Download Saccades and multisaccadic gaze shifts are gated by different

Exp Brain Res (1999) 125:287–301
© Springer-Verlag 1999
R E S E A R C H A RT I C L E
Julien Petit · François Klam · Alexej Grantyn
Alain Berthoz
Saccades and multisaccadic gaze shifts are gated
by different pontine omnipause neurons in head-fixed cats
Received: 20 January 1998 / Accepted: 22 October 1998
Abstract Pontine omnipause neurons (OPNs) have so
far been considered as forming a homogeneous group of
neurons whose tonic firing stops during the duration of
saccades, when the head is immobilized. In cats, they
pause for the total duration of gaze shifts, when the head
is free to move. In the present study, carried out on alert
cats with fixed heads, we present observations made during self-initiated saccades and during tracking of a moving target which show that the OPN population is not homogeneous. Of the 76 OPNs we identified, 39 were
found to have characteristics similar to those of previously described neurons, “saccade” (S-) OPNs: (1) the
durations of their pauses were significantly correlated
with the durations of saccades; (2) the discharge ceased
shortly before saccade onset and resumed before saccade
end; (3) visual responses to target motion were excitatory; and (4) during tracking, S-OPNs interrupted the discharge for the duration of saccades and resumed firing
during perisaccadic “drifts”. However, the characteristics
of 37 neurons (“complex” (C-) OPNs) were different: (1)
the pause duration was not correlated with the duration
of self-initiated saccades; (2) time lead of pause onsets
relative to saccades was, on average, longer than in the
group of S-OPNs, and firing resumed after the saccade
end; (3) visual target motion suppressed tonic discharges; and (4) during tracking, firing was interrupted for the
total duration of gaze shifts, including not only saccades
but also perisaccadic “drifts”. We conclude that cat
OPNs can be subdivided into two main groups. The first
comprises neurons whose firing patterns are compatible
with gating individual saccades (“saccade” OPNs). The
second group consists of “complex” OPNs whose firing
characteristics are appropriate to gate total gaze displacements rather than individual saccades. The function of
A. Grantyn (✉) · J. Petit · F. Klam · A. Berthoz
Laboratoire de Physiologie de la Perception et de l’Action,
UMR C-9950, Centre National de Recherche Scientifique,
Collège de France, 11 Place Marcelin Berthelot,
F-75005 Paris, France
e-mail: [email protected]
Tel.: +33-1-44-27-16-28, Fax: +33-1-44-27-13-82
these neurons may be to disinhibit pontobulbar circuits
participating in the generation of saccade sequences and
associated perisaccadic drifts.
Key words Omnipause neurons · OPN · Saccade ·
Gaze shift · Tracking · Perisaccadic drifts · Moving
target · Cat
Introduction
Evinger and Fuchs (1978) demonstrated that the oculomotor repertoire of cats includes movements that are
slower than saccades but faster than smooth pursuit.
Such eye movements often follow saccades or are intercalated between saccades during multisaccadic gaze
shifts (Olivier et al. 1993; Missal et al. 1993). Two lines
of evidence suggest that efferent activity of the superior
colliculus (SC) may be at the origin of such intermediate-velocity eye movements, which we shall henceforth
call “drifts”. Firstly, bursts of some visuomotor tectoreticulospinal neurons (TRSNs) continue beyond the end of
saccades and may account for a facilitation of preoculomotor circuits during postsaccadic drifts (Olivier et al.
1993). Secondly, sufficiently prolonged stimulation of
the cat SC evokes saccades followed by slow movements
comparable to postsaccadic drifts observed during visually guided orienting (Grantyn et al. 1996; Missal et al.
1996). Firing patterns and connections of TRSNs (Olivier et al. 1993) and of their target neurons in the pontine
reticular formation (Grantyn et al. 1992) show that, in
the cat, the SC has access to two intimately related premotor systems which differ in their dynamic properties.
The first one is the saccadic burst generator which consists of medium-lead and long-lead bursters whose activity is gated by the pontine omnipause neurons (OPNs)
(reviewed in Moschovakis et al. 1996). The second one
is a phylogenetically older system primarily subserving
rapid head movements through spinal projections of
TRSNs and of “eye-neck” (Grantyn and Berthoz 1987)
reticulospinal neurons (RSNs). Neurons of the second
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system establish collateral connections with ocular motoneurons and with the nuclei harbouring the oculomotor
integrator (Grantyn et al. 1992; Olivier et al. 1993). They
are thus likely to drive not only neck but also ocular
motoneurons. The resulting eye movements should be of
low velocity if it is assumed that the saccadic generator
is totally or partially bypassed.
Relationships of TRSNs and orienting-related RSNs
with neurons of the saccadic generator are not yet completely understood. With regard to OPNs, previous experimental studies and models (reviewed in Hepp et al.
1989; Moschovakis et al. 1996) have emphasized the
role of these neurons in gating the activity of mediumlead excitatory and inhibitory neurons. On the other
hand, intracellular labelling of OPN axons revealed a
broad divergence of their connections in the brain stem
(Ohgaki et al. 1987; Strassman et al. 1987). Markham et
al. (1992) suggested therefore that the role of OPNs may
not be limited to the timing of individual saccades and
that “OPN projections to reticular or reticulospinal neurons may help to synchronize eye and neck motor control of the visual gaze axis”. Indirect evidence supporting
this view was obtained by Paré and Guitton (1990,
1998), who found that cat OPNs pause for the entire duration of gaze shifts in head-free cats. However, the same
authors found that all of these OPNs resume firing before the end of individual saccades when the head is
fixed. Thus, in this behavioural condition, OPNs would
not provide a gating signal for postsaccadic drifts.
In the present study we have re-examined the activity
of OPNs, in particular during multisaccadic tracking of
moving targets by head-fixed cats. We found that, besides typical saccade-related OPNs (Evinger et al. 1982;
Paré and Guitton 1994a), the midline region of the pons
contains OPNs displaying different relationships with
eye movements. These cells stop firing for the total duration of complex gaze shifts during tracking. They may
therefore gate eye movement sequences which include
not only saccades but also intersaccadic and postsaccadic
drifts. Omnipause neurons of this type have not been described in previous studies in head-fixed cats. Some of
our results have already been published as an abstract
(Petit et al. 1997).
