Download The Relationship of Monkey Frontal Eye Field Activity to Saccade

The Relationship of Monkey Frontal Eye Field Activity
to Saccade Dynamics
MARK
A. SEGRAVES
AND
KATHRYN
PARK
Department ofNeurobiology and Physiology, Northwestern University, Evanston, Illinois 60208-3.520; and Laboratory
Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, Maryland 60892
SIJMMARY
AND
CONCLUSIONS
I. In this study, we compared the temporal waveforms of the
activity of monkey frontal eye field movement neurons with the
dynamics of saccadic eye movements.
2. Movement neurons in the frontal eye field were selected
according to previously published criteria. They had little or no
response to visual stimuli in a fixation task, and equivalent activity before visually guided and memory-guided
saccades. We studied corticotectal neurons and corticopontine
neurons identified by
antidromic excitation, as well as neurons whose projections were
not identified.
3. These neurons had a peak activation at a mean of 13 ms
before the saccade began. However, rather than falling off rapidly
as the saccade ended, most neurons continued to fire after the
saccade. returning to baseline at a mean of 93 ms after the end of
the saccade.
4. We measured the decrement in activity for these neurons
during the saccade. Although a few neurons showed decrements of
~60% of their peak activity level, the average activity dropped
only 16.9%, with some neurons actually showing a rise in activity
during the saccade. If we ignored the latency between peak in
activity and saccade start and measured the fall in activity for a
period equal to one saccade duration after the peak, the average
drop in activity was still only 34.9%. Thus the activity of these
neurons did not appear to be closely related to dynamic motor
error, which falls from its maximum value to zero over the time
course of a saccade.
5. These results suggest that a focus of movement activity
within the topographic map in the frontal eye field specifies the
amplitude and direction for an impending saccade, whereas the
peak of movement activity signals the time to initiate a saccade.
6. Unlike the superior colliculus, the activity of frontal eye field
movement neurons does not appear to be related to dynamic
events that occur during the saccade, such as motor error.
INTRODUCTION
The frontal eye field has an important role in the control
of saccadic eye movements. Microstimulation
of this portion of frontal cortex produces saccades with short latency
and low threshold (Bruce et al. 1985; Robinson and Fuchs
1969); its movement neurons discharge before purposive
saccades, including those made to remembered target locations ( Bruce and Goldberg 1985 ). Frontal eye field movement neurons project to both the superior colliculus and to
oculomotor regions of the pons, including the region of
omnipause neurons in the paramedian pontine reticular
formation ( Segraves 1992; Segraves and Goldberg 1987 ).
Although it is likely to participate in the generation of all
voluntary saccades, the frontal eye field appears to be essential for the generation of cognitively difficult forms of saccades, including saccades to remembered target locations
1880
of
(Deng et al. 1986) and antisaccades-saccades
directed
away from the spatial location of a visual cue (Guitton et al.
1985).
Within cerebral cortex, several regions are involved in
the control of saccades besides the frontal eye field, including posterior parietal cortex (Andersen and Gnadt 1989;
Barash et al. 199 la,b; Duhamel et al. 1992; Kurylo and
Skavenski 199 1 ), the supplementary eye field ( Schall 199 1;
Schlag and Schlag-Rey 1987) and the cortex surrounding
the principal sulcus (Both and Goldberg 1989; Funahashi
et al. 199 1). These regions share many connections and
appear to form a cortical network involved in the control of
saccades. Recently, it has been reported that lesions of the
frontal eye field or parietal regions alone do not have a
substantial effect on visually guided saccades, whereas combined lesions reduce the accuracy and i ncrease the latency
for saccades to visual targets (Lynch 1,992). These monkeys, however, recovered from th e effects of th ese lesions
after several weeks. Schi ller and colleagu es (1 980) have
shown that combined bilateral lesions of the superior colliculus and frontal eye field cause substantial reductions in the
range of eye movements, as well as decreases in the frequency and velocity of saccades. These deficits do not diminish over time, and suggest that the frontal eye field generates an essential output from the cortical network.
The frontal eye field has many features in common with
the superior colliculus. Both regions have neurons that discharge before movements; both can support saccades in the
absence of the other; and of all cortical regions studied,
only the frontal eye field can evoke saccades by electrical
stimulation in the absence of the superior colliculus (Keating et al. 1983; Schiller 1977). Although they seem to have
parallel functions in the generation of saccades, the frontal
eye field does have the ability to influence the colliculus in
the generation of saccades in the normal monkey. It sends a
powerful presaccadic signal to the colliculus (Segraves and
Goldberg 1987), and may also help to control the basal
ganglia circuits, which themselves exert an influence on the
colliculus (Hikosaka et al. 1989). It is believed to exert a
cognitive influence on a more stimulus-bound
colliculus,
helping to select the appropriate eye movement to make
from a variety of possibilities (Goldberg and Segraves
1987).
