Rapid coordinated eye–head movements, called saccadic gaze shifts, displace the line of sight from one location to another. A critical
structure in the gaze control circuitry is the superior colliculus (SC) of the midbrain, which drives gaze saccades by relaying cortical
commands to brainstem eye and head motor circuits. We proposed that the SC lies within a gaze feedback loop and generates an error
signal specifying gaze position error (GPE), the distance between target and current gaze positions. We investigated this feedback
hypothesis in cats by briefly stopping head motion during large (?50°) gaze saccades made in the dark. This maneuver interrupted
the position of the cell and then declined back to zero near gaze saccade end. In brake trials, the activity level just preceding a brake-
induced plateau continued steadily during the plateau and waned to zero only near the end of the corrective saccade. The duration of
A dominant question in oculomotor control is how the spatially
encoded signal on the motor map of the superior colliculus (SC)
is transformed into the temporally encoded signal required by
reticular gaze control circuits that receive collicular commands
(for review, see Moschovakis et al., 1996; Scudder et al., 2002). It
has been proposed that ocular saccades are controlled by a local
brainstem feedback loop that compares desired with actual eye
rotation to generate an eye motor-error signal that in turn drives
the saccade burst generator until the error is nullified. In one
hypothesis, the SC is within the feedback loop (for review, see
Scudder et al., 2002; Guitton et al., 2003a,b): in primate, its out-
put has been assumed to encode eye motor error either exclu-
sively at the initially active site on the motor map (Waitzman et
al., 1991) or by a spreading front of activity across the map that
stops saccades when it invades the fixation zone (Munoz et al.,
1991a,b; Munoz and Wurtz, 1995a,b).
If the SC is in a feedback loop, collicular discharges should
respond to perturbations of saccadic eye movement trajectories.
This important test has been attempted in the head-fixed mon-
key. Saccade trajectories were perturbed by using either electro-
physiological or pharmacological approaches (Keller and Edel-
man, 1994; Munoz et al., 1996; Keller et al., 2000; Soetedjo et al.,
bation, and gaze arrived on target. Concurrently, the firing-
to that in unperturbed saccades. Specifically, discharge duration
increased in relation to the increased overall duration of the eye
movement necessary for the eye to get on target. The interpreta-
tion of the results varied greatly among the studies, varying from
a support of the SC being in a feedback loop encoding either
motor error (Munoz et al., 1996) or saccade end (Soetedjo et al.,
2002a) or an unknown mechanism (Keller et al., 2000) to the
argument that the SC functions open loop and sends to the pons
a fixed number of spikes (Goossens and Van Opstal, 2000a,b).
Head-unrestrained gaze saccades are also thought to be con-
trolled by a feedback loop that produces a signal encoding gaze
position error (GPE), the distance between target and current
2003a,b). We proposed that cat SC efferents, tectoreticular neu-
2000, 2002; Bergeron et al., 2003). According to our moving-hill
model, during a gaze shift, the locus of neural activity on the
motor map continuously encodes GPE by moving rostrally from
an initial location that encodes the overall direction and ampli-
Gaze shifts are ideally suited for testing feedback to the SC,
because they can be easily perturbed by briefly braking the head
trajectory in-flight. Head perturbations are a natural phenome-
non that occurs readily in the daily life of animals and in human
Correspondence should be addressed to Dr. Daniel Guitton, Montreal Neurological Institute, 3801 University
2760 • TheJournalofNeuroscience,March17,2004 • 24(11):2760–2773
sporting activities. In comparison, it is unnatural to perturb
cuits. Our recordings in the SC during mechanical interference
with gaze motion support the hypothesis that the cat SC is in a
gaze feedback loop, and that it encodes GPE.
Animal preparation. All of the surgical and experimental protocols were
approved by the Animal Care Committee of the Montreal Neurological
Institute and complied with the Canadian Council on Animal Care pol-
to the target in our barrier paradigm (see Behavioral procedures). The
data described here were obtained in four of the eight cats that provided
the material for our previous papers describing the discharges of cat
collicular cells during multiple-step gaze shifts (Bergeron and Guitton,
an intramuscular injection of ketamine hydrochloride (10 mg/kg). The
cats were then intubated and maintained on anesthesia using halothane.
During surgery, heart rate, respiratory rate, and body temperature were
monitored. A wire coil consisting of three turns of Teflon-coated multi-
strand stainless-steel wire (California Fine Wire, Grover Beach, CA) was
1963). The wire leads passed subcutaneously to an acrylic skull explant
that was anchored to the skull with T-shaped stainless-steel bolts. To
permit access to the SC for single-unit recording, a stainless-steel cylin-
der, constructed to hold a small micropositioner (Narishige, Tokyo, Ja-
pan), was positioned vertically on the midline of the cranium surface at
anteroposterior stereotaxic coordinate 0 (Berman, 1968).
To determine by antidromic stimulation whether the collicular cell
being recorded was a tectoreticular neuron, we implanted into the pre-
100; Kopf, Tujunga, CA), which was fixed to the explant. This electrode
was lowered into the brainstem at an angle of 20–30° posterior to the
frontal plane, to a site within the predorsal bundle just rostral to the
abducens nucleus (stereotaxic coordinates, posterior, 5.5; horizontal,
?5.0; mediolaterial, 0) (Berman, 1968). The final stimulating-electrode
ing, the electrode position was adjusted such that a recording microelec-
trode in the SC could record antidromically activated SC cells and/or
strong evoked potentials.
The connectors for the eye coil, the recording cylinder, and the stim-
ulating electrode were embedded in the explant. A screw, attached to the
explant, held a second search coil used to measure head movements. A
thin stainless-steel U-shaped crown was also embedded in the posterior
perimeter of the explant for the purpose of attaching the cat’s head to a
universal joint, itself attached to a freely rotating vertical shaft (see Be-
or cefazolin (35 mg/kg) was administered as a prophylactic measure
against infection. This treatment was continued on a daily basis for 10
postoperative days. At the end of the surgery, an analgesic medication
(buprenorphine hydrochloride; 0.01 mg/kg) was given and continued
for 2 d. Cats recovered for at least 10 d before experimental procedures
oped in a loosely fitting cloth bag and placed in an open-top box that
gently restrained its body and limb movements. The animal box allowed
full ranges in horizontal and vertical-up head motion except for down-
ward head motion, which was restricted to ?35° below normal head
posture. The U-shaped crown in the explant was attached, via two uni-
versal joints, to a vertical shaft rotating in low-friction bearings. The
double universal joints permitted about ?30° of vertical head motion
and minimized constraint on the animal’s orienting behavior in the
earth-horizontal plane, which is what we focused on here. Our previous
(Bergeron and Guitton, 2000, 2002). To perturb a horizontal gaze shift
in-flight, the rotating shaft was unexpectedly halted by a friction clutch,
onset of head motion (determined by a velocity threshold).
To obtain memory-guided gaze shifts, we used a barrier paradigm
(Munoz and Guitton, 1991). A cat faced an opaque barrier of variable
width (40–60°) directly in front at a distance of ?35 cm. Initially, in a
trial, there was no target of significance to the cat. A small food target on
redirected its visual axis to the target and was fed. To obtain the time of
target appearance, the rapidly moving food target intercepted infrared
detectors located on the edges of the barrier, which generated a marker-
measured using a search coil attached to the food holder. This coil was
sensitive to the translational motion of the target, because it moved far
from the center of the field coil assembly in a path where the horizontal
magnetic field was not uniform. The calibration of this coil signal was
Using these two methods, our estimate of time of target appearance was
within ?3 msec.
