 |
 Previous Article | Next Article 
The Journal of Neuroscience, November 15, 2002, 22(22):9877-9884
Saccadic Target Selection Deficits after Lateral Intraparietal
Area Inactivation in Monkeys
Claire
Wardak1,
Etienne
Olivier1, 2, and
Jean-René
Duhamel1
1 Institut des Sciences Cognitives, Unité Mixte
de Recherche 5015 Centre National de la Recherche
Scientifique-Université Claude Bernard Lyon 1, 69675 Bron Cedex,
France, and 2 Laboratoire de Neurophysiologie,
Université Catholique de Louvain, 1200 Bruxelles, Belgium
 |
ABSTRACT |
We investigated the contribution of the lateral intraparietal area
(LIP) to the selection of saccadic eye movement targets and to saccade
execution using muscimol-induced reversible inactivation and compared
those effects with inactivation of the adjacent ventral intraparietal
area (VIP) and with sham injections of saline into LIP. Three types of
tasks were used: saccades to single visual or memorized targets,
saccades to synchronous and asynchronous bilateral targets, and visual
search of a target among distractors. LIP inactivation failed to
produce deficits in the latency or accuracy of saccades to single
targets, but it dramatically reduced the frequency of contralateral
saccades in the presence of bilateral targets, and it increased search
time for a contralateral target during serial visual search. In the
latter task, the observed deficits might reflect either an ispilateral
bias in saccadic search strategy or an attentional impairment in
locating a target among flanking distractors within the contralateral
field. No effects were observed on any of these tasks after VIP
inactivation. These results suggest that one important contribution of
LIP to oculomotor behavior is the selection of targets for saccades in the context of competing visual stimuli.
Key words:
saccades; target selection; parietal; monkey; LIP; inactivation; visual salience
| |
INTRODUCTION |
Saccadic eye movements constitute
the primary means by which we explore our visual environment. Several
cerebral structures participate in the selection of eye movement
targets and in the execution of saccades. One of these is the lateral
intraparietal area (LIP). LIP receives input from several extrastriate
visual areas (Andersen et al., 1990 ; Felleman and Van Essen, 1991;
Bullier et al., 1996) and is reciprocally connected with the frontal
eye field and the superior colliculus (Lynch et al., 1985; Blatt et al., 1990). Single-cell recording experiments have shown that LIP
neurons carry visual signals that are modulated by attention (Colby et
al., 1996; Ben Hamed et al., 2002) as well as motor signals in relation
to the planning and execution of saccades (Barash et al., 1991a,b;
Colby et al., 1996). However, the exact role of LIP in relation to
saccadic behavior remains unclear. One hypothesis proposes that LIP
controls selective spatial attention and acts as a salience map of the
visual field (Gottlieb et al., 1998; Kusunoki et al., 2000). Another
hypothesis suggests that LIP is directly involved in the representation
of motor plans for saccades (Mazzoni et al., 1996). Although these two
proposals do not appear a priori incompatible because
attention and eye movements are often coupled, much of the controversy
about the role of LIP is centered on the issue of whether neuronal
activity in this area corresponds to a general attentional signal
uncommitted to a particular motor effector or whether this signal is
intrinsically linked to saccade preparation. The results from
single-cell recording experiments are equivocal in this respect. On the
one hand, the observation that LIP activity during a motor preparation
period is stronger for saccades than for reaching movements (Snyder et al., 1998) would appear to support the latter view. On the other hand,
it has been shown that LIP activity during saccade preparation reflects
the dynamics of attention as it is deviated from, and then returns to,
the saccade goal (Goldberg et al., 2002).
One empirical argument, which has received relatively little attention
in this debate, is the effect of lesions. Large parietal cortex
resections, which include LIP, cause minor increases in saccade latency
and negligible effects on accuracy (Lynch and McLaren, 1989). Li et al.
(1999) also found increased latency and slight hypometria of
memory-guided saccades after muscimol-induced inactivation of LIP. Such
deficits appear relatively minor compared with the near disappearance
of memory-guided saccades after frontal eye field (FEF) inactivation
(Dias and Segraves, 1999).