Materials and methods
Chronic experiments were performed on two cats. Surgical and
experimental techniques have already been described in detail
(Olivier et al. 1993; Grantyn et al. 1996). They were in agreement
with the directives of the French Ministry of Agriculture and of
the Commission of the European Community. The surgery was
conducted under aseptic conditions. The anaesthesia was induced
by intramuscular injection of ketamine (Imalgène, 25 mg/kg) and
maintained by a continuous intravenous infusion of propofol (Rapinovet). Adjustments of the infusion rate (7–15 mg/kg per hour)
were guided by variations in the heart rate. Rectal temperature was
automatically stabilized at 37°C. An eye coil consisting of three
turns of Teflon-insulated multistrand stainless steel wire was implanted beneath the insertions of the extraocular muscles of the
right eye. A dental acrylic socket was fixed to the skull. The sock-
et contained three screws which served for painless fixation of the
head during recording sessions. A stainless steel chamber was implanted over an opening trephined in the occipital bone, posterior
to the tentorium. The chamber provided access to the caudal brain
stem in the vicinity of the abducens nuclei. It was hermetically
closed between recording sessions, and the surface of the cerebellum was protected by local antibiotics. A systemic antibiotic with
protracted action (Extencillin, 600,000 IU, i.m.) was given prophylactically during the surgery.
During the experiments the head of the animal was fixed in
stereotaxic orientation. To prevent distracting stimuli the visual
field was limited to the central ±35 deg by a circular mask. The visual target was a cardboard square subtending 10 deg of the visual
angle. It was positioned in the centre of the visual field and could
be moved at constant velocity on a tangent rail fixed to a homogeneous screen at a distance of 65 cm from the eyes. The trajectory
could be set in any direction and the velocity could be varied between 10 and 100 deg·s–1. However, in the experiments reported
here we used only four axes (horizontal, vertical, +45 deg and –45
deg) and one speed (60 deg·s–1) of target motion. To evoke tracking eye movements and to evaluate visual responses of neurons,
the target was moved by a servo-controlled motor between the two
extremities of the rail (+32 deg to –32 deg). The delay between
successive displacements was 2 s. The animals were not conditioned for either fixation or tracking of the target, which became
behaviourally neutral at the very beginning of the experiments. Its
permanent presence in the centre of the visual field did not therefore impede spontaneous scanning saccades. By contrast, a sudden
displacement of the target immediately attracted the cats’ attention
and reliably elicited tracking eye movements. In the absence of
any reward, the response habituated rapidly, changing from a sequence of tracking saccades, to single saccades and finally to neglect of the moving target. For this reason we limited the number
of target excursions to six in a sequence and repeated such sequences at irregular intervals. When an OPN was isolated, the first
part of the recording was made while the target remained stationary, to obtain a sample of spontaneous eye movements. Thereafter
we started the tests with the moving target and recorded the activity of OPNs during different combinations of saccadic and driftlike tracking movements. In addition, if cats eventually abandoned
the tracking completely, modulation of firing by the moving visual
stimulus was evaluated in the absence of concomitant eye movements. During the experimental sessions of 5–6 h, cats were regularly fed and given short periods (15–30 min) of complete rest.
We used glass microelectrodes filled with 3.8 M NaCl and
bevelled to tip diameters of 1.5–2.0 µm and resistances of 1.5–2.0
M. Only perisomatic extracellular recordings were retained for the
study. We identified them by triphasic spikes with a negative main
component that could be monitored over a depth of 150–250 µm
while adjusting the position of the electrode. Cell activity was
stored, along with horizontal and vertical eye and target positions,
on the hard disk of a microcomputer using a CED 1401 Plus analog-digital converter (Cambridge Electronic Design, UK). Sampling rates were 10 kHz and 2 kHz for neuron and eye position
signals, respectively. Action potentials were reliably discriminated
using CED Spike2 software, which was also employed for the data
analysis. After filtering eye position signals (FIR low-pass filter
with maximally flat pan and stop bands, band width 100 Hz),
identification of saccades was based on acceleration criteria. Velocity and acceleration were calculated applying a 41-point Sawitzky-Golay smoothing filter (Press et al. 1992) to the position signals. For eye movements to be classified as saccades the absolute
magnitude of the horizontal or vertical eye acceleration had to exceed 500 deg·s–2. The onset of saccades was defined as the time
when the absolute value of the acceleration exceeded the threshold
of 200 deg·s–2. The same value was used to determine the saccade
end. Movements that did not satisfy the criteria of saccades were
considered to be drifts, and were not quantitatively analysed. Eye
position was defined as “steady” if it did not change by more than
0.1 deg over a 0.2-s time bin.
The following parameters were calculated: the mean firing rate
during intersaccadic periods, the durations of the pauses in cell ac-
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Fig. 1A–E Locations of omnipause neurons. A Biocytin deposits (arrows) at two sites of
recordings of multiunit OPN
activity. B Reconstruction of
positions of individual OPNs
recorded in two tracks 100 µm
rostral and 100 µm caudal to
the track shown in A. Saccade
OPNs and complex OPNs (as
defined in the text) are indicated by S and C, respectively.
C–E Parasagittal maps of all
OPNs recorded in two cats.
Numbers on top indicate mediolateral coordinates (mm) of
OPNs included in each map.
Orientation of maps is shown
at the bottom (d dorsal, r rostral) (open squares saccade
OPNs, filled circles complex
OPNs, Abd abducens nucleus,
CT trapezoid body, GVII genu
of the facial nerve, Nrt nucleus
reticularis tegmenti pontis,
Pyr pyramidal tract,
RPc nucleus reticularis pontis
caudalis, SO superior olive,
VI root of the abducens nerve)
A
B
C
tivity, the total durations of the saccades, the maximum velocity of
the horizontal and vertical saccade components, the eye positions
prior to the saccades as well as the polar amplitudes and directions
of saccades. Statgraphics software was used for the statistical
analysis. Unless otherwise specified, the t-test was used to assess
the significance of the relations between variables. The significance level was set at 99% (P≤0.01). It should be noted that our
definition of saccades was not the same as in previous studies of
OPNs. Evinger et al. (1982) defined the beginning and the end of
a saccade as the first and the last non-zero points on eye velocity
traces. Paré and Guitton (1990; 1994a) used a 10 deg·s–1 velocity
threshold, and later changed its value to 20 deg·s–1 (Paré and Guitton 1998). Both research groups placed the cursors manually. Our
method of acceleration threshold is more appropriate for automatic identification of saccades. It gives intermediate values of saccade duration: shorter than in Evinger et al. (1982) and longer than
in Paré and Guitton (1994a). The differences are small enough to
allow valid comparisons between the data from the three research
groups.
