades monkeys could make and, thus, changed the motor set. The
initial visual response was correlated with changes in the number of
possible saccade targets. Moreover, the initial visual response was
greater in the blocked target trials compared with the mixed target
trials, indicating that change in buildup neuron activity reflected
more than the stimulus configuration. Buildup neuron visual response
changes are reminiscent of changes in the response of neurons in the
superficial layers of the SC referred to as visual enhancement
(Goldberg and Wurtz, 1972b; Wurtz and Mohler, 1976). When the
visual target falling in the receptive field of the neuron became the
target for a saccade, the visual response was larger. Thus, in both the
superficial layer neurons and the intermediate layer SC neurons, the
response to a stimulus is greater when that stimulus is a likely
saccade target. Visual responses of intermediate layer neurons have
been shown to facilitate the production of saccades (Edelman and
Keller, 1996), which is also consistent with our interpretation of this
activity as being related to motor set.
Delay activity
The delay period activity in our experiment, the activity after
the stimulus presentation but before identification of the target, is
similar to the delay period activity described for buildup neurons
(Munoz and Wurtz, 1995). In their task, monkeys were presented with
only two stimuli, either one of which could be the target for a saccade
on any given trial. During the delay period of a gap saccade task (in
which the fixation point disappeared but the monkey was required to
continue to fixate), the activity continued until one of the two
stimuli was specified as the target of the impending saccade. The
present experiments show that although the decrease in delay activity
is relatively slight moving from one to two possible targets, the
activity declines sharply for four or eight possible targets (Fig. 3).
As in the experiments of Munoz and Wurtz (1995), with only two targets
possible, the activity of the buildup neurons increased before the
target was identified.
This is in contrast to the observations of Glimcher and Sparks (1992)
that the activity increased after specification of the target in the
two target case. This led them to conclude that the increased activity
was dependent on the specification of the metrics of the saccade; that
is clearly not the case in our experiments because the increase
occurred before the metrics could be specified. One possible
explanation for this difference is that the prelude burst neurons do
not overlap the neurons we classified as buildup, although from their
example they appear to overlap. Another possibility is that the
temporal intervals of the tasks account for the differences. For
example, behavioral experiments indicate that the efficacy of
maintaining a high level of motor preparedness is limited in time (for
review, see Requin et al., 1991). Our pre-selection period was only 1.2 sec, in which case the monkeys may try to predict the upcoming saccade.
Glimcher and Sparks (1992), in contrast, used delays of 7 sec that
might have minimized the monkeys' attempts to predict the upcoming
saccade.
Changing the conditions of the task from presenting a different target
out of eight possible saccade targets on every trial to blocking a
single target repeatedly on every trial influenced motor set. We
confirmed this by determining that the saccade latency was shorter in
the blocked target trial condition than in the mixed target trial
condition. If the delay period activity reflects motor set, a simple
hypothesis is that the delay period activity should predict the latency
of the saccadic eye movement. Indeed, the neuronal activity was higher
in blocked target trials, and saccade latency was shorter. Thus, an
independent, behavioral measure of the change in motor set supports the
interpretation of buildup activity as reflecting motor set, or saccade
preparation (Munoz and Wurtz, 1995; Dorris et al., 1997).
Recently, the delay period activity of neurons in the rostral SC has
been shown to be active during pursuit eye movements as well as
saccades (Krauzlis et al., 1997). Also, neurons further caudal in the
SC, including those containing delay period activity, have activity
related to gaze changes that include movement of the head as well as
the eye (Freedman and Sparks, 1997). Thus, this activity is perhaps
best thought of as a general motor preparatory or readiness signal,
whereas in our experiments we manipulated only the level of saccade
preparation.
Target selection activity
After dimming the target, we always saw an increase in activity of
the buildup neurons. This increase is entirely consistent with that
seen by Glimcher and Sparks (1992) for prelude burst neurons using two
possible targets and with the increased activity of buildup neurons
seen by Kustov and Robinson (1996) after a cue indicated one of two
possible targets. What we found was that this increase was
substantially larger when the probability of any one target being
selected was less (Figs. 2, 3, 7), not because the selection activity
was greater but because the pre-selection activity was reduced.