Here, we investigated the contribution of LIP to saccadic behavior
using several eye movement tasks to distinguish between effects of LIP
inactivation on target selection and saccade execution. We observed no
significant deficits during visually or memory-guided saccades to
single visual targets. However, the monkeys showed a strong
ipsilesional saccadic bias when two targets were presented simultaneously or with a small asynchrony. During visual search, LIP
inactivation biased ocular exploration ipsilesionally and increased
search time for a contralesional target. These results suggest the
implication of both attentional and decisional factors in the observed
saccadic target selection deficits.
| |
MATERIALS AND METHODS |
Two adult monkeys (Macaca mulatta, monkeys A and M)
weighing 5.5 and 6.5 kg were used in these experiments following
procedures approved by the local animal care committee in compliance
with the guidelines of European Community on animal care. Each monkey underwent a single surgical session under propofol anesthesia to
prepare for chronic recording of eye movements and extracellular recording within the parietal cortex. The animals were implanted with
scleral search coils (Judge et al., 1980) and a head-restraining device. On the basis of stereotaxic coordinates, a craniotomy was made
over the right parietal sulcus, and a stainless steel recording chamber
was implanted to allow access to LIP with microelectrodes and injection needles.
Throughout the duration of the experiments, the monkeys were seated in
a primate chair with their heads restrained, facing a tangent
translucent screen 35 cm away, which spanned ±55° of the visual
field. Behavioral paradigms, visual displays, and storage of both
neuronal discharge and eye movements were under the control of a
personal computer running a real-time data acquisition system (REX)
(Hays et al., 1982). Visual stimuli were back-projected onto the screen
by a digital light processing video projector. Eye movements were
recorded with the magnetic search coil technique (Primelec), and
horizontal and vertical eye positions were digitized at 250 Hz. All
data analyses were performed off-line.
Single neuron activity was recorded extracellularly with tungsten
microelectrodes (Frederick Haer; 1-2 M at 1 kHz), which were
lowered through a stainless steel guide tube by means of a hydraulic
microdrive (Narishige). Visual and saccade-related neuronal responses
were recorded in the lateral bank of the intraparietal sulcus to
determine precisely both the location and extent of LIP. The
limits of VIP were also identified on the basis of its distinctive
neuronal activity in relation to visual motion and somatosensory
stimulation (Duhamel et al., 1997, 1998).
Behavioral tasks. In the visually guided saccade paradigm,
monkeys were required to maintain central fixation for 1000-1600 msec
until the fixation point disappeared. At this time, a visual target
appeared at one of eight possible locations (14° of eccentricity, radially distributed about the fixation point at 45° intervals) in
randomly interleaved order. The monkeys received a liquid reward if
they made a saccade toward the target within 1000 msec of its appearance and maintained fixation there for at least 500 msec.
The memory-guided saccade task required the monkey to fixate centrally
for 300 msec. A target was then flashed for 100 msec at one of eight
locations (14° of eccentricity, radially distributed about the
fixation point at 45° intervals). The monkeys maintained fixation for
another 1200-1800 msec, until the fixation point disappeared, which
was the cue to look at the memorized target. If the monkeys made a
saccade at the appropriate time to the location of the target, the
target reappeared, and monkeys had to maintain fixation for another 500 msec to obtain a reward. The eye position tolerance windows were set at
2.5 and 5° at the central and peripheral locations, respectively.
The double-target paradigm was used to test for extinction as observed
in human patients with neglect. These patients are unable to report a
contralesional event when two bilateral events are in competition. The
monkeys fixated centrally for 500-1100 msec. On half of the trials, a
single eccentric target was flashed (50 msec for monkey M, 100 msec for
monkey A) at one of two possible locations (14° to the left or right
of fixation). On the other half of the trials, both targets were
flashed with a variable delay. Asynchrony ranged between  40 msec
(contralesional lag) and +280 msec (contralesional lead), by steps of
40 msec. The monkeys could make a saccade to any one of the two
but were rewarded for only 50% of the trials to avoid reinforcing a
possible natural directional bias. Fixation point extinction and
peripheral target appearance were offset by a 100 msec gap to prevent
the perception of an illusory movement toward the first target that
could influence the monkeys' choice.