Many characteristics of saccade-related activity in the superior colliculus have been known for some time. The most
prominent feature of the firing pattern of neurons with saccade-related activity is a burst of firing that begins ~20 ms
before the start of the eye movement (Mays and Sparks
0022-3077/93 $2.00 Copyright 0 1993 The American Physiological Society
FRONTAL
EYE FIELD AND SACCADE DYNAMICS
1980; Mohler and Wurtz 1976; Sparks 1978). For some
neurons, this burst is preceded by a gradual increase in firing rate beginning shortly after the signal to make a
saccade-several hundred milliseconds before the beginning of the movement. Because the focus of this activity
arises from a location within the movement map in the
intermediate and deep layers of the colliculus, this activity
could signal the amplitude and direction of an impending
movement. The burst of activity occurs at a time appropriate to trigger brain stem saccade-generating circuitry.
Recent evidence, however, suggests that the activity of subpopulations of collicular neurons helps to control dynamic
aspects of the saccadic eye movement. Focal lesions in the
superior colliculus result in decreased saccadic velocity as
well as dysmetria (Hikosaka and Wurtz 1986; Lee et al.
1988), suggesting that the superior colliculus is involved in
the actual motor programming of the saccade. Berthoz and
colleagues ( 1986) showed that part of the collicular discharge resembles the velocity profile of the ongoing saccade, and Waitzman and colleagues ( 1988, 1991) have
shown that the discharge of some collicular eye movement
neurons decreases as a linear function of the distance remaining in the saccade, the motor error.
Because of its close relationship to the superior colliculus
in the generation of movement, we thought it likely that the
frontal eye field would also be involved in the control of
saccade dynamics. Such a relationship would be particularly important in neurons that project to the pons, neurons
that are likely to drive saccadic eye movements in the absence of the superior colliculus. In these experiments, we
compared the relationship between neuronal discharge and
saccadic eye movements to see if the frontal eye field, like
the superior colliculus, was important in the dynamic programming of saccades. We studied three populations of
movement neurons: identified corticotectal neurons, identified corticopontine neurons, and neurons that could not
be excited antidromically
from either the superior colliculus or the pons. The presaccadic component of the activity
of these neurons was similar to the original descriptions of
saccade-related neurons in the colliculus. This activity began to rise above baseline - 100 ms before the beginning of
the saccade, and peaked just before the start of the eye movement. This signal might I) relay the amplitude and direction of an impending saccade to the superior colliculus and
pons and 2) initiate the trigger to make a saccade. We failed
to show a consistent relationship between saccade dynamics and neuronal discharge for these cortical neurons.
In particular, frontal eye field neurons did not appear to
emit a signal that could be related to motor error or velocity
during the saccade. A preliminary report of these experiments has been published elsewhere (Segraves et al. 1990).
1881
V
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StimuIusOnset
0
2ooms
Visual response of corticopontine movement neuron. Activity
in visual no-saccade task. The monkey fixed his gaze on a fixation point
(FP) directly in front of him. During the time that he was fixating, a light
was turned on for 50 ms at a location with radius of 18’ and angle of 109O
(S). The monkey was rewarded for keeping his gaze on the fixation point.
The stimulus light was used to test the neuron’s visual responsiveness.
Below the schematic of fixation point and stimulus light positions are the
recordings of vertical (V) and horizontal (H) eye position during the trial.
Below the eye position traces are a raster and histogram showing the activity of this neuron (sampled at 250 Hz) during a period of 200 ms before
and after the onset of the peripheral stimulus. Each line in the raster contains the activity from a single trial, and each small vertical line indicates
the time at which the neuron fired. The data from 16 consecutive trials
included in this raster are aligned on the onset of the stimulus. This time is
indicated by the large vertical line drawn through the center of the raster.
The histogram shows the sum of the activity from these trials, with the
vertical line again indicating the onset of the stimulus. The vertical bracket
at the bottom l@ of the histogram indicates the amplitude of a firing rate of
100 spikes per second. Note the faint visual response beginning -80 ms
after the onset of the stimulus. The same general configuration used in this
figure is used in Figs. 2 and 3.
FIG.