The barrier paradigm permitted a wide range of gaze shift amplitudes
gaze shift required to fixate the target depended on the initial gaze posi-
fluorescent light with very fast decay time (?100 ?sec). To obtain gaze
shifts in complete darkness, to the remembered location of the target,
ambient lighting was extinguished for 1 sec beginning 120 msec after an
infrared detector was triggered by the passing food target. Gaze shifts in
the light were obtained by keeping ambient lighting on. The occurrence
the barrier and the location where the target appeared.
We recorded cell activity in four randomly interposed trial types: the
cat oriented in either the light or dark and with or without a head brake.
In 20 and 80% of the trials, the cat oriented in the light and dark, respec-
and light trials for durations ranging from 50 to 300 msec.
electrical stimulation (train duration, 300 msec; pulse width, 300 ?m;
frequency, 300 Hz; current, 5–30 ?A) (Pare ´ et al., 1994). The organiza-
tion of the map was deduced on the basis of the amplitude and direction
of gaze shifts evoked at different electrode positions (Pare ´ et al., 1994).
With this method, it was possible to predict the stereotaxic location of
both the fixation zone in the rostral SC, and the locus of points that
encoded horizontal gaze shifts. We then confirmed these locations by
applying electrical stimulation and verifying that (1) for the fixation
zone, gaze shifts could be interrupted, and (2) for the motor map, stim-
ulation at different points along the predicted horizontal meridian
evoked horizontal gaze shifts.
the dorsal surface of the SC. The neurons we describe here presented the
pattern of firing frequency previously described in our previous studies
of identified tectoreticular neurons (Munoz and Guitton, 1991; Munoz
et al., 1991a,b; Bergeron and Guitton, 2000, 2002; Bergeron et al., 2003).
this was the following: (1) a low-frequency prelude of activity that began
of the gaze shift, (2) a subsequent decline of firing frequency to zero at
about the end of the gaze shift, (3) an open-ended movement field,
meaning that the cell discharged for all of the movements larger than its
optimal, and (4) for large gaze shifts, a peak discharge in cells of the
rostral one-half of the SC that lagged gaze shift onset. Some of these
criteria are in accordance with other descriptions of cat tectoreticular
neurons projecting from the collicular motor map (Grantyn and
Berthoz, 1985; Olivier et al., 1993). In addition, we verified in cat W
whether the recorded cells were tectoreticular neurons by stimulating
antidromically the main descending axons from the SC, at a site in the
predorsal bundle just rostral to the abducens nucleus (see Animal prep-
aration). Stimulation consisted of a biphasic current pulse (30 ?A) that
Matsuoetal.•GazeFeedbacktotheCatSuperiorColliculusJ.Neurosci.,March17,2004 • 24(11):2760–2773 • 2761
was isolated from ground (S88, PSIU 6; Grass, Quincy, MA). The anti-
dromic nature of the evoked spike was determined according to the
criteria described by Lipski (1981). Cells identified as tectoreticular neu-
rons are indicated in Table 1.
As described in our previous studies (Munoz et al., 1991b; Bergeron
and Guitton, 2000, 2002; Bergeron et al., 2003), but contrary to Peck
(1987), we did not encounter the typical burst cells frequently observed
in the monkey’s SC, which have closed movement fields and a strong
(for review, see Moschovakis et al., 1996; Scudder et al., 2002).
our recordings to the zone encoding horizontal gaze shifts. This was
nearly horizontal saccadic gaze shifts. For example, stimulating the site
Figure 1B shows the vectors evoked at the sites where we recorded neu-
rons that form the database for this paper. Cells K2, K2A, and K10, used
as major examples in this paper, are specifically identified.
SCFNs previously (Munoz and Guitton, 1991; Bergeron and Guitton,
2000, 2002), which provided the following criteria, used here, to identify
these cells: (1) SCFN tonic activity increases when the cat actively fixates
a visible target; (2) this activity persists when the target momentarily
disappears but the animal maintains fixation in the dark; (3) the tonic
saccades; (4) at the end of primarily contraversive gaze saccades to a
target, the tonic activity of most cells exceeds that at the start, even if the
cat SCFNs are tectoreticular neurons.
Data analysis. During the experiments, action potentials were con-
verted to logic pulses via a time–amplitude window discriminator (BAK
Electronics, Mount Airy, MD). The target, eye and gaze positions, cell
were stored on DAT tape (RD-200T; Teac, Montebello, CA) for off-line
analysis. The gaze and head coils gave signals proportional to eye and
head positions in space, respectively. [Horizontal gaze (G) ? horizontal
eye position in space ? horizontal eye in head (E) ? horizontal head in
in magnetic-field technique (Robinson, 1963) have been reported previ-
ously (Guitton et al., 1984). In off-line analysis, using the data stored on
at 1 kHz and digitized at 2 kHz with data acquisition software and sub-
sequently analyzed with MatLab (MathWorks, Natick, MA). The start
and end of saccadic eye and gaze movements were determined by a
velocity threshold corresponding to velocity of 25°/sec. For head move-
ments, the criterion was that velocity ? 15°/sec. In brake trials, we mea-
sured gaze plateau duration as follows. The beginning of the plateau
corresponded to when the velocity of the first gaze saccade dropped to
25°/sec. The end of the plateau was when the velocity of the corrective
saccade reached 25°/sec.
During an experiment, contact with a cell was frequently lost, partic-
ularly during brake trials, and this imposed serious limitations on the
number of cells per cat available for analysis. For a cell to be retained for
a comparative analysis of brake and control trials (Table 1), we required
that there be at least four large (?50°) control single-step gaze shifts and
condition. This was in addition to the data on the discharge characteris-
tics of the cell during multiple-step gaze shifts that we needed to accu-
rately localize the cell on the SC map (see Calculation of the spatial
(Table 1): 13 cells in cat K, 1 cell in cat S, and 6 cells in cat W. An
is given in Materials and Methods. Note that fixation cells are placed at 0 mm, but in our analysis of the spatial
firing frequency occurs during single-step gaze shifts. GI, Gaze shift interrupted by stimulation; NC, value not
pulses (300 Hz; 300 msec duration) was delivered to the left SC at the position of cell K2.
Gaze saccades evoked by stimulating the SC. A, A train of rectangular cathodal
2762 • J.Neurosci.,March17,2004 • 24(11):2760–2773 Matsuoetal.•GazeFeedbacktotheCatSuperiorColliculus
of two cats, three cells in cat N, and two cells in cat W. We described
previously (Bergeron and Guitton, 2000, 2002; Bergeron et al., 2003), in
relation to variations in GPE during multiple-step gaze shifts, the dis-
charge characteristics of 3 of 5 of our SCFNs and 15 of 20 of our cells on
the motor map. The new cells in this report are marked NC in the
GPEOmsgscolumn in Table 1.
In cat W, one SCFN and three of the six cells that we studied in detail
on the motor map were tectoreticular neurons identified antidromically
as projecting to the reticular formation (Table 1). Note that there have
been very few studies of the discharge properties of identified collicular
output neurons in the alert animal. Our identification of these neurons
provides important insight into the type of signals sent by the SC to
downstream pontine circuits. The exact proportion of cells that were
collicular output neurons is difficult to state because of the inherent
experimental difficulties in identifying tectoreticular neurons in the
head-free cat, namely, variability in the long-term reliability of the stim-
ulating electrode as well as the possibility that a cell in the SC sends its
axon through a part of the predorsal bundle far from the tip of the
2002; Bergeron et al., 2003). We believe that we underestimated the
percentage of tectoreticular neurons.
duration of the plateau. The number of spikes during a gaze shift was
obtained in the period 10 msec before gaze shift onset to 10 msec before
end. Other specific measures are given in Results. Spike density histo-
grams were generated in most cases by substituting for each spike a
Gaussian function with a width of 10 msec (MacPherson and Aldridge,
1979; Richmond et al., 1987) and then summing all of the Gaussians
together to generate a continuous function in time (spike density histo-
gram). However, in those analyses in which we needed to calculate short
latencies, we reduced the Gaussian width to 4 msec (see Fig. 3B,C) to
increase the low-pass filtering cutoff frequency.