In the visual search task, a central fixation period of 1000-1600 msec
was followed by presentation of a visual array containing one target
(0.8° red square) and several distractors. The stimuli were
distributed uniformly around a virtual circle of 14° radius, such
that the angles between adjacent stimuli were 90, 45, and 22.5° for
the 4-, 8-, and 16-stimulus arrays, respectively. The search array
remained visible for 2-3.5 sec, depending on array size. Monkeys were
allowed to perform several saccades and were rewarded when the target
was fixated for at least 500 msec. Two standard search conditions were
used, differing in their attentional demands. In the conjunction search
condition, a third of the distractors had the same shape as the target
but a different color (orange squares), a third had the same color but
different shape (red triangles), and the remaining third differed in
both shape and color (orange triangles). The target was thus defined by
a conjunction of form and color. In the feature search condition, a
single distractor type (orange triangle) was used. Linear regression
was used to characterize the effect of array size on search time. In
agreement with previous results in both humans and monkeys (Treisman
and Gelade, 1980; Bichot and Schall, 1999), feature search yielded virtually flat regression slopes of 1.08 and 1.04 msec per item, whereas in the conjunction condition search slopes rose to 5.4 and 11.5 msec per item. In one variant of the conjunction task, tested only in
monkey M, all items were placed on either the left or right side of the
fixation point, along a virtual semicircle of 14° radius for the 4 and 8 items conditions and of two semicircles of 12 and 16° radius
for the 16 items conditions. The target and distractors sets were
constructed from diamond and square shapes that could be yellow or
green. We used different stimuli because monkey M had developed over
time a rather shallow search slope with the previously used stimuli,
which may be an effect of overtraining. The novel objects produced a
slope of 17.1 msec per item, which is closer to those typically
obtained in human studies.
LIP inactivation. A solution of 2-6 µg/µl of muscimol
(Sigma) in saline was injected with a 5 µl Hamilton syringe connected to a 29 gauge stainless steel needle. Muscimol, a
GABAA agonist, was used because it interacts
specifically with GABAA receptors and does not
induce conduction block in fibers of passage. Two to three needle
tracks were performed in each experiment, and along each track, two
injections were made at distinct physiologically characterized sites of
LIP, separated by 2-4 mm. Tracks were made to depths of ~4-8 mm
below the cortex surface; the volume injected at each site was 0.5-1
µl and was delivered, by steps of 0.2 µl, every 2 min. The total
amount of muscimol injected in each experiment ranged between 12 and 24 µg. In both animals, the injections were made into the right parietal
cortex. After the injections were completed, double-target saccade
trials were run to detect the onset of muscimol effects, because
extinction was a reliable on-line behavioral marker of those effects,
which generally started 15-60 min after injection. All of the
different tasks could not be performed on a given inactivation
experiment; however, each one was tested several times (two to five for
visually and memory-guided saccade tasks, four to six for extinction
tasks, and five to seven for visual search tasks). The order of the
different tasks was counterbalanced across inactivation experiments,
and control data were always obtained on the following day and under
the same conditions. The entire duration of behavioral testing never
lasted >2 hr, well within the accepted temporal range of muscimol
effects (Malpeli, 1999; Martin and Ghez, 1999). Seven LIP inactivation
experiments were conducted in monkey M, and five were conducted in
monkey A. A physiological saline injection into LIP and a muscimol
inactivation of adjacent VIP in monkeys A and M, respectively, served
as a further control for the specificity of the effects.
Data analysis. Preliminary analysis of the data did not
indicate a systematic tendency for LIP inactivation to affect
particular target locations within the contralesional hemifield. Thus,
for the sake of presentation clarity, data for different target
locations were grouped by hemifield. Statistical comparisons between
performance on control and inactivation sessions were achieved by means
of two-way, inactivation condition × hemifield, ANOVAS, unless
specified otherwise. Because the monkeys performed many different tasks on a given inactivation session, relatively few trials were obtained for each level of the different factors manipulated in any given task.
This was particularly true of the visual search task in which target
location, number of distractors, and search condition were
systematically varied. Therefore, data from inactivation sessions and
for following-day control sessions were pooled together to increase
statistical power.
Histological procedure. In monkey A, an anatomical study was
performed at the end of the experiments to verify the approximate location of muscimol injection sites in LIP (Fig.
1). Fluorescent tracer (Fast Blue, Sigma;
5% in saline) was injected in two tracks, which had served previously
to inactivate LIP. The two tracks were separated by ~6 mm, and in
each track, two injections of 0.2 µl were performed at two depths,
separated by 1.5 mm. After a 24 hr survival period, anesthesia was
induced by ketamine injection (10 mg/kg, i.m.), and then the animal was
administered a lethal dose (60 mg/kg, i.p.) of sodium pentobarbital.