1.
neuronsencounteredduring experimentsdesignedto identify and
characterize neuronswith projections to the superior colliculus
and pons.The proceduresfor training, surgery,electrophysiology,
METHODS
and histology for these monkeys appear in the original reports
The data describedin this paper were obtained during single- (Segraves1992;Segravesand Goldberg 1987).
unit recordingsfrom four behavingrhesusmonkeys(A4acacamulcltfcr)identifiedasLSR30,LSRSO,LSRS1, and MASO 1.All exper- Behavioral tasks
imental proceduresfor monkeysLSR30,LSRSO,and LSRS1 were
performedat the National Eye Institute. The experimentalproceTo obtain the data describedin this report, behavioraltaskswith
duresfor monkey MASOl and subsequentdata analysisfor all and without saccadeswere used. I) Visual no-saccadetask: the
four monkeys was performed at Northwestern University. The monkey fixated the stationary light spot in the center of the tanneuronsdescribedin this report are a subsetof frontal eye field gent screen(FP in Fig. 1) for the duration of the trial. During the
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M. A. SEGRAVES
A
AND K. PARK
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Saccade Beginning
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2. Activity in the visually guided saccade task. While the monkey was fixating, the fixation point was turned off and
a target light (T) turned on for 50 ms at the same location used in the visual no-saccade task illustrated in Fig. 1. The rasters
and histograms illustrate activity occurring 200 ms before and after the onset of the target light (A), the beginning of the
saccade ( B), and the end of the saccade ( C). In this task, the saccade begins ~200 ms after the onset of the target, and so it is
difficult to separate visual- from movement-associated activity. It is clear, however, that the activity is much stronger than
when the monkey did not make an eye movement (Fig. 1 ), and that the increase in activity peaks near the beginning of the
saccade.
FIG.
trial, at an unpredictabletime, a secondlight spot(S in Fig. 1) was
flashedfor a variable period of time. The position of the second
light wascontrolled by mirror galvanometersand could be placed
anywherewithin the monkey’s visual field. The monkey wasrewardedfor maintainingfixation of the center light throughout the
trial. The peripheralstimulushad no behavioral significance.Its
position wasusedto map the visual receptivefieldsof frontal eye
field neurons. 2) Visually guided saccadetask: after a variable
period of fixation, the center light wasextinguishedat the same
momentthat a peripheraltarget light (T in Fig. 2) wasturned on.
When the peripheraltarget appeared,the monkey wasrequiredto
make a saccadeto the target’slocation within 500 ms. After the
saccade,the monkey wasrewardedeither for maintainingeye position within a window with -3-6’ radiussurroundingthe new
targetposition or for having madea saccadewhoseend point was
within the window. The movable light spotwasagainusedfor the
peripheraltarget, and could be positionedanywhere on the tangent screen.The duration of the target flashwasvariable. For the
trials illustratedin Fig. 2, the target wason for only 50 ms,and the
saccadewasactually madein darknessafter the disappearanceof
the target. In another version of this task, the target remainedon
until the saccadewascomplete and the trial ended.3) Memoryguided saccadetask: in a second,more difficult form of saccade
task, the center light cameon to start the trial, asbefore, and the
monkey wasrequiredto beginand maintain fixation of the center
light until it wasturned off. During the central fixation period, a
peripheraltarget wasturned on for 50-300 ms.When the center
light wasturned off, the monkey wasrequiredto makea saccade
to the position of the flashedperipheraltarget light. The duration
and time of occurrenceof the target flashwereadjustedsothat the
target light wasturned off during the fixation period, requiring the
monkey to maintain fixation for 5250 ms after the target light’s
disappearance
and then make a saccadeto a rememberedtarget
location. This task enabledusto distinguishbetweenvisual- and
movement-associated
neuronal activity during the trial.
In this study, the location of visual stimuli and targetsare expressedin polar coordinates,radius, and angle, where radius is
equal to the distance,in degreesof arc, of the target or stimulus
from the central fixation point. An angleof 0” describesa rightward horizontal direction, and a 90” angledescribesan upward
vertical direction.
Data analysis
Rastersand histogramswere constructed with neuron activity
alignedon important eventswithin a trial.
We classifiedneuronson the basisof their activity during visuomotor tasks,usingthe criteria of Bruceand Goldberg( 1985). Our
presentanalysiswasconfined to neuronswith movement activity.
Movement neuronshave little or no responseto visualstimuli, but
very strong activity before both visually guided and memoryguided saccades.Movement neuronsin the frontal eyefield have
definable movement fields. Their peak dischargeoccurs for saccadesof a specificamplitude and direction, with theseparameters
dependingon the neuron’slocation in the frontal eyefield’stopographic map.