We showed in previous publications that, in cat SC, tectoreticular
neurons encode GPE (Munoz et al., 1991a,b; Bergeron and Guitton,
2000, 2002; Bergeron et al., 2003). To examine this relationship in the
present situation, we aligned, for any one cell, the gaze shifts in control
1° steps) of GPE in the range from the largest gaze shift amplitude avail-
able (?50°), in at least four trials, to 0°. We then calculated the mean
firing frequency in each ?GPE ? 1° bin, which permitted us to generate
a phase plane plot of firing frequency versus GPE. We also calculated
phase plane plots for brake trials by cutting out the plateau (constant
GPE) portion of the perturbed gaze trajectory and the corresponding
segment of the firing-frequency profile. We analyzed separately the pla-
teau discharges. To compare phase plane plots in the control and brake
trials, we used the two-sample Kolmogorov–Smirnov goodness-of-fit
hypothesis test (K–S test).
Calculation of the spatial distribution of activity on the SC map. To
ied with GPE across our population of cells on the SC map (see Fig. 11),
of firing frequency versus GPE for single-step gaze shifts, the firing fre-
quency at its peak (GPEOcontrol) and at GPE of 40, 10, and 0°. We chose
10°, because cells at this location are physically about midway between
frequency at each GPE by dividing by the peak response of the cell, at its
optimal GPE. Third, for each value of GPE, we plotted the normalized
firing frequency of each cell versus its position on the map (see next
(Bergeron and Guitton, 2002).
could be either of the following two values: (1) GPEOstim, the mean gaze
amplitude obtained by stimulating the recording site, or (2) GPEOmsgs,
for multiple-step gaze shifts, the GPE at which peak firing frequency
occurs in the phase plane plot of firing frequency during an intersaccade
gaze plateau versus the GPE of the plateau (Bergeron and Guitton, 2000,
2002; Bergeron et al., 2003).
We showed previously (Pare ´ et al., 1994; Bergeron et al., 2003) that a
gaze saccade evoked by stimulating a given site has, on average, a vector
similar to that deduced from the discharge properties, of a cell recorded
at that site. Indeed, for our cells on the motor map, the relationship
between GPEOstimand GPEOmsgs(Table 1) was excellent: GPEOstim?
(0.99 ? GPEOmsgs) ? 4.62; r ? 0.96. In Bergeron et al. (2003), we also
verified that GPEOmsgswas similar to that obtained by measuring the
retinotopic location of the optimal visual response of a cell. Note that
experiments from the GPE at which peak firing frequency occurs in the
phase plane plot (see Fig. 10) of firing frequency versus GPE for single-
shifts, was linearly related to, but ?20% less than, the optimal GPE
calculated from multiple-step gaze shifts. We cannot explain this differ-
firing frequency may be more accurate than for single-step control gaze
need to be concerned with time delays between cell firing and GPE.
Indeed, the GPE of a given gaze plateau is constant, and the plateau lasts
generally ?125 msec; mean firing frequency in the plateau can be esti-
mated reliably by counting spikes.
We had data from 24 of 25 cells in Table 1 from which to estimate the
pattern of discharge on the SC map during large single-step control and
braked gaze shifts. (We had no control gaze shifts of the appropriate
amplitude for cell W113C.) We could not calculate GPEOmsgsfor five
cells on the motor map. We estimated their position in Figure 11G–I
An accurate estimate of the spatial pattern of discharge on the collicu-
lar map benefits from data from as many cells as possible. Therefore, to
improve our estimate in the control condition, we used a group of 10
had no brake data for these 10 extra cells. Seven of them were studied in
cats M and P, not used in the brake studies. Seven (not the same as the
seven in the preceding sentence) of the 10 extra cells were SCFNs (cells
of 11 ? 5 trials (minimum, 4; maximum, 19). Three of the 10 extra cells
were on the motor map (cells K7a, M57a, and M58a) for which we had a
mean of 44 ? 26 trials (minimum, 19; maximum, 64). The 10 extra cells
could be localized on the map using either GPEOstimor GPEOmsgs. Thus,
to estimate the position of a cell on the collicular map, we used both
GPEOmsgs(see Fig. 11A–C) and GPEOstim(see Fig. 11D,E).
Our population of cells in two cats sampled well that part of the
collicular map that included the rostral fixation zone and a band
along the horizontal meridian lying 1.9–4.3 mm caudal to it
a region of the rostral SC ?0.5–0.7 mm long in the rostrocaudal
direction (Munoz and Wurtz, 1995b; Anderson et al., 1998). We
could not objectively assign SCFNs to specific positions within
that region. As we will see in the ensuing sections, there was an
excellent link between the discharge properties of a cell and its
location on the motor map.
turbations and the implications of these results for the feedback
control of gaze saccades, it is important to show that our cats
actually compensated for the brake-induced gaze perturbation.
Figure 2A–D shows typical examples of control and perturbed
gaze shifts, respectively, both made in the dark by cat K to the
Matsuoetal.•GazeFeedbacktotheCatSuperiorColliculusJ.Neurosci.,March17,2004 • 24(11):2760–2773 • 2763
remembered target location. The 45 and 20° control gaze sac-
well known pattern of coordinated eye and head motion (for
opposite to head motion to stabilize eye position in space. The
perturbed gaze shifts in Figure 2, C and D, are of the same in-
tended amplitude as those in Figure 2, A and B, respectively, but
gaze trace) that immobilized the head shortly after its onset. The
during the ensuing period of head immobilization, the eye re-
mained immobile in the orbit. For our entire data set on braked
movements (Table 1), the mean time between the onset of the
brake-induced head deceleration and when eye velocity became
zero (i.e., the onset of the gaze plateau) was 44.5 ? 18.6 msec.
After brake release, the head resumed its movement, and an oc-
bilize gaze, resulting in a gaze plateau of ?250 msec duration,
?200 msec longer than brake duration.
The considerable variability in plateau duration for a given
brake duration is illustrated for cat K in Figure 2F by the linear
regression line: plateau duration ? [0.85 ? (brake duration)] ?
209; r ? 0.55. For cat W, this relation was as follows: plateau
duration ? [0.82 ? (brake duration)] ? 201; r ? 0.61. The fact
that gaze plateaus were longer than brake duration can be ex-
plained as follows: (1) the rapid head deceleration truncated the
saccade by suppressing the discharge in the burst generator
(Cullen and Guitton, 1996); (2) this placed the system in the
slow-phase mode of the VOR, producing an eye rotation that
continued, the eye was driven in the contralateral direction,
thereby prolonging gaze plateau duration. Eventually, with the
corrective saccades that preceded head release were ever seen.