Four electrodes were lowered in the recording chamber, at each corner
of the grid. Once a deep anesthesia was attained, the animal was
perfused through the heart with a vascular rinse (0.9% NaCl in 0.1 M phosphate buffer, 5000 U of heparin at 36°C).
This was followed by fixative (3 l of 4% paraformaldehyde in 0.1 M phosphate buffer and 10% sucrose in 2 l
of 4% paraformaldehyde in 0.1 M phosphate
buffer, pH 7.3, at 4°C). After 45 min, the perfusion with fixative
was stopped and continued with 0.1 M phosphate
buffer (at 4°C) containing 20% sucrose. After perfusion, the head
was fixed in a stereotaxic apparatus, and the dorsal part of the
cranium was removed. One block containing the portion of the
intraparietal cortex delimited by the electrodes was made in the
stereotaxic coronal plane (approximately P15-P25); the block was kept
in 30% sucrose in 0.1 M phosphate buffer at
4°C until sinking. Coronal frozen sections were cut at 80 µm,
stored refrigerated in 0.1 M phosphate buffer,
and then mounted onto glass slides coated with gelatin-chrome alum.
High-power micrographs of sections containing injection sites
were obtained from a fluorescent microscope and a macrophotography
system by Olympus. Selected sections were then stained with cresyl
violet, and lower-power micrographs were taken to determine the
injection site location.
View larger version (59K):
[in this window]
[in a new window]
|
Figure 1.
Estimate of injection site
location in LIP. The top left panel shows a lateral view
of the right hemisphere in monkey A. The gray-shaded
area highlights the approximate position of LIP as
characterized electrophysiologically and projected onto the brain
surface. Vertical dashed lines indicate the level of the
coronal sections through the injection sites of Fast Blue. These
injections of fluorescent tracer reproduced the location of the two
more distant muscimol injections performed in this animal. The
top right panel shows the coronal sections indicated by
the vertical dashed lines on the lateral view of the
brain. The boxed outlines on the coronal sections
a and c indicate, respectively, the
location of the photomicrographs A and C
shown in the bottom panel. Scale bar, 10 mm. The
bottom panels illustrate photomicrographs of injection
sites at two different magnification factors. A,
C, Low-power photomicrographs showing coronal sections
from posterior and middle portions of the intraparietal sulcus stained
with the Nissl method. Black stars identify the
approximate location of the two Fast Blue injections performed along
each track. The boxed outlines indicate the location of
the photomicrographs B and D.
B, D, Higher-power photomicrographs
showing the core of the fluorescent tracer injections. Scale bars, 1 mm.
|
|
| |
RESULTS |
No effects on saccades to single targets
LIP inactivation did not alter the latency of visually and
memory-guided saccades directed to one of the eight possible targets (two-way ANOVA; no significant main effect of inactivation or hemifield × inactivation interaction in monkeys A and M, for both eye movement tasks). Figure
2A shows the mean
latency of visually guided saccades across three inactivation
experiments for monkey M and two inactivation experiments for monkey A. Figure 2B presents mean latency of memory-guided
saccades obtained in two inactivation experiments for each monkey.
Other saccade parameters, i.e., accuracy, duration, amplitude, and
omission rate, remained unchanged after LIP inactivation (two-way
ANOVA; no significant main effect of inactivation or hemifield × inactivation interaction in monkeys A and M) (Fig.
3). Similar results were obtained when
statistical analyses were performed on individual targets rather than
on data grouped by hemifield. The same analyses conducted on individual inactivation experiments did not reveal any deficits. Neither muscimol
injections in VIP nor saline injections in LIP produced deficits in
visually and memory-guided saccades (two-way ANOVA; no significant
inactivation main effect nor hemifield × inactivation interaction).
View larger version (42K):
[in this window]
[in a new window]
|
Figure 2.
Saccadic eye movement latency for eight target
directions spaced 45° apart. On all panels, the contralesional field
is on the left: visually guided saccade latencies
(A) and memory-guided saccade latencies
(B) for monkeys M and A, displayed in polar
coordinates. Dashed lines represent control data;
solid lines represent data obtained during LIP
inactivation.
|
|
View larger version (16K):
[in this window]
[in a new window]
|
Figure 3.