Locations of the recorded neurons were determined from their
coordinates with respect to the abducens nuclei. The outlines of
the nuclei were obtained during the first recording sessions by a
systematic mapping of the activity of abducens motoneurons. Before sacrificing the animals, small electrolytic lesions were made
at a known depth along selected recording tracks and cell positions were reconstructed with reference to the lesion marks. In the
second of the two cats this technique was supplemented by direct
labelling of the recording sites. To run the last track we used an
electrode (3.5 µm) filled with 4% solution of biocytin in a mixture
of 1.9 M NaCl and 0.05 M Tris buffer (pH 7.9). The coordinates
of the track approximately corresponded to the region where the
D
E
probability of encountering OPNs in preceding experiments was
the highest. At two sites of multiunit OPN activity (Fig. 1A), biocytin was injected by iontophoresis (+0.5 µA over 30 min). Cats
were put to death by an overdose of pentobarbital and perfused
through the ascending aorta with phosphate-buffered saline (PBS,
1.5 l) followed by 4% paraformaldehyde in PBS (2.0 l). During
dissection, the head was placed in a stereotaxic orientation. Vertical and horizontal guide needles were inserted to define the plane
of the sections and to permit a reconstruction of the brain stem in
exactly the same coordinate frame as used during the recordings.
We used conventional histological techniques to prepare serial
sections of the brain stem and to reveal the labelling at the sites of
biocytin iontophoresis.
Results
Quantitative analysis was performed on 76 OPNs identified by the characteristics of their discharge during saccades (see below) and by their location. Figure 1A shows
the locations of biocytin deposits (arrows) at the sites
where we recorded multiunit activity from two OPN
clusters. The locations of individual OPNs encountered
in two adjacent tracks, respectively situated 100 µm rostrally and 100 µm caudally from the labelled track but in
the same mediolateral position, are illustrated in Fig. 1B.
The positions of all OPNs are marked on standard parasagittal maps of the caudal pons in Fig. 1C–E. The re-
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Fig. 2 Activity of a representative saccade OPN in relation to a
spontaneous saccade (A) and during a multisaccadic gaze shift in
the direction of a moving target (B). A Upper two traces instantaneous firing rate and the original spike record. Lower traces vertical (V) and horizontal (H) eye position (Pos), eye velocity (Vel)
and eye acceleration (Acc). Positive sign on scale bars denotes
rightward and upward movement directions. Vertical dash-dotted
lines mark saccade onset and saccade end. B Same arrangement
and notation of traces as in A, except that the second trace from
the top is the record of target position, and eye acceleration traces
are omitted. The onset and the end of target displacement are
marked by vertical interrupted lines. Target moves from left-up to
right-down along the –45° meridian, with a total angular displacement of ±32 deg. Note postsaccadic drift (arrow) after the third
saccade in the sequence
gion of recordings extended from the level of the abducens nucleus to 1.9 mm rostrally. A majority of OPNs
were located close to the midline (0.0–0.25 mm; Fig.
1C,D) and only a fifth of them were found more laterally
(0.3–0.5 mm; Fig. 1E).
As in previous studies on OPNs, we identified these
neurons by the cessation of their tonic activity during
saccades of any direction and amplitude. We found that
their firing patterns were qualitatively different. Figure 2
illustrates an OPN whose properties are very close to
those described in studies on alert cats (Evinger et al.
1982; Paré and Guitton 1994a). When the target was stationary and the cat made scanning eye movements, the
pause began before the start of the spontaneous saccade
and ended before the end of the saccade (Fig. 2A). Activity of the same neuron during tracking of the moving
target is shown in Fig. 2B. During the illustrated half-cycle of stimulation, the target moved along an oblique (45
deg) trajectory from upper left to right and down. The
gaze of the cat followed the target by a sequence of saccades and a terminal postsaccadic drift. The discharge of
the OPN exhibited the same saccade-related behaviour
as seen during scanning movements: it stopped during
saccades and usually resumed before the saccade ended.
As can be seen in Fig. 2B, the presence of a postsaccadic
drift after the last saccade in the sequence did not delay
the resumption of activity. In addition, we often observed
a small increase in discharge frequency at the start of the
target displacement and after the termination of individual saccades.
Typical examples of recordings from an OPN with
different discharge properties are shown in Fig. 3. During horizontal target displacement from right to left (Fig.
3A), the discharge frequency began to decrease shortly
after the start of the target movement and exhibited a
long pause for the whole duration of the initial presaccadic drift and the subsequent leftward saccade. The discharge was restored slowly and with a long delay after
the saccade. Such a slow recovery of firing can also be
seen after pauses associated with spontaneous saccades,
as shown by the examples in Fig. 3A (rightward saccade
after the target stopped its leftward movement) and Fig.
3B (upward saccade before the onset of target displacement). In general, saccade-related pauses were longer
when the target was moving than when it was stationary.
The discharge of the same OPN could pause during al-
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Fig. 3A, B Activity of a representative complex OPN during gaze
shifts evoked by horizontal target motion. Arrangement and notation of traces as in Fig. 1B. Calibrations of eye velocity and eye
position are to the left and to the right of the records, respectively.
The period of target displacement is marked by vertical interrupted lines in A and B. A Leftward target displacement accompanied
by a presaccadic drift (arrow) followed by a double saccade to the
left. Note the decrement of cell firing rate shortly after the beginning of target motion and a complete cessation of firing before the
presaccadic drift. B Rightward target displacement accompanied
by a complex gaze shift containing intersaccadic and postsaccadic
drifts (arrows). This neuron stops firing for the total duration of
the eye movement sequence
most the entire period of target displacement if a series
of saccades were elicited at short intervals, regardless of
saccade direction (Fig. 3B: horizontal target displacement from left to right). Figure 3A shows that at the onset of target motion the firing rate decreased slowly, long
before any eye movement could be detected. We shall
show below that motion of the target suppressed the firing of some OPNs independently of eye movements.
In our sample, 39 OPNs had discharges qualitatively
similar to those shown in Fig. 2, whereas 37 were of the
type shown in Fig. 3. It seemed justified to classify them
into two groups. The first consists of OPNs whose pauses are unequivocally related to individual saccades regardless of whether they are spontaneous or elicited by a
moving target. The second consists of OPNs that stop
firing for the whole duration of complex gaze shifts,
such as saccade sequences and associated slow eye
movements. We shall call them “saccade” OPNs (SOPNs) and “complex” OPNs (C-OPNs), respectively,
and present the quantitative analysis which supports this
classification.
Responses to target motion
In some instances, it was possible to demonstrate that
target displacement alone had a suppressive effect on the
discharge of C-OPNs. The example in Fig. 4A shows
that the firing rate began to decrease shortly after the
start of horizontal motion of the target. The discharge
then stopped completely even though no eye movements
were detectable, even with increased gains of position
and velocity traces. Since the discharge slowly resumed
while the target was still in motion, the slow decrease in
the firing rate and the pause could represent a response
to target acceleration rather than to velocity, which was
constant throughout the target’s excursion. In order to increase the number of such observations, we have analysed all trials including those during which cats made
tracking eye movements. Peristimulus time histograms
(PSTHs) of discharges of each OPN were constructed by
averaging spike activity in 10-ms bins, with the start of
the target displacement serving as the trigger (Fig.