The accuracy of gaze shifts in the control and perturbed trials
was indistinguishable. We define gain as the ratio of overall gaze
before ambient lighting resumed—in brake trials divided by tar-
get offset angle relative to starting gaze position. We found that,
were 0.94 ? 0.089 and 0.94 ? 0.086, respectively. In cat S, these
values were 0.86 ? 0.139 and 0.86 ? 0.135, respectively. Clearly,
in all of the cats, the corrective saccades compensated in the dark
for the perturbations and brought gaze with normal accuracy to
the remembered location of the target.
In the following sections, we will first present the typical dis-
parison of the population responses in the control and brake
microstimulation delivered to the recording site of this cell in-
duced, on average, a 38° nearly horizontal rightward gaze shift.
Analysis of its discharge during multiple-step gaze shifts placed
cell K2 at the 48° location on the horizontal meridian of the SC
map (Table 1) (Bergeron et al., 2003). In the present report, we
will assume that the cell is at 48°. Note that small uncertainties in
its location are not critical in terms of distance on the SC map,
gaze shift (Fig. 2A) by ?200 msec. The activity gradually in-
creased until gaze saccade onset, and there was no distinct burst
preceding the gaze shift, although it was about the optimal am-
is frequently observed in cat tectoreticular neurons during gaze
shifts in the dark (Munoz et al., 1991b). For a smaller 20° gaze
shift, the cell had a shorter, lower-frequency discharge (Fig. 2B).
Plotting the total number of spikes in a discharge (see Materials
are vertical tic marks representing action potentials. Closed and open circles above G trace
indicate offset and onset of ambient lighting. This and all of the other illustrated gaze shifts
tude (20°). Note lower firing frequency compared with large movement. C, Discharge of cell
single-step control gaze shifts and gaze amplitude. The cell had an open-ended movement
field. F, Relationship between gaze plateau duration and brake duration. Correlation is not
2764 • J.Neurosci.,March17,2004 • 24(11):2760–2773 Matsuoetal.•GazeFeedbacktotheCatSuperiorColliculus
described by Munoz et al. (1991b).
Interestingly, the cell activity continued during the brake-
induced gaze plateaus. In the perturbed 45° gaze shift (Fig. 2C),
the firing frequency during the plateau was almost the same as
that just preceding the plateau. For the smaller movement (Fig.
2D) (about one-half of the amplitude of the optimum for that
recording site), there was a transient suppression of activity after
the brake, and activity resumed again during the plateau. In Fig-
ure 2, both C and D, firing frequency gradually decreased to near
zero during the corrective gaze saccade, similarly to that occur-
ring toward the end of the control movements. Note that the
constant tonic firing frequency during the gaze plateau in Figure
the brake nor by the ocular counterrotation (VOR) that accom-
Figure 3A generalizes these observations for cell K2 by show-
ing a series of control and perturbed large 50° gaze shifts, the
latter selected and classified according to different plateau dura-
tions. All of the trials were selected from the database such that
position at ?50° on the motor map, the
firing frequency of cell K2 reached a max-
gaze shifts. The firing rate held about
shift and then, when GPE reached ?25°,
files in the control and perturbed trials
were the same until the beginning of the
brake-induced plateaus. The important
all of the brake-induced plateaus, even if a
plateau lasted 400 msec. Furthermore, the
discharge declined to zero at the end of
These observations imply that the SC was
that the gaze shift had been interrupted
and when it was completed.
In some, not all, head brake trials, a
slight transient suppression of the dis-
charge of K2 occurred, corresponding to
the onset of head deceleration (Fig. 2D
shows one example). As a result, for this
cell, there was a shallow and brief notch in
the spike density histogram when all 35
brake trials in Figure 3A were aligned on
the onset of head deceleration (Fig. 3B).
Activity after the notch returned to the
after brake release or before the corrective
view of the discharges of all of the cells in
the caudal SC will be presented later.
istics of another cell, K10 in cat K, located at ?20° (based on
shows that the discharge preceded small 10° gaze shifts, as ex-
pected from the position of the cell on the map. We had no
control 20° gaze shifts for this cell. The discharge pattern of cell
K10 during large gaze shifts was strikingly different from that of
cell K2 in both control and brake trials. For example, in the
former, the cell had little activity preceding 50° leftward control
gaze shifts (Fig. 4C). Rather, for these large gaze shifts, the peak
firing frequency was delayed relative to gaze shift onset, a phe-
et al., 1991a,b). Plotting the total number of spikes in a burst for
all of the amplitudes shows that the cell had an open-ended
movement field (Fig. 4B). (Although we did not obtain control
single-step gaze shifts of the optimal amplitude for this cell, we
could calculate the optimal GPE using both stimulation and
multiple-step gaze shifts.)
Figure 4C compares the discharge of the cell during control
and perturbed large gaze shifts, the latter selected and classified
according to different plateau durations. We show trials with
plateaus at GPE of ?20°, close to the preferred GPE of the cell.
Note that, in all of the brake trials, the activity profile of the cell
before the brake-induced plateaus was the same as in the control
and 397 msec, respectively. Trials were also selected such that plateaus are about at a fixed position relative to the target, at
Matsuoetal.•GazeFeedbacktotheCatSuperiorColliculus J.Neurosci.,March17,2004 • 24(11):2760–2773 • 2765
movements. In all of the brake trials, there was a sharp decrease,
relative to control, in firing frequency that began just after the
brake-induced head deceleration (Fig. 4D) and gradually
dropped to zero during the longest plateaus (C, bottom trace).
Accordingly, the time at which activity reached a minimum in-
creased with plateau duration. Activity increased after the mini-
mum, in relation to the time of occurrence of head acceleration
(Fig. 4E). Firing frequency reached its maximum at about the
middle of the 30° corrective saccades (Fig. 4F). (The location of
peak discharge will be considered in more detail subsequently in
relation to Fig. 11.)
The firing-frequency profile of cell K10 contrasts with that of
cell K2 recorded more caudally in that the latter maintained a
nearly steady tonic discharge during plateaus. Nevertheless, the
overall discharge duration of cell K10, measured from gaze shift
Figure 5 shows the activity of a collicular fixation neuron (SCFN
N42a) during a large gaze shift made by cat N in a direction
contralateral to the recording site. This cell was located in the
rostral pole of the right SC. The cell had a low discharge at the
start of the trial (Fig. 5A) when the cat faced the blank opaque
barrier. The firing of the cell paused completely, shortly after
target presentation, and resumed during the gaze shift.
The pause clearly was prolonged when the gaze trajectory was
perturbed in midflight, at the time at which the cell was already
silent (at GPE of 30° in this example). In previous studies of
natural multiple-step gaze shifts, we found that the first spike
after the pause is determined by when gaze arrives at a particular
distance from the target, on average when GPE ? 13° (Bergeron
and Guitton, 2000, 2002). In the present example, cell N42a be-
gan to fire, after the pause, on average at GPE of ?20° in both
control and brake trials. After the pause, the firing frequency
on their end (Fig. 5B) showed that firing frequency peaked very
turbed gaze shifts. A, Ten degree gaze (G) shifts and associated cell discharge. B, Number of
spikes in a discharge versus gaze saccade amplitude. Cell discharges for all of the gaze shifts
large gaze shifts. Top traces show superimposed gaze trajectories in control trials (top gaze
illustrated gaze traces have gaze plateau durations with means of 175, 243, and 321 msec.
plateau durations. All of the traces aligned on gaze onset (left vertical dotted line). Onset of
trials, arrows on spike density histograms indicate average time of onset of corrective gaze
gaze saccade. Overall discharge duration increased with plateau duration. D, Effect of brake.
end of plateaus. B, Traces aligned on gaze shift end. Note that activity peaks at end in both
2766 • J.Neurosci.,March17,2004 • 24(11):2760–2773 Matsuoetal.•GazeFeedbacktotheCatSuperiorColliculus
not test whether firing frequency during brake-induced plateaus
depended on GPE, as in Bergeron and Guitton (2000, 2002),
because most brake trials occurred during the pause in activity,
and, by extension, we obtained too few brake trials in which gaze
was immobilized after the pause in activity had ended.