To facilitate the comparisonbetween neuron activity and the
changesin eye position and velocity during saccades,the static
rasteror histogramplot of activity wasconverted to a continuous
spike density function (Richmond et al. 1987; Sandersonand
Kobler 1976). This wasdone in two ways.For most neurons( n =
33), both neuron firing activity and eye position data during eye
movementtrials werestoredat 250or 1,000Hz. A Gaussiancurve
with 0 = 8 mswasfitted to the time of occurrenceof eachneuron
spike during a trial. For each trial, Gaussiancurves representing
each spike were summed,providing a continuous function ex-
FRONTAL
EYE
FIELD
AND
pressing the expected spike frequency for any point in time during
the trial. This activity was then averaged across trials to produce
the average spike density for the neuron in a particular task. For
these data, the beginning and end of the saccade were defined as
the times at which eye velocity exceeded and then decreased below
100’ /s. For the remaining neurons ( II = 15 ), continuous records
of eye position during each trial were not available. For these cells,
spike density functions were generated from rasters of neuron activity that contained timing marks to indicate the beginning and
end of the saccade. These rasters were generated during the recording experiment with a sampling frequency of 250 Hz. The beginning and end of the saccade were determined on-line at the time of
the experiment, and corresponded to the times at which eye velocity exceeded and then decreased below 3O”/s. For these data, a
histogram of activity averaged across 16 trials was generated and
then a spike density function, with CI again equal to 8 ms, was
derived from the histogram. Although two different velocity criteria were used to distinguish the beginning and end of saccades,
these times, as well as the durations of saccades obtained with both
techniques, were very similar.
RESULTS
We examined the activity of a total of 48 frontal eye field
movement neurons. These included 35 identified neurons:
26 corticotectal neurons and nine corticopontine neurons.
In addition, our analysis included 13 movement neurons
whose projections were not identified: one neuron that
could not be antidromically excited by a collicular stimulating electrode, and 12 neurons that were not antidromically
excited by a pontine electrode.
The activity of a corticopontine movement neuron is illustrated in Figs. l-4. This particular neuron was chosen
for illustration because the timing of the beginning, peak,
and end of its saccade related activity was similar to the
average times for the entire sample. During the visual nosaccade task (Fig. 1 ), this movement neuron gave only a
few spikes per trial in response to the 50-ms flash of a spot of
light in the center of its movement field. In contrast, it gave
brisk bursts of activity that preceded and continued
through the duration of both visually guided saccades (Fig.
2) and saccades made in darkness to the remembered location of the target spot (Fig. 3). Although the rasters show
some variability from trial to trial, the histograms illustrate
that, overall, the activity of this cell began to rise - 150 ms
before the start of the saccade, peaked near the beginning of
the saccade, and fell back to a baseline level - 100 ms after
the end of the eye movement. The cell’s activity for both
visually guided and memory-guided saccades was quite similar.
Figure 4 illustrates the mean spike density for the same
neuron shown in Figs. l-3. The mean spike density is superimposed on plots of vertical eye position and velocity.
Velocity was computed by digital differentiation. The spike
density is compared to saccades made to both visually (Fig.
4A ) and memory-guided saccades (Fig. 4B).
A qualitative examination
of the spike density profile
confirms what was seen in the histograms of Figs. 2 and 3.
The rise in spike density related to the saccade begins and
ends > 100 ms before and after the saccade, and peaks near
the start of the eye movement. Note that the spike density
profile was similar for firing activity generated in both visually guided ( Fig. 4A ) and memory-guided ( Fig. 4 B) saccade tasks.
SACCADE
DYNAMICS
1883
For each of the 48 neurons included in our sample, we
made quantitative measurements of the timing of the rise in
spike density relative to the saccade. Figure 4A illustrates
how these measurements were made. The baseline level of
spike activity was determined by examining the activity for
5 1,000 ms before and after the start of the saccade. The
beginning and end of the spike density rise were defined as
the times at which spike density rose above and later returned to the baseline level of activity. The time for the
beginning and peak of the rise in spike density was measured relative to the start of the eye movement. The time for
the end of saccade-related spike density activity was measured relative to the end of the saccade.
Figure 5 illustrates the distributions of times for the beginning, peak, and end of the change in spike density associated with saccades. For 27 neurons, the times used for
these distributions were measured from data obtained during the visually guided saccade task. For the remaining 21
neurons, sufficient data for visually guided saccades did not
exist, and the times for these distributions were measured
from data obtained during the memory-guided
saccade
task. These movement neurons began to increase their activity from 3 1 to 2200 ms before the start of the saccade (Fig.
5A ). The mean time for activity to rise above the baseline
level was 148 ms before the beginning of the saccade. Their
activity peaked from 120 ms before to 93 ms after the start
of the saccade (Fig. 5 B), with 58% of the neurons having a
peak of activity within 40 ms of the start of the saccade. The
mean time for activity to peak was 13 ms before the saccade
began. Some significant differences ( t test, P < 0.05) were
found for the mean times of peak activity for the different
groups of neurons included in this study. The peak of activity for corticotectal neurons (-34 ms) occurred earlier than
it did for both corticopontine
(-2 ms) and unidentified
(+20 ms) movement neurons. All neurons, except three
corticotectal cells, finished firing after the saccade was completed (Fig. 5C). Most neurons continued firing for a substantial period of time after the end of the eye movement,
with a mean of 93 ms after the end of the saccade.