4B,C). Initially we derived PSTHs separately for each
direction of target excursion but since the results for the
different directions were very similar we pooled them to-
292
Fig. 4A–C Sensory responses of OPNs to target motion. A Example of a complex OPN (same cell as in Fig. 3) showing firing rate
decrement and pause evoked by horizontal target displacement in
the absence of eye movements. B Peristimulus time histogram (bin
width 10 ms) of the same complex OPN. PSTH is obtained by
synchronizing the records at the onset of target displacement
(t=0). Numbers of spikes in each bin have been converted to firing
frequency. Average frequency begins to decrease with a latency of
about 100 ms, before any tracking eye movement could be generated (see text). C Similarly constructed peristimulus time histogram for a saccade OPN (same cell as in Fig. 2) demonstrating the
facilitatory effect of target motion
gether. A representative average response of a C-OPN is
shown by the PSTH of Fig. 4B. There is a substantial decrease in the average firing rate at a delay of 100 ms after the beginning of target motion. The decrease in activity develops slowly until a constant level is reached prior
to the end of the target movement which, in this case,
lasted 1.1 s. The onset latency of the firing rate decrease
is much shorter than the minimum latency (171 ms) of
the first tracking saccades occurring after the start of target motion. The mean latency of such earliest saccades
was 335 ms. The beginning of the decrease in discharge
was therefore related to the target displacement but not
to eye movement. It should be noted that the late large
decrement in the average firing rate observed beyond
170 ms depends to a large extent on the averaging of
asynchronous saccade-related pauses. A purely visual response to target displacement cannot therefore be evaluated during this period.
The PSTH of the discharge of an S-OPN is shown in
Fig. 4C. In contrast to the C-OPN, this histogram exhibits an initial firing increment with a peak latency of 80
ms which is comparable to the latencies of visual responses of OPNs studied by Evinger and coworkers
(1982). After the end of the transient excitatory response, the level of the discharge is slightly lower than
that observed before the start of the target displacement.
This small reduction is caused by the averaging of the
pauses in the discharge during the saccades evoked at
widely varying latencies after the onset of target movement.
Mean firing rate between spontaneous saccades
The background firing rate was calculated as the average
of mean rates collected in time bins of 0.2 s during the
periods free of any eye movement and in the absence of
target motion. Data recorded when the position of the
eyes had varied by more than 0.1 deg were excluded. To
avoid the effects of firing rate modulation preceding or
following the saccade-related pauses, we also discarded
the periods of 0.3 s before and after saccades. Plots of
the OPN firing frequency as a function of the vertical
and horizontal eye position were examined and no correlation was found. The background discharge was irregular, so that the mean frequencies in individual bins were
widely distributed around the global mean value. The
distributions of the mean background frequencies of Sand C-OPNs are shown in Fig. 5A,B. The ranges were
broad in both groups of neurons, from about 20 imp·s–1
to 135 imp·s–1, but the distribution was shifted towards
lower values in C-OPNs. The mean firing rates calculated over all neurons in each group were 61±29 imp·s–1 for
C-OPNs and 86±25 imp·s–1 for S-OPNs. The difference
293
Fig. 5 Distribution of background discharge frequencies of saccade (A) and complex (B) OPNs. C Scatterplot of mean discharge
frequency (abscissa) and of coefficient of variation (ratio of standard deviation over the mean frequency) (ordinate) in saccade
(filled squares) and complex (empty squares) OPNs. Each symbol
represents an individual neuron
between the two groups was statistically significant
(df=73; P=0.00014). Firing rates below 50 imp·s–1 were
observed in 16 out of 37 (43%) C-OPNs, whereas only
13% (5/39) of S-OPNs fell in this range (Fig. 5A,B). The
standard deviation of the mean discharge rate was less
widely distributed (7.9–37.5 imp·s–1). Therefore the discharge of the cells which fired at lower frequencies
seemed more variable. This was confirmed by the calculation of the coefficient of variation (CV), which is the
ratio of the SD to the mean rate. The CV (14.9–61.8%)
decreased as the mean frequency of discharge increased
(Fig. 5C), so that OPNs with the lowest rates of discharge had the highest coefficients of variation. Since the
sample of C-OPNs contained more neurons discharging
at low rates, high values of CV (>40%) were also more
frequently encountered.
Previous reports specified the range of mean firing
rates of OPNs as 50–130 imp·s–1 (Evinger et al. 1982;
Paré and Guitton 1994a) and the range of CV as
16.0–45.1% with a mean of 29.1±7.9 (SD) (Paré and Guitton 1994a). A majority of S-OPNs in our sample had similar characteristics, whereas C-OPNs tended on average to
have lower rates and correspondingly higher coefficients
of variation. Indeed, OPNs discharging at rates below 50
imp·s–1 have not been reported by others. It is important to
note that neurons displaying such low rates were present
in the groups of both saccade and complex OPNs.
Relation between durations of pauses
and of spontaneous saccades
We limited the analysis of relations between pause and
saccade durations to spontaneous saccades in the absence of target motion. Pause durations were included in
the data only if OPNs resumed firing between successive
saccades. Figure 6A shows a representative example of a
C-OPN (same cell as in Fig. 3). Linear regression analysis did not indicate a statistically significant correlation
between the pause duration (TP) and the total saccade duration (TS). Practically all data points were above the line
of unity slope, which corresponds to pauses of longer duration than saccades. As can be seen in Fig. 6A (open
circles), the majority of pauses ended after saccade termination. The relations observed in a representative SOPN (same cell as in Fig. 2) are illustrated in Fig. 6B.
The linear correlation was highly significant, with a
slope of 1.008 and an intercept of –7 ms. The negative
intercept results from the fact that the duration of pauses
was on average somewhat shorter than the duration of
saccades.
The linear regression analysis of TP versus TS was
performed for each OPN. A significant relation was
found for all 39 S-OPNs, whereas in none of the COPNs did the tendencies to positive correlations reach
statistical significance. In the group of S-OPNs the
slopes of the TP vs. TS plots varied between 0.53 and
2.03 (mean 0.94±0.29), with correlation coefficients of
0.42–0.94 (mean 0.71±0.14). The slopes of the majority
of S-OPNs (85%) were distributed over a more restricted
range (0.65–1.23). Only a small number of cells had
more shallow slopes and large positive intercepts or
294
Fig. 6A–C Relationships between pause durations and saccade
durations in complex OPN and saccade OPNs. Pauses terminating
before the end of the saccades are represented by filled circles,
those terminating after saccade end by open circles. A Complex
OPN. The correlation between pause and saccade durations is not
statistically significant (r=0.17; P=0.111). Data points lie above
the unity slope (interrupted line) indicating that pauses last longer
than saccades. B Saccade OPN showing a significant linear correlation between pause and saccade durations (slope 1.008, intercept
–7.0 ms, r=0.89, P<0.0001). C Regression lines for 39 saccade
OPNs. All correlations are statistically significant at the P≤0.01
level
steeper slopes and large negative intercepts (Fig. 6C).