The present experiments also show that although some of the neurons
showed a decline in activity as soon as the stimulus falling in the
movement field of the neuron was not identified as the target [as
shown by Munoz and Wurtz (1995) with two targets], other neurons did
not show such a decline (Fig. 6B). What this indicates is that some neurons convey little information about which
saccade target is not identified but rather convey information only
about which target is identified. In other words, the saccadic decision
process at this level in the system involves increased activity of SC
neurons voting for their location on the map (Robinson, 1972) and not
necessarily a suppression of activity at distracter locations. Slight
SC neuronal activity for targets located outside of the movement field
was also observed by Glimcher and Sparks (1992) in their task. The lack
of suppression of SC neuronal activity for these distractor stimuli
(Fig. 6C) contrasts with the flanking-inhibition mechanism proposed for saccade target selection at the level of the
frontal eye field (Schall et al., 1995).
Saccade initiation
In the buildup neurons we saw little change in the activity in any
burst preceding the saccade, nor did we see any such change in
presaccadic activity in the burst neurons. Neither result is surprising
because by the time of the saccade, the target had been identified and
all the trials were the same. We did see some alteration in the slight
earlier activity that we could identify in the burst neurons (Fig. 8),
but because this activity was so small to begin with, a reduction with
decreased target probability was minimal.
What is important for the differences in these two classes of neurons
is that the experimental conditions greatly affect the identification
of buildup neurons but not of burst neurons. We could convert what we
classified as a buildup neuron in a conventional visually guided
saccade task into a burst neuron simply by decreasing target
probability. However, we could never convert a burst neuron into a
buildup neuron. The identification of buildup neurons, therefore,
depends on the conditions under which the neuron is studied. We would
predict that any condition with low probability that a given saccade
would be made on any given trial would lead to a reduction in the
amount of delay period activity and would reduce the frequency of
identification of buildup neurons.
Behaviorally mediated changes over the SC map
The specification of saccades over time has been clearly
demonstrated at the behavioral level (Becker and Jürgens, 1979) where the accuracy of saccades evolves in the time between target presentation and saccade initiation. Thus, one would expect that the
activity in the SC would also evolve over time (Sparks et al., 1987).
This was demonstrated by Glimcher and Sparks (1993), who showed that
low-frequency electrical stimulation in one part of the SC, which
itself did not elicit saccades, increased the frequency of saccades
related to the part of the field served by the stimulated SC. The
temporal increase in the activity of buildup neurons (Munoz and Wurtz,
1995) is further evidence of the evolution of the saccade, so that
evidence from both neuronal activity and electrical stimulation is
consistent with a role for the SC in the specification of saccades over
time.
The present experiments demonstrate that the specification also
develops over space on the SC map. Saccade-related neurons in the
intermediate layers of the SC are organized on a movement map (for
review, see Sparks and Hartwich-Young, 1989), and within this map,
different regions become active before the onset of saccades of
different amplitudes and directions. We altered the development of the
spatial specification within the SC as revealed in two aspects of the
activity changes. First, when there was a high probability that a
particular saccade would be made, the activity of buildup neurons was
relatively high but confined to a restricted locus (Fig. 7). When there
was a low probability that a particular saccade would be made, the
activity of buildup neurons was much lower over the map. Second, when
the probability became 100% after the target dimmed, the activity
converged to a restricted locus; the activity increased at that point
but did not decrease throughout the SC. Thus, unlike the saccadic
movement map created by the burst neurons that is completely quiescent until the saccade, the buildup neuron map is slightly active for all
target locations. Any saccadic decision process that may be imposed on
the SC is accompanied by a focusing and an enhancement of the low-level
activity present throughout the map of SC buildup neurons into one
area. This focus occurs over the spatial map within the SC as the time
of the saccade approaches.
| |
FOOTNOTES |
Received May 21, 1998; revised June 23, 1998; accepted June 29, 1998.
We would like to thank our colleagues at the Laboratory of Sensorimotor
Research, the two anonymous reviewers, and Dr. Lee Stone for critical
comments on previous versions of this manuscript. We are also thankful
to Dr. Rich Krauzlis for data analysis software and the Laboratory of
Diagnostic Radiology for providing magnetic resonance images.
Correspondence should be addressed to Dr. Michele A. Basso, Laboratory
of Sensorimotor Research, National Eye Institute, Building 49, Room
2A50, Bethesda, MD 20892.
| |
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Top
Abstract
Introduction