In the superior colliculus, neurons that are believed to
code dynamic motor error showed a sharp decrement in
their firing activity during a saccade (Waitzman
et al.
199 1). These collicular neurons had peak activity at the
beginning of a saccade, and their activity decreased nearly
100% during the course of the eye movement. We examined the decrement in activity during saccades for the frontal eye field neurons included in this study.
For each neuron, we determined the magnitude of the
change in activity during the saccade and expressed this
value as a percentage of the peak firing activity. A change in
activity from peak to baseline level during the saccade was
represented as a 100% drop. Increases in activity during the
saccade were expressed as negative percent drops. For example, for the neuron illustrated in Fig. 4, activity dropped an
amount equal to 33% of the peak activity during the visually guided saccade task ( Fig. 4A), and dropped 28% during the memory-guided saccade task (Fig. 4 B). Figure 6 is a
plot of these values for the 48 frontal eye field neurons included in this study. Each value is referenced to the latency
of the neuron’s peak discharge to the beginning of the saccade. Overall, the activity of these neurons dropped 16.9 t
M. A. SEGRAVES
AND K. PARK
B
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FIG. 3. Activity in the memory-guided saccade task. While the monkey was fixating, a target light was turned on for 350
ms and then turned off. Fifty milliseconds after the target was extinguished, the fixation point was turned off, signaling to the
monkey that he could make a saccade. The saccade was made, in darkness, to the remembered location of the flashed target.
The monkey was rewarded for making a saccade of appropriate amplitude and direction. Rasters and histograms are
arranged as in Fig. 2. In this task, the onset of the target and the beginning of the saccade were separated by -500 ms. As a
result, it is easyto distinguish the faint visual response in A from the substantial movement-related activity shown in R and (‘.
3 1.3% (mean t SD) during the eye movement. Note that
only a few neurons showed drops >60%, and many neurons
actually increased their activity during the saccade. The activity of unidentified movement neurons tended to drop
less during the saccade than did other neurons, although
this difference was only significant when comparing unidentified with corticotectal neurons (t test, P < 0.05 ).
We attempted to allow for delays between the drop in
activity after the peak and the actual time of generation of
the movement by measuring the drop in activity during a
time period equal to one saccade duration immediately
after the peak in discharge. For the neuron illustrated in
Fig. 4, this value was equal to 40% for visually guided saccades (Fig. 4A) and 27% for memory-guided saccades (Fig.
4B). This procedure eliminates the generation of negative
percent drops. Figure 7 plots the distribution of these values
for all 48 neurons. This manipulation
ignores the latency
required for frontal eye field activity to have an effect on eye
movement dynamics, and produces a narrower distribution
of changes in activity. We found an average of 34.9 t 15.4%
(mean t SD) drop in activity. Again, only a small number
of neurons showed a drop in activity of >60% of the peak
activity level. Corticopontine
neurons tended to drop less
quickly after the peak of activity, but this tendency was only
significant when comparing the means for corticopontine
with unidentified movement neurons (t test, P < 0.05).
DISCUSSION
We have examined the activity of movement neurons in
the frontal eve field and have comnared that activitv with
the dynamics of saccadic eye movements. The population
of movement neurons that we studied included cells with
identified projections to the superior colliculus or to the
pons, as well as neurons whose termination sites were unknown. As a group, these neurons began to increase their
activity > 100 ms before the start of a saccade. Their activity
peaked with a mean of 13 ms before the beginning of the
saccade, and then gradually fell toward baseline levels.
Their activity reached baseline 93 ms after the completion
of the saccade. On average, the activity of these neurons fell
during the saccade by an amount equal to only 17% of the
peak activity level. There was a great deal of variability in
this measurement, with a few neurons showing decrements
of >60% during the saccade and a number of neurons
showing increases in activity during the eye movement.
This discussion will consider the probable role of frontal
eye field movement activity in the generation of saccades,
and the relationship of that activity to feedback control
models of the saccadic system, and will make comparisons
with the role performed by the superior colliculus in this
process.