Evinger and coworkers (1982) reported a mean slope of
0.9 and a mean correlation coefficient of 0.70 for the relationship of the TP with the duration of horizontal saccade components. In the present study we analysed TP in
relation to the total saccade duration, like Paré and Guitton (1994a). These authors obtained the slopes and correlation coefficients in the ranges of, respectively,
0.77–1.32 and 0.85–0.99. With a few exceptions, SOPNs of the present study correspond to the above descriptions. In contrast, C-OPNs must be considered as a
separate group because the durations of their pauses are
not significantly correlated with saccade durations.
Timing of pause onsets and terminations with respect
to saccades
The distributions of time intervals between pause and
saccade onsets are shown in Fig. 7A,B. Saccade OPNs
began to pause in advance of saccades and usually resumed firing before the saccade end. The mean values of
pause lead time (TON) with respect to saccade onset varied between –2 and –36 ms (overall mean –15±7 ms).
The mean TON values of pauses in C-OPNs (Fig. 7B)
were distributed over a much broader range (–7 to –180
ms; overall mean –49±39 ms). Although the distributions characterizing the two groups showed an overlap in
the range of –40 to 0 ms, cells with very short mean TON
were uncommon among C-OPNs. For example, only
22% of cells exhibited a TON shorter than –20 ms, whereas 80% of values from S-OPNs were in this range. On
the other hand, mean pause lead times greater than 40 ms
were observed only among C-OPNs (Fig. 7B). In general, the variability of timing was higher in cells with longer lead times. In order to compare our data with the previously published reports, we calculated the mean SD in
two groups of OPNs, restricting the range of TON to that
of S-OPNs (–40 to 0 ms). Within this range, the mean
SD of S-OPNs was 16.5±9.8 ms and that of C-OPNs
24.6±11.1 ms. Timing of pause onsets in C-OPNs with
very long TON values was extremely variable, as indicated by the overall mean value of the SD (59.1±55.9 ms).
In a sample of 24 OPNs, Paré and Guitton (1994a) obtained the mean TON, ranging from –5.6 to –35.1 ms,
with the overall mean of –19.7±7.5 ms, and a mean SD
of 11.2±4.0 ms. The characteristics of their sample were
practically identical to those of our S-OPNs but clearly
different from those of C-OPNs. It should be recalled
that all neurons studied by Paré and Guitton (1994a)
showed significant correlations between pause and saccade durations, which means that cells with properties of
C-OPNs were not encountered in their sample.
As shown in Fig. 7C, a majority of S-OPNs (82%) resumed firing before the end of the saccade. The range of
the time intervals between pause and saccade offsets
(TOFF) extended from –35 ms to 13 ms (mean –13±12
ms), in which the negative sign is attributed to pauses
terminating before the saccade end. These values correspond well to those reported by Paré and Guitton
(1994a) (range –35.2 to 4.6 ms; mean –14.1±8.3 ms) and
by Evinger et al. (1982), who illustrated, for a few
“short-lead” OPNs, a range of approximately –60 to –6
ms (taken from their Fig. 3I). The variability of TOFF was
higher in our sample of S-OPNs (mean SD 26.8±11.0
ms) than in the sample of Paré and Guitton (1994a)
(mean SD 12.0±4.1 ms).
295
Fig. 7A–D Timing of pauses relative to saccades. A,B Distribution of time intervals between the last spike before the pause and
saccade onset (TON) in saccade and complex OPNs. Negative values correspond to pauses beginning earlier than saccades. C,D
Distribution of time intervals between the last spike after the
pause and the saccade end (TOFF). Negative values correspond to
resumption of activity before the saccade end
In contrast to S-OPNs, resumption of firing by COPNs occurred after the saccade end in 87% of neurons.
The range of TOFF was very broad (–27 to 222 ms), with
an overall mean of 58±64 ms. The standard deviations of
the mean values increased with increasing time lags.
Therefore, in order to compare the variability of timing
between C- and S-OPNs, we selected the 15 C-OPNs
whose mean TOFF values were in a similar range (–30 to
30 ms) to that of S-OPNs. The standard deviation of
TOFF in this group (41.8±16.9 ms) was significantly
greater than among S-OPNs (P<0.002). Cells with very
long mean time lags (>100 ms) displayed standard deviations in the range of 60–200 ms. C-OPNs are thus different from S-OPNs not only by a later resumption of the
discharge but also by a higher variability of timing. To a
large extent, the latter can be accounted for by the presence of postsaccadic drifts during which complex OPNs
remained silent.
Recovery of background firing rates after pauses
In addition to the delayed termination of pauses in COPNs, comparison of the records shown in Figs. 2 and 3
suggests that these cells also differ from S-OPNs with
respect to the dynamics of firing rate recovery after the
pause. Whereas in S-OPNs the backgound level is attained quickly and even shows a transient overshoot, in
C-OPNs the recovery of the firing rate is slow. This
property may be of functional significance because the
firing rate during shorter intersaccadic intervals would
have no time to return to the normal background level.
We studied the recovery curves for each OPN by averaging the discharge rate over a series of similar pauses.
Similar pauses were selected according to the following
criteria: (1) the duration of saccade-related pauses had to
be within ±20% of the median pause duration of a given
neuron, (2) the time difference between pause onset and
saccade onset had to be within ±20% of the median value of this parameter, and (3) the OPN discharge during
0.3 s preceding the pause had to be equal to or above the
mean discharge rate between saccades. The averaging
process (10-ms time bins) was triggered by the first
spike generated at the pause end. Examples of the time
course of the firing rate recovery of representative Cand S-OPNs are shown in Fig. 8A,B, respectively. The
mean discharges were fitted by a third-order polynomial
f=α+βt+γt2+δt3, shown by the continuous lines in Fig. 8.
296
Fig. 8 Time course of recovery
of the firing rate after pauses in
a complex (A) and in a saccade
(B) OPN. Averaging of spike
activity in bins of 10 ms, with
the first spike after the pause
serving as trigger (t=0) (diamonds numbers of spikes in
each bin, rescaled in the dimension of firing frequency, solid
lines fitting of the data points
by third-order polynomial; see
text)
Since the zero-order coefficient α was small and insignificant, the first-order coefficient β approximated the
rate of the frequency increase near the time origin. This
was 882 imp·s–2 for the C-OPN of Fig. 8A and 2167
imp·s–2 for the S-OPN of Fig. 8B. The S-OPNs tended to
have faster rate increases (mean β 3180 imp·s–2; range
995–8002) than the C-OPNs (mean β 2068 imp·s–2;
range 218–6440). This difference was statistically significant (Kolmogorov-Smirnov test, P=0.0009). Since it
could be due, on average, to the higher mean rates of discharge of S-OPNs, the ratio of the speed of recovery (β)
to the mean frequency of discharge was calculated for
each OPN. The mean ratio for S- and C-OPNs was
40.3±7 and 30±9, respectively. These two means were
statistically different (Kolmogorov-Smirnov test:
P=0.002). Therefore, the differences in the speed of recovery between saccade and complex OPNs cannot be
simply explained by the differences in the mean discharge.