In this section, we expand on the examples shown in Figures 3–5
for the purpose of introducing specific properties of the spatio-
temporal discharge pattern on the SC map that will be addressed
more quantitatively in subsequent sections. Figure 6 compares
(five in cat K and four in cat W) whose positions on the map
spanned the distance between the rostral and caudal ends of the
SC. This figure and the preceding Figures 2–5, showing cells K2,
K10, and N42a, together illustrate the discharges of 12 of our 25
cells. As in Figures 3–5, we show the firing-frequency patterns
during large (?50°) gaze shifts.
Cells in each row of Figure 6 were recorded at about similar
locations on the motor map in each cat. We had neither fixation
neurons in cat K, nor neurons in the very caudal SC in cat W; all
were lost in brake trials. Plateau duration varied from cell to cell,
because we retained brake trials only when at least four plateaus
ing a firing-frequency histogram, and sometimes this could be
obtained only for a limited range of plateau durations. An im-
pression of the differences in the activity patterns in the rostral
scanning each column in Figure 6 from top to bottom.
those we described previously on numerous occasions and are
compatible with the moving-hill hypothesis. This can be appre-
ciated by considering the timing of the peak discharge relative to
just below the gaze traces in each panel. Thus, for caudal cells
on horizontal line) occurred close to the onset of the 50° gaze
shifts (Fig. 6A5). In comparison, for rostral cells (top of Fig. 6),
the peak of the control activity lagged gaze shift onset (Fig.
6A1,2), and occurred progressively closer to gaze shift end as the
cell lay nearer to the rostral pole of the SC (to be considered in
more detail later in Figs. 10 and 11). This discharge pattern—the
delayed burst in the rostral SC during large gaze shifts—is neces-
sary (but not sufficient) in the moving-hill hypothesis.
The fact that control and brake trials had similar initial dis-
the animals could not predict in which trials the brake would be
applied. In general, for large gaze shifts, activity at the start of
plateaus, having GPE of ?25°, was as follows: low for cells in the
rostral SC at ?0–15° on the map (e.g., cells K6a and W51), high
for cells in the middle SC at ?20° (e.g., cells K7, W110, and
W112d), and low again for very caudal cells at ?60° (e.g., cell
K2a). The latter is particularly striking. The large (?50°) gaze
and the firing-frequency profile appropriately rose to a maxi-
mum at gaze shift onset and declined as it progressed. Thus, the
firing frequency of K2a had declined substantially when the pla-
teau began, and it continued to decline after the brake and for
?50 msec after plateau onset. The discharge held about steady
during most of the remaining plateau, as in K2, and declined to
in the caudal SC (K5, K9, and K9a; not all shown in Fig. 6) had
variable rates of decreasing firing frequency during plateaus,
ranging from no decline in cell K5 to moderate in K9 (Fig. 6A4)
In comparison, for cells in the middle SC (W112d, W110, K7,
and K10), all at about the 20° location, the firing frequency de-
creased after the head brake and rose again during the plateau
before the onset of the corrective gaze saccade. The rate of de-
crease in firing frequency varied between cells; compare K7 and
W112d (Fig. 6). As in K10 (Fig. 4), the decrease in firing of most
middle-SC cells was interrupted by the increasing discharge,
linked to the onset of corrective gaze saccades.
their rostrocaudal location on the map. Each panel shows the mean control gaze (G) profile
(dashed line) and some superimposed brake trials, selected to have about constant plateau
cut out and the two ends slid toward each other. For most cells, these are similar to control
Matsuoetal.•GazeFeedbacktotheCatSuperiorColliculusJ.Neurosci.,March17,2004 • 24(11):2760–2773 • 2767
Despite differences in the postbrake firing-frequency profiles of
cells in the middle and caudal SC, the discharge frequency was
nearly the same at the start and end of plateaus. To show this, we
Recall that, on average, brake and plateau onsets were separated
by 44.5 ? 18.6 msec. We selected brake trials in which plateaus
were at least 220 msec long (mean, 255 ? 62 msec). We did not
analyze activity in the period beyond 120 msec after plateau on-
set, because, in the middle SC, the rising activity levels that pre-
ceded the corrective gaze saccades started ?100 msec (Fig. 4F)
before plateau end. Figure 7 shows normalized (relative to the
mean activity level in the 20 msec period just preceding brake
onset) mean population activity levels in the periods: 0–20 msec
after brake onset, ?20 to 0 msec before plateau onset, and at
various time intervals after plateau onset including plateau end.
Activity in middle-SC cells kept increasing after brake onset.
As we shall see later in relation to Figure 10, B and C, this was
eye motion, which, for these large gaze shifts, reduced GPE and
increased firing frequency. At about plateau onset, activity in
middle-SC cells began decreasing until ?40 msec after plateau
onset, followed by a steady discharge (Fig. 7). At plateau end,
ing GPE (see Fig. 10D,E). After plateau onset, activity levels kept
decreasing slightly to reach a steady level ?15% lower at plateau
end than at plateau onset (Fig. 7). However, this difference was
a gaze plateau was 49 ? 16 spikes/sec compared with 48 ? 12
spikes/sec in the final 20 msec period at the end of a plateau.
These means are not significantly different ( p ? 0.05).
On the basis of these results, it follows that, when the plateau
portion of every perturbed gaze trajectory was cut out, and the
onset, and averaged (thick black profiles in each panel of Fig. 6),
the reconstituted firing-frequency profiles of 23 of 24 cells (cell
control profiles ( p ? 0.05; K–S test).
An assessment of the effect of the brake, applicable to most cells,
each cell (Materials and Methods) and comparing the control
for each cell, was about as long as control gaze shifts (mean pla-
K8), located rostral of the middle SC, there were more spikes in
the brake than in the control trials (Fig. 8, filled circles). The
increase in number of spikes for most cells occurred, because
plateaus provided an added discharge. For brake trials, in all of
the cells, the number of spikes resulting when the plateaus were
cut out resembled that in the control trials (Fig. 8, open circles).
The reason rostral cells K6a and K8 did not show an increased
spike count in brake trials can be easily appreciated from Figure
6A1 showing the discharge of cell K6a. Because peak activity in
control trials lagged gaze onset for this cell, there was a low-
frequency discharge at plateau onset and during the ensuing pla-
Behaviorally, the effect of the brake was to delay the time,
relative to control trials, at which gaze acquired the target. The
increased spike count was associated with a prolongation in the
trials to achieve the end of discharge. For example, for cell K2
(Figs. 2, 3), the overall discharge duration, measured from 10
msec before gaze onset to when activity decreased to 30% of its
peak, was proportional to plateau duration (Fig. 9A). For the 12
caudal cells located 3 mm and more caudally in the SC (Table 1),
levels in the 20 msec period before plateau end are shown to far right. Short vertical lines
and end of plateaus were equal despite a transient decrease during the plateau. See Activity
ods). Filled circles show data for brake trials selected such that plateau duration was ?250
2768 • J.Neurosci.,March17,2004 • 24(11):2760–2773 Matsuoetal.•GazeFeedbacktotheCatSuperiorColliculus
follows: durationdischarge? [(1.11 ? 0.23) ? durationplateau] ?