Frontal eye jeld movement neurons signal the amplitude
and direction qf an intended movement, and the time to
initiate that movement
The scope of this study was restricted to an examination
of neurons with movement-related
activity. Movement neurons form the largest population of cells that project to the
superior colliculus and pons (Segraves 1992; Segraves and
Goldberg 1987). Thus their activitv generates a maior out-
FRONTAL
EYE FIELD AND SACCADE DYNAMICS
1885
V. Positian
V. Velocity
Saccade Beginning
-200
End
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-200
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4. Spike density during visually guided and memory-guided saccades. A plot of mean spike density is superimposed
on the vertical component of eye position and eye velocity for a period of 200 ms before and after the beginning of the
saccade. A: mean spike density for 10 trials of the visually guided saccade task. B: mean spike density for 1 1 trials in the
memory-guided saccade task. A illustrates how the quantitative measurements used for this study were made: the neuron’s
activity was examined for 5 1,000 ms before and after the beginning of the saccade, and a line drawn to indicate the activity
baseline. The beginning and end of the rise in spike density were marked at the points where spike density rose above and
later fell below the baseline level of activity. Eye velocity was computed by digital differentiation of the eye position trace, and
was used to identify the beginning and end of the saccade. The beginning and end of the saccade were defined as the points at
which the rise and fall of eye velocity passed the 100” /s level. The time of the beginning and peak of the spike density rise
were measured relative to the beginning of the saccade. The end of the spike density rise was measured relative to the end of
the saccade. Note that the changes in spike density associated with the saccade are quite similar for both visually guided and
memory-guided saccades. In this example, neuron activity was sampled at 1 kHz; thus a spike density value ofO.1 signifies an
expected firing frequency of 100 Hz.
FIG.
put signal that is sent from frontal eye field to the brain
stem. We have not included fovea1 neurons in this study.
Frontal eye field fovea1 neurons are responsive to visual
stimulation of the fovea and, in addition, have activity related to fixation (Bizzi 1968; Bruce and Goldberg 1985;
Suzuki and Azuma 1977; Suzuki et al. 1979). Fovea1 neu-
rons compose the second-largest group of neurons that project to the superior colliculus and pons. Their activity is
believed to contribute to the maintenance and release of
fixation (Segraves 1992; Segraves and Goldberg 1987).
Figure 8 summarizes our current understanding of the
signals sent by frontal eye field movement neurons to both
1#86
M. A. SEGRAVES
AND K. PARK
507 A
100%
Beginning
Standard
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Deviation
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Density
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Saccad; Beginning
Peak
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Mean
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Standard
Density
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A
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Rise
= 49
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---.-
~-~-r---T-
t
-200
Saccade
Latency
5 1200
End
Mean
Standard
Saccad; Beginning
of Spike
Density
2 +200
Rise
+200
Beginning
of Peak Discharge
to Start
of Saccade
(ms)
FIG. 6. Drop in activity during saccade. Drop in activity during the
saccade is expressed as a percentage of peak activity for the cell, and referenced to the latency of the cell’s peak discharge to the beginning of the
saccade. Negative percentage values signify a rise in activity during the
saccade.
= +93
Deviation
= 66
Saccade End
Time (ms)
5. Timing of the beginning, peak, and end of the rise in spike
density associated with the saccade. Measurements taken from plots such
as those illustrated in Fig. 4 were used to produce histograms of the distribution of the times for beginning (A), peak (R), and end (C) of the rise in
saccade-related spike density. These data were put into bins 20 ms wide.
Note that for A and B, time = 0 marks the beginning ofthe saccade, and for
C‘, time = 0 marks the end of the saccade. Time values less than -200 ms
were included in the -200-ms bin: values greater than +200 ms were
included in the +200-ms bin. Values for 48 neurons are included in these
histograms.
FIG.
the superior colliculus and pons. Our interpretation of the
present results is that the movement neurons in the frontal
eye field provide two signals relevant to the generation of a
saccadic eye movement. I) The peak of their activity signals the time to initiate the saccade. It is a trigger signal. The
peak in movement neuron activity, at a mean of 13 ms
before the saccade, occurs at about the time that omnipause
neurons are turned off at lo- 15 ms before the saccade
(Henn and Cohen 1976; Keller 1974; Luschei and Fuchs
1972; Robinson 1975 ). On the basis of the latencies of corticopontine, corticotectal, and tectopontine cells, this signal
could directly excite pontine cells within 1.4-4.0 ms and
within 2.3-4.9 ms via a projection from cortex to colliculus
to pons (Raybourn and Keller 1977; Segraves 1992; Segraves and Goldberg 1987). Because it is unlikely that the
corticopontine neurons are directly inhibitory (Schwartz et
al. 1985, 1988) if frontal eye field neurons turn off pause
neurons, they probably do so via inhibitory neurons in the
vicinity of the pause cells. 2) The sustained increase in activity output from a group of movement neurons signals the
amplitude and direction for the impending saccade. This
activity would originate from a restricted area within the
movement map of the frontal eye field that represents large
eye movements dorsomedially and small eye movements
ventrolaterally ( Bruce et al. 1985 ). Our study does not rule
out the possibility that some frontal eye field neurons send a
dynamic motor error signal to the midbrain and pons; our
sample may have missed those neurons. The present analysis, however, makes it clear that the frontal eye field is sending both a trigger and a desired change in eye position signal
to the midbrain and pons. These signals are very similar to
those ascribed by Sparks and colleagues to saccade-related
burst neurons in the superior colliculus. Those collicular
neurons gave a burst of activity that began - lo-20 ms
before the start of a saccade with optimal amplitude and
direction. About one fourth of superior colliculus movement neurons showed a gradual rise during the period between the signal to make a saccade and the beginning of the
saccade (Mays and Sparks 1980; Sparks et al. 1976). This
collicular activity may arise, in part, from frontal eye field
input, but is probably also due to the integration of input
from many other sources. Concerning the slow rise in fronf$ 10096,
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0
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-200
0
of Peak Discharge
+200
Beginning
to Start of Saccade
(ms)
FIG. 7. Drop in activity during the time beginning with the peak in
activity and lasting for a period equal to the duration of the saccade. See
text for additional details.