Discussion
Two groups of omnipause neurons
Alert head-fixed cats often track a rapidly moving target
by a sequence of two or more saccades separated by periods during which the eyes are either stationary or, more
often, continuously moving at low velocity. We found
that some OPNs stop firing for the total duration of such
composite gaze shifts [“complex” (C-) OPNs], whereas
others continue to pause for every saccade in the sequence [“saccade” (S-) OPNs]. Cells of these two types
are often closely located, as illustrated in Fig. 1B, which
shows the depth of recordings in tracks separated by only 200 µm. The overlap of locations was complete also in
the anteroposterior and mediolateral directions (Fig.
1C–E) within the region, which corresponds exactly to
the OPN area in the cat (Evinger et al. 1982). In previous
studies OPNs were identified by their location and by
their characteristic pause during saccades in all directions (Evinger et al. 1982; Strassman et al. 1987; Paré
and Guitton 1994a). Based on these two criteria, cells
classified as C-OPNs belong to the OPN population, in
the conventional sense of the term.
The properties of S-OPNs that we have analysed are
similar to those described by Paré and Guitton (1994a).
The pauses began shortly before saccade onset, terminated before the saccade end, and pause duration showed
significant linear correlations with saccade duration.
These temporal relationships remained the same during
single saccades and saccade sequences, no matter whether the movements were spontaneous or evoked by a
moving target. In addition, we found that all S-OPNs increased their firing rate following the onset of target displacements regardless of subsequent eye movements.
The transient character of the responses suggests a sensitivity to the acceleration of the visual stimulus, in agreement with Evinger and coworkers (1982).
Complex OPNs interrupted their tonic discharges for
the whole duration of saccade sequences. In contrast to
S-OPNs, they did not resume their activity during intersaccadic intervals. This particular behaviour was readily
recognized during recording from the moment the cats
made their first multisaccadic gaze shifts. Subsequent
quantitative analysis showed that C-OPNs can also be
distinguished from S-OPNs on the basis of behaviour
during single spontaneous saccades. Pauses of C-OPNs
started, on average, with a longer time lead and terminated after the saccade end. Thus they were of longer duration than the saccades. The relationships between pause
duration and saccade duration were not statistically significant. The tendency to stop firing for periods exceeding saccade durations was even greater in the presence of
297
a moving target. In contrast to S-OPNs, this visual stimulus suppressed the firing of C-OPNs. The combination
of two properties – long pauses and visual suppression –
accounts sufficiently well for the total cessation of firing
during tracking gaze shifts consisting of repetitive saccades and intercalated slow movements.
We found that, during fixation periods, C-OPNs fire,
on the average, at lower rates than S-OPNs. It is known
that the transition to drowsiness is accompanied by a reduction of OPN firing rate, presumably because of the
weakening of tonic facilitatory inputs (Keller 1977; Henn
et al. 1984). One could therefore suppose that prolonged
pauses of C-OPNs are a consequence of low firing rates
which, in turn, are due to a low level of alertness. This
explanation is unsatisfactory because all OPNs with
“complex” behaviour were tested during multisaccadic
tracking, which cannot be elicited in drowsy cats. Moreover, some cells clearly identified as S-OPNs displayed
very low firing rates and, vice versa, some C-OPNs discharged at high frequencies, eventually reaching the extreme values encountered among S-OPNs (Fig. 5A,B).
Differences in firing rates alone cannot therefore account
completely for the differences in the saccade-related behaviour of C- and S-OPNs. This is in agreement with an
earlier demonstration (Evinger et al. 1982) that any given
OPN conserves its relationship with saccades during transition from higher (in the light) to lower (in the dark) firing rates. Besides mean firing rates, S- and C-OPN
groups also overlapped with respect to the timing of
pause onsets and terminations relative to saccades (Fig.
7), and with respect to the speed of the postsaccadic recovery of their background activity. These observations
are important because they prove that the properties of COPNs, which have not been reported by others, are not
due to the particular behavioural conditions of our study.
Indeed, Evinger et al. (1982) and Paré and Guitton
(1994a) rewarded the cats for making saccades, whereas
the oculomotor behaviour of our cats was self-initiated.
In the absence of any control experiments, it can only be
guessed that the level of vigilance of their subjects was,
on the average, higher than that in our study. However, in
the behavioural situation we used, S-OPNs with properties described in trained cats were recorded together with
C-OPNs which had some unusual characteristics. It can
be concluded therefore that the population of OPNs in the
cat is genuinely inhomogeneous.
Complex OPNs are distinct from S-OPNs in three
characteristics: (1) they cease firing for the whole duration of saccade sequences, including the perisaccadic
slow movements; (2) visual target motion transiently suppresses their tonic discharge; and (3) they do not show a
correlation between pause and saccade durations. The
two groups overlap with respect to other quantitative
characteristics: background firing rate, timing of pauses
relative to saccades and speed of firing rate recovery after
the pauses. They may therefore represent the extremes of
a continuum rather than strictly separate classes.
Functional variability of OPNs has occasionally been
mentioned in previous studies. Fuchs and coworkers
(1991) reported that only a minority of monkey OPNs
show strong (r>0.9) correlations between pause and saccade durations, with slopes close to unity. A majority of
their cells displayed moderate or weak correlations and
eventually resumed the activity after the end of saccades.
Sometimes their pauses continued during postsaccadic
drifts. Variability of OPN characteristics in the cat has
been reported by Evinger et al. (1982). They distinguished “short-lead” and “long-lead” groups displaying a
mean TON of, respectively, –18.2±3.4 ms and –32.4±4.6
ms. The former group is similar to the S-OPNs of our
study. C-OPNs appear to be roughly comparable to longlead OPNs with respect to their mean TON (–49±39 ms).
However, long-lead OPNs resumed firing long before the
saccade end (mean TOFF –66.2±33.6 ms), in contrast to
the substantial lags displayed by C-OPNs (mean TOFF
58±64 ms). Pause durations of long-lead OPNs were correlated with saccade durations (see Fig. 2D in Evinger et
al. 1982), similarly to short-lead and S-OPNs but in contrast to C-OPNs. We conclude therefore that OPNs of the
complex type are different from the long-lead OPNs described by Evinger et al. (1982). The latter may correspond to S-OPNs in our study, those with a mean TON of
about –30 ms.