(123.8 ? 114.1); mean r ? 0.81 ? 0.14. All of these neurons
showed a significant linear regression correlation coefficient of
in the middle SC, because there were two peaks in the discharge
zero (Fig. 4C, bottom trace).
tor map, the gaze shift-related silence of fixation cells increased
during brake trials. For example, fixation cell N42a (Fig. 9C)
the time between onset of the gaze shift and when the activity of
this neuron had resumed and built up to 70% of its peak value,
the latter measured at gaze shift end. This relationship between
gaze plateau duration and pause duration had a positive signifi-
mean regression line was as follows: durationpause? [(1.0 ?
[Recall that one of the two SCFNs in cat W was identified as a
tectoreticular neuron (Table 1).]
In the moving-hill hypothesis, the spatiotemporal pattern of fir-
ing frequency in the population of cells on the SC map encodes
where gaze is relative to the ultimate goal of the gaze shift. This is
implemented on the SC map by displacing, as a function of GPE,
gaze shift varying as a function of GPE, independent of whether
the gaze shift is made as a single-step or as a multiple-step se-
quence. This phenomenon also holds true for the present data.
of firing frequency versus GPE for five cells ranked from top to
preferred GPEs of caudal cells K2 and K2a (Fig. 10D,E) were 48
and 58°, respectively, calculated from multiple-sep gaze shifts,
but we could not obtain enough larger single-step control gaze
drop off as GPE increased, thereby demonstrating a clear peak in
this condition (Bergeron et al., 2003).
cutting out both the plateaus in gaze trajectories and the corre-
sponding time period in the firing-frequency histograms. This
procedure assumes continuity in firing frequency between pla-
analysis of plateau firing frequency in Figure 7. The GPE of each
plateau varied from trial to trial, and the mean ? 1 SD is marked
in each panel by the solid circle and the intersecting horizontal
dotted line. For cell K2 (Fig. 10D), we had enough brake trials to
permit a comparison between the mean phase plane plots for all
of the brake trials combined (solid line) with a subgroup of trials
having a narrower distribution of plateau GPEs (dotted line and
dark circle labeled Brake 2).
A K–S test (Materials and Methods) showed that the phase
peak discharge. Linear regression correlation coefficient r ? 0.84. B, Regression lines of dis-
29 ? 3° (dotted line), a narrower range than for the solid line. Note for each panel that the
phase plane plots in each condition are statistically identical (Materials and Methods) ( p ?
Matsuoetal.•GazeFeedbacktotheCatSuperiorColliculusJ.Neurosci.,March17,2004 • 24(11):2760–2773 • 2769
plane plots for the control and cut-out
perturbed gaze shifts were identical ( p ?
0.05) for all of the SCFNs and for 17 of 20
cells on the motor map. No cell illustrated
in Figure 10 had significant differences.
That the control and brake trial plots are
and end. This property is particularly
striking for those cells in the middle SC
(Fig. 9B,C) for which firing frequency
during plateaus was not constant. The
lower-than-control (but nonsignificant)
firing frequency in the postplateau phase
of caudal cells K2 and K2a of Figure 10 is
typical of events in the caudal map.
The fact that the phase plane plots in
control and brake trials were similar, once
needs to be interpreted in light of the ob-
servation that the gaze trajectories in the
control and cut-out brake trials were also
similar in the time domain (Fig. 6). In-
deed, if the firing-frequency profile can
vary with both time and GPE, then what is
the relevant dependence? We will show in
the next section that the moving-hill hy-
pothesis unifies the different time- and
GPE-dependent discharge properties of a
We now show (Fig. 11) that the distribu-
tion of activity on the collicular map dur-
ing a hypothetical 40° single-step control
gaze shift and a braked 40° gaze shift sup-
ports the moving-hill hypothesis (Munoz
et al., 1991a,b). For these calculations, we
first determine the location of each cell on
the collicular map on the basis of its pre-
ferred GPE (Materials and Methods).
Given the controversy of the moving-hill
hypothesis, we compared, for cells on the
motor map, the outcome of using two dif-
ferent estimates of GPE: (1) in Figure 11A–C, from the GPE at
peak firing frequency in the gaze position plateaus of multiple-
step gaze shifts (Table 1, GPEOmsgs) (Table 1), and (2) in Figure
11D–F, from the mean amplitude of the gaze shift evoked by
stimulating the recording site (Table 1, GPEOstim).
Regarding SCFNs, note that the extent of the collicular fixa-
tion zone is unknown and might encompass a rostral zone 0.5–
0.7 mm long in the rostrocaudal direction (Munoz and Wurtz,
a zone 0–0.5 mm long, and accordingly, we assigned to them
random positions within this space along the horizontal merid-
significantly alter the conclusions of this section (data not
To calculate the position of a cell using GPEOmsgsin the con-
1 and 10 extra cells (Materials and Methods). For the same cal-
For each cell in Figure 11A–F, we obtained the firing fre-
10) (Materials and Methods). The best-fit Gaussians to the data
points in Figure 11, A and D, show that, at the onset of a control
40° gaze shift, activity was located at a site in the caudal SC ap-
propriate for driving the entire movement. This is entirely con-
sistent with classic views of SC function. At GPE of 10° (Fig.
11B,E), activity in both the rostral and 2–3 mm zones had in-
creased, whereas that in about the 3.5–4.3 mm zone had de-
had increased further, and that in about the 2.5–4.3 zone had
decreased even more, with the result that peak activity was ap-
proximately centered on the rostral fixation zone. The fact that,
in the latter panels, the Gaussian was not quite centered at zero,
when GPE ? 0°, presumably was caused by noise in the best-fit
2770 • J.Neurosci.,March17,2004 • 24(11):2760–2773 Matsuoetal.•GazeFeedbacktotheCatSuperiorColliculus
procedure. The choice of GPE ? 10° was quite arbitrary, and we
obtained similar results using different GPEs.
These calculations show that, in Figure 11, A–C and D–F, the
peak of activity moved progressively rostrally to different rostro-
caudal locations for the three successive GPEs. The Gaussian
curves were statistically indistinguishable in the two approaches
to localizing the cells, as can be seen by visually comparing the
solid and dotted profiles in A and D, B and E, and C and F. Thus,
the spatial distribution of firing frequency was indifferent to the
method used to localize cells. It follows that activity during a
control single-step gaze shift in cat moved continuously on the
map in the caudorostral direction, from gaze shift start to finish,
Unfortunately, we lacked a sample of cells in the 0.5–2 mm
zone, and our conclusions are based on the assumption of conti-
nuity between the properties of SCFNs and cells on the motor
of cells in the 0.5–2 mm zone—if we had them—would have
provided contradictory evidence, for two reasons: (1) in our ini-
covered the entire map, including this zone, and continuity of
properties was observed (Munoz et al. 1991a,b); (2) during
multiple-step gaze shifts, there is continuity between the dis-
charge properties of SCFNs and cells on the motor map
(Bergeron and Guitton 2000; Bergeron et al., 2003).
The distributions of activity on the map in Figure 11G–I were
calculated using data from brake trials only. (We included the 24
cells in Table 1 for which we had both control and brake data.)
The mean values of GPE and their associated mean firing fre-
quency for the brake trials were taken from data in which the
plateaus had been cut out, as in Figure 10. Cells were localized
using GPEOmsgswhen available (Table 1, 19 cells), but if this
shows that activity during a brake trial behaved similarly to con-
trol trials and moved continuously rostrally on the map begin-
ning at a caudal starting position encoding overall gaze shift am-
plitude. Given that activity at plateau end equaled that at plateau
start (Fig. 10), we conclude that the caudorostral movement
stopped during a plateau and resumed moving rostrally at the
end, activity in primarily the middle region of the map under-
went a transient modulation not shown in Figure 11G–I.