FRONTAL
EYE
FIELD
AND
SACCADE
DYNAMICS
1887
demonstrated that some neurons in the monkey superior
colliculus appear to have activity that codes dynamic motor
error (Waitzman et al. 1988, 199 1). They propose that the
colliculus generates this signal by continually subtracting a
current change in eye position signal from the initial desired
change in eye position signal. The current change in eye
position signal would be obtained by integrating the eye
SUPERIOR
PONTINE
OMNIPAUSE
!
velocity command output by burst neurons (Waitzman et
& BURSTNEURONS
-(
coLLIcuLus
+
al. 1988, 199 1). Munoz and colleagues have proposed that
neurons in the cat superior colliculus lie within a gaze feedback loop and exhibit changes in activity that are related to
the
dynamics of movements of the eyes and head (Munoz
FIG. 8. Input of frontal
eye field movement
neurons to the superior
et al. 199 1). In this case, brain stem feedback is used to shift
colliculus and pons. The signals output by the frontal eye field are based on
the center of activity across the collicular movement map,
the present study. Signals sent between superior
colliculus
and pons are
compiled from a number of works cited in the text. See text for additional
from the region coding the desired saccade amplitude and
detail.
direction toward the fixation zone at the rostra1 pole of the
colliculus. Their model also requires that the feedback sigtal eye field activity before the movement, it is interesting to nal pass through a neural integrator (Guitton 199 1; Munoz
note that Sparks and colleagues ( 1987) have reported that et al. 1991).
activity within the paramedian pontine reticular formation
The superior colliculus may also help to control the velocconcerning an impending eye movement builds up graduity of saccades (Berthoz et al. 1986; Hikosaka and Wurtz
ally over a IOO-ms period before the start of the saccade. 1986; Lee et al. 1988). We did not, however, find evidence
This corresponds closely to the rise time for frontal eye field in this study for a relationship between eye velocity and the
movement activity.
activity of movement neurons in the frontal eye field. In
most cases, frontal eye field activity declined slowly during
Frontal evefield does not contribute tofiedback control or
the
saccade-an inappropriate
signal for coding the dythe specljication of eye velocity during saccades
namics of eye velocity. Waitzman and colleagues ( 199 1)
Feedback is an important component of the control sys- have pointed out that a steadily declining signal could not
tem for generating saccades [see Van Gisbergen and Van code the increase and decrease of velocity that occur during
Opstal ( 1989) for review]. Early experimental evidence for a saccade. If it did, equal velocities during the acceleration
this feedback came from patients with spinocerebellar de- and deceleration phases of the movement would be coded
generation whose saccades were sufficiently slow to allow by different levels of neuron activity. Unfortunately,
our
intrasaccadic modification of their trajectories (Zee et al. experiments did not allow us to address the possibility that
1976). Other evidence came from normal human subjects frontal eye field activity might code the peak velocity for an
(Becker and Jurgens 1979; Hallett and Lightstone 1976) impending saccade. Although it has been reported that the
and monkeys (Sparks and Mays 1983). Robinson ( 1975, velocity of equal-length saccades can vary depending on the
198 1) proposed a local feedback control model where de- eye movement task (Rohrer et al. 1987) we noted very
sired eye position is compared with an efference copy of little variation in the velocity of saccades generated in our
visually versus memory-guided saccade tasks. One possible
actual eye position to yield a motor error signal. The motor
error signal drives the burst neurons, which in turn produce
explanation is that the gap between target disappearance
and the cue to make a saccade tended to be relatively short
the pulse of eye velocity that provides the major component
in our memory task (5250 ms).
of the motor neuron discharge. In subsequent modifications of the feedback model (Jiirgens et al. 198 1; Scudder
1988; Van Gisbergen and Van Opstal 1989), desired sac- Relative contributions of’the fkontal eye field and superior
cade amplitude is compared with the distance traversed by colliculus in the genera&z of ‘saccad& *
the current saccade to produce the motor error signal. The
Placing the superior colliculus, but not the frontal eye
present results suggest that the frontal eye field does not
participate in the feedback process, because its signals are field, within a feedback loop involved in the dynamic control of saccades is difficult to reconcile with the finding that
relatively constant during the saccade. Thus the feedback
loop must occur at a level downstream from the frontal eye monkeys can make visually guided saccades after bilateral
field cortex. Scudder ( 1988) has proposed that the feedback
removal of the superior colliculus (Schiller et al. 1980).