In spite of suggestions of functional variability, previous studies in monkeys (Luschei and Fuchs 1972; Keller
1974; Raybourn and Keller 1977; Coble et al. 1994; Everling et al. 1998) and in head-fixed cats (Curthoys et al.
1981; Evinger and Fuchs 1982; Paré and Guitton 1994a)
agreed that in both species OPNs are a qualitatively homogeneous population with properties suitable for the
control of the duration of saccades. The “saccade” OPNs
of the present study have characteristics which are consistent with this conclusion. But this is not the case for
C-OPNs: indeed, cells of this type may have been rejected in preceding studies because of the lack of significant
linear correlations between pause durations and saccade
durations.
Sensory inputs to complex OPNs
The background firing of OPNs is thought to be caused
by tonic excitatory inputs which are derived from different sensory modalities and are modulated by the state of
vigilance (Keller 1977). According to anatomical studies, the OPN region in the cat indeed receives convergent
connections from many brain stem areas known to integrate visual, auditory and somatosensory afferents (Ito et
al. 1984; Langer and Kaneko 1984). The tendency of COPNs to fire at lower firing rates than S-OPNs suggests
that they receive a somewhat weaker tonic excitatory bias. The difference between the two groups is more clear
cut with respect to the transient responses to visual stimulation. Movement of a visual target always elicited firing increments in S-OPNs, in agreement with other studies of cat OPNs under a variety of stimulation conditions
(King et al. 1980; Evinger et al. 1982). On the contrary,
firing of C-OPNs was suppressed by target motion, even
298
in the absence of tracking gaze shifts. When gaze shifts
were elicited by moving target, the latencies of suppression were much shorter than the reaction time. It is therefore obvious that inhibitory responses were caused by an
abrupt change in the visual environment. Apparently, COPNs lack afferent input from visual pathways transmitting phasic, short-latency excitatory effects.
Two structures have been identified as providing such
inputs to cat OPNs: the superior colliculus and the visual
cortex (King et al. 1980). Repetitive stimulation of the
SC evokes in OPNs an early excitatory response, followed by suppression of the discharge, even if the stimulus fails to evoke saccades (Raybourn and Keller 1977;
Kaneko and Fuchs 1982). Pathways linking the SC to
OPNs are therefore mixed, i.e., contain excitatory and
inhibitory components. Since C-OPNs show only suppression in response to phasic visual stimuli, they must
receive an input predominantly or exclusively through
the inhibitory component. The structure of the visual
field was not analysed in our experiments. Therefore, we
cannot exclude that some of its regions induce net inhibitory responses while other regions are excitatory. Such
an inhomogeneity of receptive field has not been observed for the excitatory effects on saccade-related
OPNs (Evinger et al. 1982). It remains to be studied
whether this is also true for the inhibitory responses of
C-OPNs.
Saccade-related inputs to complex OPNs
The origin of inhibition which causes the cessation of
OPN firing prior to and during saccades has not yet been
identified. Indirect evidence suggests that it is provided
by inhibitory neurons of the paramedian pontine reticular
formation (PPRF) that discharge like saccade-related
long-lead burst neurons (LLBs). This was initially suggested by Raybourn and Keller (1977), who observed
that a brief electrical stimulation of the SC elicits an afterdischarge of LLBs and a delayed suppression of OPN
firing, and that these two events have about the same duration. Later it was shown (Kamogawa et al. 1983) that
the complete arrest of discharges shortly before saccades
is preceded by a period of decreased excitability detectable 40–50 ms before the saccade onset, i.e., at the time
when “typical” LLBs begin to discharge. Finally, Kamogawa and coworkers (1996) elicited short-latency
(mono- or disynaptic) inhibition of OPNs by stimulating
the PPRF in the region of higher concentration of LLBs
in the cat (Sasaki and Shimazu 1981). Taken together,
these studies provide arguments in favour of inhibitory
pontine LLBs that project to OPNs. The total suppression of OPN firing, the pause, has been ascribed to the
input from medium-lead inhibitory bursters (IBNs)
(Fuchs et al. 1985; Scudder 1988) because this would
better explain the close correspondence of pause and saccade durations. However, evidence concerning projections of IBNs to OPNs is negative (reviewed in Strassman et al. 1986).
The lead times of LLB bursts in the cat cannot be
characterized by any single representative value. They
form a continuum which extends from the arbitrary limit
of about 15 ms (transition to medium-lead burst neurons)
to about 150 ms (Curthoys et al. 1981; Kaneko et al.
1981; Sasaki and Shimazu 1981). Because of such variation in timing, it is obvious that the number of recruited
LLBs, either excitatory or inhibitory, must increase with
time approaching the saccade onset. The strength of inhibition exerted on OPNs by inhibitory LLBs should then
also increase with time. OPNs that receive stronger connections will be the first to slow down and then stop firing which may be the case for C-OPNs displaying the
most advanced pauses. Similarly, a stronger connection
from inhibitory LLBs would also explain the slower and
later resumption of firing by C-OPNs. It could be argued
that LLBs in the cat usually stop firing well in advance
of saccade end (Kaneko et al. 1981) and cannot be a
source of the postsaccadic suppression of the discharges
of C-OPNs. Nevertheless, the same research group (Kaneko et al. 1981; Kaneko and Fuchs 1981) presented
specimen records from LLBs displaying a conspicuous
postsaccadic activity. Similarly, postsaccadic discharge
was observed in a presumably inhibitory LLB whose
projection to the OPN region was documented by intracellular labelling (McCrea and Evinger, published in
Moschovakis et al. 1996).
In addition to the inhibitory input from pontine burst
neurons, recent studies have suggested a complementary
mechanism of the saccade-related modulation of OPN
activity. This is the disfacilitation of OPNs caused by the
cessation of the discharge of “fixation” cells located in
the rostral pole of the SC. Fixation cells (SCFN) are tonically active during attentive fixations and pause during
refixation saccades, except for small contraversive ones
(Munoz and Guitton 1991; Munoz et al. 1991; Munoz
and Wurtz 1993a). Stimulation of the “fixation” zone in
the SC decelerates and interrupts saccades at short latencies (Munoz and Wurtz 1993b; Paré and Guitton 1994b)
and evokes, with a high probability, monosynaptic excitatory responses in OPNs (Paré and Guitton 1994b). Taken together, these studies suggested that SCFNs provide
OPNs with tonic excitatory input during active fixations,
and this input is removed during saccades that interrupt
such fixations. However, a recent quantitative comparison of saccade-related activity of monkey OPNs and
SCFNs (Everling et al. 1998) has clearly shown that such
a mechanism alone is insufficient and that multiple inputs to OPNs must be invoked to explain an accurate
timing of their pauses with respect to saccades. Among
several arguments in favour of this conclusion is the observation that pauses of SCFNs begin too early (–74 to
–1 ms) before saccades and terminate too late (–15 to
173 ms) after saccades. The respective ranges of OPNs
in the same monkeys (Everling et al. 1998) were –16 to
–3 ms and –13 to 65 ms, which is roughly comparable to
the characteristics of OPNs in the cat (Evinger et al.