Note that the moving-hill hypothesis unifies the different
time- and GPE-dependent discharge properties of a cell (Figs. 6,
10). The position on the map of the peak of the hill encoded the
current GPE, independent of the temporal profile of a trajectory,
kinematic properties of the translational motion of the locus of
activity on the map.
There is now considerable evidence supporting the hypothesis
that saccadic gaze shifts made with coordinated eye–head move-
ments are driven by an error signal (GPE) derived from a gaze
feedback loop that compares the current gaze vector with the
desired vector (for review, see Scudder et al., 2002; Guitton et al.,
2003a,b). One test of this gaze feedback hypothesis is to perturb,
unexpectedly to the subject, gaze trajectories made in the dark
that gaze accuracy remains unaltered relative to control. Such
experiments have been done in cat, monkey, and humans (for
review, see Guitton et al., 2003a,b). The accurate corrective gaze
saccades in the present head brake experiments provide not only
additional behavioral support for the gaze feedback control con-
head perturbations were obtained in the context of an opera-
tional feedback system.
Keller (1981) first proposed that the SC in the head-fixed pri-
mate is within an eye saccade feedback loop. This concept has
been tested in the head-fixed monkey by perturbing saccade tra-
jectories and examining whether cell discharges respond to per-
turbations and correlate to compensatory movements. The re-
sults are controversial. For example, eye blinks result in
concurrent changes in both saccade trajectories and collicular
saccade-related discharges (Goossens and Van Opstal, 2000a,b).
Saccades do compensate for blink-induced perturbations, but
such observations have been explained by suggesting that blink-
cells, and that the internal circuitry of the SC emits a site-specific
constant number of spikes without receiving feedback from the
ing an increased number of spikes in brake trials (Fig. 8) opposes
this assumption for perturbed gaze shifts.
SC, saccades have been interrupted by electrically stimulating
(for review, see Scudder et al., 2002). After the cessation of stim-
ulation, accurate corrective saccades were generated. The dis-
charge of collicular burst neurons was interrupted by stimula-
tion. Activity resumed at the same SC site just before and
synchronously with the corrective saccade. In comparison,
?30% of the collicular buildup neurons were not suppressed by
stimulation, and their activity continued tonically throughout
the interruption period. These results have been used to support
Keller et al., 2000) but were unclear regarding what feedback
In comparison, Soetedjo et al. (2002a) slowed saccades by
deactivating the primate omnipause neuron area using pharma-
cological techniques. The reason saccades were slowed is un-
longed, showing that the SC received information about the
slowed trajectory. The authors argued that feedback to the SC
encodes saccade end, not motor error.
In summary, the results of different experiments that per-
the on-line feedback control of eye saccades. One reason for the
debate is that the technique of perturbing saccade trajectories in
the head-fixed primate is subject to artifacts. For example, in the
electrical stimulation experiments, neurons that project to the
stimulated site and that themselves are involved in driving the
movement can be directly affected by stimulation (e.g., anti-
dromically). Such problems are avoided when head-free gaze
life phenomenon experienced in many sporting activities that
require precise visuomotor control.
Using head brakes, we provided in this paper the following
evidence for gaze feedback to the cat SC. First, for virtually all of
the cells on the map, the discharge pattern in perturbed move-
was informed about the perturbation). Second, the pause in
Matsuoetal.•GazeFeedbacktotheCatSuperiorColliculusJ.Neurosci.,March17,2004 • 24(11):2760–2773 • 2771
9C,D). Third, the discharge of cells on the motor map was pro-
spikes emitted by a cell was greater than control and increased
with plateau duration (Fig. 8). In comparison, when the number
of spikes in the plateaus was subtracted out, the total number of
spikes emitted in the perturbed and control conditions became
about equal (Fig. 8).
Recall that the cells we describe here had discharge properties
similar to those of cat tectoreticular neurons (Grantyn and
Berthoz, 1985; Munoz et al., 1991b; Olivier et al., 1993), and we
verified this in cat W in which we antidromically identified some
cells as tectoreticular neurons. Therefore, feedback occurred on
collicular output cells.
Although the brake experiments demonstrated feedback to the
cat SC, the question arises as to whether this feedback imple-
mented the encoding of GPE via the moving-hill phenomenon.
In this model, derived in the head-unrestrained cat, the locus of
centered on the appropriate instantaneous GPE [modeled by
Lefe `vre and Galiana (1992)]. The gaze shift ends whenever
zero of the map, the rostral pole of the SC where SCFNs are
The present control discharge patterns are compatible with
this model. Indeed, an analysis of the spatial distribution of the
population discharge on the map showed that the locus of the
who studied single-step gaze shift in cat, and with Bergeron and
step gaze shifts. As a result of the moving bell-shaped hill, the
firing frequency of all of the cells (including SCFNs) presented a
stereotyped, position-dependent relationship between firing fre-
quency and GPE (Fig. 10). Furthermore, the firing frequency of
SCFNs gradually increased as GPE approached 0° and peaked at
gaze end. Finally, for large (?50°) control gaze shifts, the peak
firing frequency of cells in the middle SC was delayed (Figs. 4, 6)
relative to gaze onset.
brake was applied was the same as control. The phase plane plots
from control data in 22 of 24 cells. Thus, in most cells, the brake
and its arrest of gaze motion did not significantly modify the
postplateau neural activity relative to control gaze shifts at the
same GPE. In spite of the fact that, for some cells, the activity
during plateaus was not constant, the population activity at the
very end of a plateau, for both middle and caudal cells, was equal
tive gaze saccade, was at control values determined by GPE. The
results imply that, in brake trials, the rostrally moving hill must
have stopped during plateaus. Our analysis showed further that
the progression of activity on the map was similar in multiple-
step gaze shifts (Bergeron et al., 2003) and in the present brake
and artificially interrupted gaze shifts.
By analogy with the moving hill in cat initially described by Mu-
noz et al. (1991a,b), Munoz and Wurtz (1995b) described for
neuron layer toward the rostral pole of the SC as the saccade
layer remained topographically immobile during a saccade. Ros-
in experiments involving the simultaneous recording of activity
enon encoded was not clear. No other investigation has suc-
ceeded in showing significant rostral movement of the locus of
activity during eye saccades [imaging SC (Moschovakis et al.,
2002b)], even less the encoding of GPE. Furthermore, deactivat-
ing the rostral SC did not lead to hypermetric saccades as pre-
dicted by the hypothesis (Munoz and Wurtz, 1993; Aizawa and
Wurtz, 1998; Quaia et al., 1998). Therefore, for the head-fixed
is evidence for feedback to the SC (Keller and Edelman, 1994;
Munoz et al., 1996; Keller et al., 2000; Soetedjo et al., 2002a),
which the latter authors have suggested controls saccade termi-
nation. By extension, in the head-unrestrained monkey, we pro-
vided preliminary evidence, using the same experimental tech-
nique as here (Choi and Guitton, 2002; Guitton and Choi, 2002;
Guitton et al., 2003a,b), that there is gaze feedback to the SC
during brake-induced gaze plateaus. However, evidence for a
moving locus of activity that encodes GPE in the head-
unrestrained monkey, if it exists, is far less striking than in cat.
original insights into collicular function.