occurs at the level of long lead burst neurons in the pons, This lesion study emphasized the parallel nature of the parwith frontal eye field and superior colliculus providing simiticipation of colliculus and frontal eye field in the generalar inputs specifying the saccade target and the trigger to tion of saccades. If, as recent findings suggest, the superior
initiate the movement. The activity of many saccade-re- colliculus is within a feedback loop that supplies the oculolated neurons in the superior colliculus seems appropriate
motor system with a dynamic motor error signal, how is
this signal derived in the absence of the superior colliculus?
for this function, and is in many ways similar to that found
in the frontal eye field (Mays and Sparks 1980; Mohler and One possibility is that the frontal eye field, as well as other
areas, modify their output in the abWurtz 1976; Sparks 1978). Recent experiments, however, oculomotor-related
sence of the superior colliculus and provide the needed moprovide evidence that would place the superior colliculus
within the feedback loop. Waitzman and colleagues have tor error signal to the brain stem. Anatomic projections
TRIGGER
DESIRED
CHANGE
IN EYE
POSITION
%rg,gcr
Dewed
Change
III Eye
Position
Velocity
VdOCl~
-
Dvnamrc
Current
hfomr
Chunge
Error
rn Eye
Posrrmn
1888
M. A. SEGRAVES
from oculomotor cortex to the brain stem that bypass the
superior colliculus are known to exist. Both the frontal eye
field and supplementary eye field project directly to oculomotor regions of the pons, including the region of omnipause neurons in the nucleus raphe interpositus; the general
vicinity of burst neurons in the paramedian pontine reticular formation; and nuclei forming relays with the cerebellum, including the nucleus reticularis tegmenti pontis and
basal pontine nuclei (Huerta and Kaas 1990; Huerta et al.
1986; Leichnetz et al. 1984; Schnyder et al. 1985; Shook et
al. 1990; Stanton et al. 1988). An alternative explanation is
that the dynamic motor error signal observed in the superior colliculus is not necessary to make accurate saccades,
but is perhaps part of a corollary discharge generated by the
colliculus. It should be noted that the anatomic targets of
the collicular dynamic motor error cells described by
Waitzman and colleagues have not been identified. Finally,
it may be possible that a desired change in eye position
signal from the frontal eye field is sufficient for other structures such as the cerebellum to drive the saccade-generating
mechanism in the absence of a motor error signal from the
colliculus.
Although it is unclear how saccades are generated in the
absence of the superior colliculus, under normal circumstances the superior colliculus and frontal eye field, as well
as other regions including posterior parietal cortex, the supplementary eye field, and periprincipal cortex operate via
both serial and parallel pathways to control the generation
of saccades. Our examination of frontal eye field activity
combined with the work of other laboratories investigating
superior colliculus activi tY reveals a significant difference
between the superior colliculus and frontal eye field in their
roles in the generation of saccades. Whereas the colliculus
appears to code signals that are related to dynamic aspects
of the movement, like velocity and motor error, the frontal
eye field functions at a higher level in the saccade generation process, signaling the target for the saccade and triggering the movement. This emphasizes a purported role for the
frontal eye field as a link between cortical cognitive processing preceding the initiation of an eye movement and the
more machine-like organization of the midbrain and brain
stem designed to execute the motor command (Goldberg
and Segraves 1987). As such, the frontal eye field may select the target for the next eye movement from a variety of
external visual stimuli and internal cues, but it is not involved in the guidance of the movement once it has begun.
We are grateful to the following for skillful support: A. Hayes for computer software; A. Ziminsky and Northwestern’s Chemistry Electronics
Shop for electronic hardware; C. Crist, T. Ruffner, and Northwestern’s
Physics Instrument Shop for machining; M. Smith for histology; C. Polchow for histology and photography; and A. Hanson, H. Macgruder, K.
Powell, and the staff of Northwestern’s Center for Experimental Animal
Resources for animal care. We are particularly grateful to M. Goldberg for
providing the computer software to generate the spike density functions
and for innumerable discussions and insights concerning this work. We
thank D. Burman for his comments and discussion concerning this manuscript.
This work was supported by National Eye Institute Grant EY-082 12,
Division of Research Resources-Biomedical Research Development
Grant-BRSG Award RR-07028, and The Sloan Foundation.
Address for reprint requests: M. A. Segraves, Dept. of Neurobiologv and
AND K. PARK
Physiology, 0. T. Hogan Hall, Northwestern
60208-3520.
University, Evanston, IL
Received 24 July 1992; accepted in final form 29 January 1993.
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