1982; Paré and Guitton, 1994a), including our group of
S-OPNs.
299
It may be noted that OPNs which are defined here as
“complex” have temporal relationships with saccades
similar to those of monkey SCFNs. Although no valid
inference can be made from such an interspecies comparison, it raises the question whether the discharge patterns of cat SCFNs might be appropriate to account for
pauses of long duration in C-OPNs. Unfortunately, this
question must be left open because of a contradiction between the presently available studies. According to Munoz and Guitton (1991), cat SCFNs discharge tonically
when the cats are conditioned to fixate a target but their
activity becomes sporadic or even stops completely
when the eyes just stay still between spontaneous saccades, not associated with reinforcement. On the other
hand, Peck and Baro (1997) reported that some cat
SCFNs discharge during spontaneous fixations at about
the same rates (typically below 30 imp·s–1) as during fixations contingent on reward. They explained the difference between their and the former results by proposing
that, during the intertrial periods, their cats were expecting the next trial and had therefore a higher level of motivation than in the paradigm of Munoz and Guitton
(1991). In our experiments the cardboard target was permanently displayed in the centre of the visual field, so
that it became behaviourally neutral. Cats were fed at irregular intervals, during the intermissions between the
periods of cell search and recordings. They did not receive any reward for making saccades or tracking the
target when it moved. The experimental situation was
therefore more comparable to that of unrewarded, spontaneous eye movements in the study of Munoz and Guitton (1991). Relying on their results we assume that
SCFNs did not display any significant discharges and
could not contribute to the generation of long-duration
pauses by C-OPNs.
Role of complex OPNs in gaze shifts
We have shown that C-OPNs stop firing for the total duration of multisaccadic gaze shifts during tracking of
large-amplitude excursions of the target while the head is
fixed. Prolonged pauses during such gaze shifts are preceded by a decrease in firing rate which is due to the
suppressive effect of the moving visual stimulus. Firing
characteristics of C-OPNs are therefore compatible with
a role in gating saccade sequences and associated perisaccadic drifts, as well as pre- and postsaccadic drifts accompanying single spontaneous saccades or saccades to
stationary targets.
Comparison between complex and saccade OPNs
suggests differences in their efferent connections. Since
S-OPNs pause for every saccade, they cannot provide a
gating signal for complex gaze shifts in head-fixed cats.
Inhibitory connections of these cells to IBNs and to vertical MLBs have been proven by intracellular recording
of IPSPs (Furuya and Markham 1982) or by probing
changes of cell excitability after stimulation of the OPN
region (Nakao et al. 1988). Connections to horizontal
medium-lead excitatory burst neurons (EBNs) have been
assumed in models of the saccadic generator (Van Gisbergen et al. 1981; Fuchs et al. 1985; Scudder 1988) because, in primates, the durations of OPN pauses and
EBN bursts are closely correlated. Further supporting evidence comes from the demonstration of collateral
branching and terminations of intracellularly labelled
OPNs in the regions containing EBNs and IBNs (Strassman et al. 1987; Ohgaki et al. 1987). However, since termination areas of OPNs in the pontine and rostral bulbar
reticular formation are widespread, it has been suggested
that gating effects of OPNs are not limited to burst neurons of the saccadic generator but may also be exerted on
neurons controlling rapid head movements (Ohgaki et al.
1987; Markham et al. 1992).
Reticulospinal neurons (RSNs) which discharge phasic or phasic-sustained bursts before and during gaze
shifts are located in the PPRF (Grantyn et al. 1992; Isa
and Naito 1995), in the regions that also contain EBNs
and IBNs and the terminations of OPNs. The onsets of
RSN bursts precede saccades or head-free gaze shifts by
20–150 ms, similarly to the previously described saccade-related LLBs (Curthoys et al. 1981; Kaneko et al.
1981; Sasaki and Shimazu 1981). Many RSNs, in particular those of the phasic-sustained type, show decremental activity after saccade termination. Intracellular labelling with horseradish peroxidase (HRP) has shown that
some neurons, besides projecting to the spinal cord,
make connections with the abducens nucleus (Grantyn
and Berthoz 1987; Grantyn et al. 1992), and may therefore represent a source of excitatory input to abducens
motoneurons during pre- and postsaccadic slow movements (Olivier et al. 1993; Grantyn et al. 1996). Because
of a protracted perisaccadic firing of orienting-related
RSNs, it is obvious that their activity cannot be gated by
S-OPNs. On the other hand, pauses of C-OPNs have appropriate temporal characteristics to induce a prolonged
disinhibition, which is required to generate multisaccadic
gaze shifts, including perisaccadic drifts. We hypothesize
therefore that C-OPNs make stronger inhibitory connections with LLBs, including RSNs, while the main targets
of S-OPNs are IBNs and EBNs.
In conclusion, our study has shown that the OPN population in the cat is inhomogeneous. Besides well-known
saccade-related OPNs, there exists a previously undescribed subset of neurons whose firing properties are
suitable for inhibitory gating of complex gaze shifts. The
behaviour of such “complex” OPNs during isolated, single saccades suggests that they are a part of the saccade
generator. At the same time, their function appears to be
more closely related to the gating of saccade-related
LLBs, as well as RSNs participating in the control of eye
and head movements. Therefore they may play an essential role in the generation of slow perisaccadic eye movements in head-fixed cats. Our demonstration of complex
OPNs is complementary to the reports by Paré and Guitton (1990; 1998), who found that saccade-related OPNs
display a dual behaviour during head-free gaze shifts:
pauses for every saccade when the eyes make a sequence
300
of saccades and a single prolonged pause, lasting for the
whole duration of the gaze shift, when head movement is
associated with a single saccade. We predict that the
complex OPNs of the present study would also consistently pause for the total duration of gaze shifts in the
head-free condition. It is unclear why complex OPNs
were overlooked in earlier studies. One possible explanation is that their identification was facilitated in the present study by the use of fast-moving targets. This has substantially increased the occurrence of composite gaze
shifts, suitable for detecting OPNs with “complex” behaviour.
Acknowledgements The study was supported by the Human
Capital and Mobility Program of the Commission of the European
Community (contract no. CHRX-CT-94 0559). We wish to thank
Prof. Y. Laporte and Dr. S. Wiener for their valuable comments on
the manuscript and for checking the language.
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