Aizawa H, Wurtz RH (1998) Reversible inactivation of monkey superior
colliculus. I. Curvature of saccadic trajectory. J Neurophysiol
Anderson RW, Keller EL, Gandhi NJ, Das S (1998) Two-dimensional
saccade-related population activity in superior colliculus in monkey.
J Neurophysiol 80:798–817.
Bergeron A, Guitton D (2000) Fixation neurons in the superior colliculus
encode distance between current and desired gaze positions. Nat Neuro-
Bergeron A, Guitton D (2002) In multiple-step gaze shifts: omnipause
gate saccades. J Neurophysiol 88:1726–1742.
Bergeron A, Matsuo S, Guitton D (2003) Superior colliculus encodes dis-
Berman AL (1968) The brainstem of the cat. Madison, WI: University of
Choi WY, Guitton D (2002) Discharge characteristics of saccade-related
Soc Neurosci Abstr 28:11.7.
CullenKE,GuittonD (1996) Inhibitoryburstneuronactivityencodesgaze,
not eye, metrics and dynamics during passive head on body rotation.
Evidence that vestibular signals supplement visual information in the
control of gaze shifts. Ann NY Acad Sci 781:601–606.
Feldon S, Feldon P, Kruger L (1970) Topography of the retinal projection
upon the superior colliculus of the cat. Vision Res 10:135–143.
GoossensHH,VanOpstalAJ (2000a) Blink-perturbedsaccadesinmonkey.
I. Behavioral analysis. J Neurophysiol 83:3411–3429.
GoossensHH,VanOpstalAJ (2000b) Blink-perturbedsaccadesinmonkey.
II. Superior colliculus activity. J Neurophysiol 83:3430–3452.
Grantyn A, Berthoz A (1985) Burst activity of identified tecto-reticulo-
spinal neurons in the alert cat. Exp Brain Res 57:417–421.
GuittonD (1991) Controlofsaccadiceyeandgazemovementsbythesupe-
ments (Carpenter RHS, ed), pp 244–276. London: MacMillan.
Guitton D (1992) Control of eye–head coordination during orienting gaze
shifts. Trends Neurosci 15:174–179.
GuittonD,ChoiWY (2002) Dischargecharacteristicsoffixationneuronsin
2772 • J.Neurosci.,March17,2004 • 24(11):2760–2773Matsuoetal.•GazeFeedbacktotheCatSuperiorColliculus
primate superior colliculus during head-perturbed gaze shifts. Soc Neu-
rosci Abstr 28:11.8.
Guitton D, Douglas RM, Volle M (1984) Eye–head coordination in cats.
J Neurophysiol 52:1030–1050.
Guitton D, Bergeron A, Choi WY, Matsuo S (2003a) On the feedback con-
trol of orienting gaze shifts made with eye and head movements. Prog
Brain Res 142:55–68.
Guitton D, Bergeron A, Choi WY (2003b) On the role of subcortical
feedback mechanisms in the control of gaze saccades made head-
sensorimotor integration (Hall WC, ed), pp 241–276. Boca Raton,
KellerEL (1981) Brainstemmechanismsinsaccadiccontrol.In:Progressin
oculomotor research, developments in neuroscience (Fuchs AF, Becker
W, eds), pp 57–62. New York: Elsevier/North-Holland Biomedical.
KellerEL,EdelmanJA (1994) Useofinterruptedsaccadeparadigmtostudy
spatial and temporal dynamics of saccadic burst cells in superior collicu-
lus in monkey. J Neurophysiol 72:2754–2770.
Keller EL, Gandhi NJ, Vijay Sekaran S (2000) Activity in deep intermediate
layer collicular neurons during interrupted saccades. Exp Brain Res
Lefe `vreP,GalianaHL (1992) Dynamicfeedbacktothesuperiorcolliculusin
a neural network model of the gaze control system. Neural Netw
Lipski J (1981) Antidromic activation of neurones as an analytic tool in the
study of the central nervous system. J Neurosci Methods 4:1–32.
MacPherson JM, Aldridge JW (1979) A quantitative method of computer
analysis of spike train data collected from behaving animals. Brain Res
MoschovakisAK,ScudderCA,HighsteinSM (1996) Themicroscopicanat-
omy and physiology of the mammalian saccadic system. Prog Neurobiol
Moschovakis AK, Gregoriou GG, Savaki HE (2001) Functional imaging of
MunozDP,GuittonD (1991) Controloforientinggazeshiftsbythetectore-
ticulospinal system in the head-free cat. II. Sustained discharges during
motor preparation and fixation. J Neurophysiol 66:1624–1641.
Munoz DP, Wurtz RH (1993) Fixation cells in monkey superior colliculus.
II. Reversible activation and deactivation. J Neurophysiol 70:576–589.
MunozDP,WurtzRH (1995a) Saccade-relatedactivityinmonkeysuperior
colliculus. I. Characteristics of burst and buildup cells. J Neurophysiol
MunozDP,WurtzRH (1995b) Saccade-relatedactivityinmonkeysuperior
colliculus. II. Spread of activity during saccades. J Neurophysiol
MunozDP,Pe ´lissonD,GuittonD (1991a) Movementofneuralactivityonthe
Munoz DP, Guitton D, Pe ´lisson D (1991b) Control of orienting gaze shifts
by the tectoreticulospinal system in the head-free cat. III. Spatiotemporal
Munoz DP, Waitzman DM, Wurtz RH (1996) Activity of neurons in mon-
key superior colliculus during interrupted saccades. J Neurophysiol
OlivierE,GrantynA,ChatM,BerthozA (1993) Thecontrolofsloworient-
ing eye movements by tectoreticulospinal neurons in the cat: behavior,
discharge patterns and underlying connections. Exp Brain Res
Pare ´ M, Crommelinck M, Guitton D (1994) Gaze shifts evoked by stimula-
tion of the superior colliculus in the head-free cat conform to the motor
Peck CK (1987) Saccade related burst neurons in cat superior colliculus.
Brain Res 408:329–333.
Port NL, Sommer MA, Wurtz RH (2000) Multielectrode evidence for
spreading activity across the superior colliculus movement map. J Neu-
Quaia C, Aizawa H, Optican LM, Wurtz RH (1998) Reversible inactivation
of monkey superior colliculus. II. Maps of saccadic deficits. J Neuro-
RichmondBJ,OpticanLM,PodellM,SpitzerH (1987) Temporalencoding
of two dimensional patterns by single units in primate inferior temporal
cortex. I. Response characteristics. J Neurophysiol 57:132–146.
RobinsonDA (1963) Amethodofmeasuringeyemovementsusingascleral
search coil in a magnetic field. IEEE Trans Biomed Eng 10:137–145.
Scudder CA, Kaneko CS, Fuchs AF (2002) The brainstem burst generator
for saccadic eye movements. A modern synthesis. Exp Brain Res
Soetedjo R, Kaneko CR, Fuchs AF (2002a) Evidence that the superior col-
liculus participates in the feedback control of saccadic eye movements.
J Neurophysiol 87:679–695.
SoetedjoR,KanekoCR,FuchsAF (2002b) Evidenceagainstamovinghillin
the superior colliculus during saccadic eye movements in the monkey.
J Neurophysiol 87:2778–2789.
Waitzman DM, Ma TP, Optican LM, Wurtz RH (1991) Superior colliculus
neurons mediate the dynamic characteristics of saccades. J Neurophysiol
Matsuoetal.•GazeFeedbacktotheCatSuperiorColliculus J.Neurosci.,March17,2004 • 24(11):2760–2773 • 2773