Memory-guided saccade accuracy. The contralesional
field is on the left. Ellipses represent mean ± 1 SD of saccadic endpoints. The central cross corresponds
to fixation point, and black dots correspond to target
location. Dashed lines represent control data;
solid lines represent data obtained during LIP
inactivation. deg, Degree.
|
|
Ipsilesional bias on saccades in the presence of two targets
The behavioral effects of LIP inactivation were also investigated
in a saccadic choice task in which monkeys were shown two briefly
flashed targets at 14° left and right of the fixation point, either
simultaneously or with a variable onset asynchrony. Extinction effects
were tested during the same inactivation experiments on which we also
tested visually and memory-guided saccade performance, and during
additional experiments for a total of six inactivations in monkey M and
four inactivations in monkey A. The effects were highly reproducible
because significant deficits were observed on every occasion.
The results pooled across all inactivation experiments are illustrated
in Figure 4. The probability of eliciting
either a left or a rightward saccade depended on the delay between the onset of the two targets. Although the transition between predominantly left and predominantly right choices was more abrupt in monkey M than
in monkey A (Fig. 4), in both animals the relationship between target
asynchrony and saccade probability shows a sigmoidal pattern. The point
of inflection of the logistic regression curve fitted to the data was
used as an indicator of the target onset asynchrony at which a switch
in saccadic preference occurred. In the control condition, the two
monkeys showed a natural bias toward the right side, because the left
target had to precede the right target slightly to obtain an equal
saccade probability in both directions (target asynchrony: +50 and +25
msec in monkeys M and A, respectively).
View larger version (19K):
[in this window]
[in a new window]
|
Figure 4.
Saccades to bilateral targets. Proportion of
contraversive saccades on double-target presentations in monkeys M and
A for the onset asynchrony of each target, and corresponding logistic
regression fits through inactivation (solid line:
p < 0.0001, r2 = 0.98 for monkey M;
p < 0.001, r2 = 0.94 for monkey A) and
control (dashed line: p < 0.001, r2 = 0.88 for monkey M;
p < 0.0001, r2 = 0.95 for monkey A) data.
Positive asynchrony means contralesional target leading the
ipsilesional one.
|
|
Disruption of LIP activity by muscimol injections led to a dramatic
decrease in the number of saccades made toward the left, contralesional
target when two targets were presented. Indeed, in both monkeys, LIP
inactivation severely altered the shape of the relationship between
target asynchrony and saccade probability ( 2; p < 0.01). In
monkey A, an equal saccade probability was obtained for a delay of
~200 msec, i.e., 180 msec later than in the control condition, and
the sigmoidal function showed a plateau at ~60%. In monkey M, even
when the contralesional target preceded the ipsilesional target by 280 msec, which was the longer delay investigated, the probability of
eliciting a saccade toward the contralesional target remained as low as
20% (Fig. 4). Given these low maximal proportions of contraversive
saccades, the inflection point of the sigmoid curve does not correspond
to an equal probability of saccades in either direction. It merely
indicates the target onset asynchrony value falling halfway between the
two extremes of the contraversive saccade probabilities under muscimol
inactivation. Relative to control inflection points, this change in
behavior occurred 120 msec later in monkey A and 176 msec later in
monkey M.
LIP inactivation also reduced the number of saccades successfully made
toward the contralesional target on interleaved trials in which a
single target was presented, whereas it did not have such effects on
visually guided saccades toward targets that are always presented
singly (see above). In monkey M, when a single contralesional target
was flashed, the percentage of error trials increased from 23.1% in
the control condition to 82.6% after LIP inactivation
(2; p < 0.0001); in
monkey A, it increased from 4.4 to 27.5%
(2; p < 0.0001) (Fig.
5). On such trials, the monkeys either
did not generate an eye movement or released an inappropriate saccade. These saccades (93% of the error trials) had a long latency (>300 msec) and did not have the stereotyped characteristics of goal-directed saccades. Rather, such saccades tended to have erratic velocity profiles and curved trajectories, similar to the saccades that monkeys
typically produce at the end of trials when breaking fixation. A small
minority of saccades (3% of the error trials) had a short latency and
were directed to the mirror position of the target, but this was also
true of error trials from control sessions. Finally, it is worth noting
that in monkey A, a significant decrease in the proportion of incorrect
trials was also observed after LIP inactivation when a single
ipsilesional target was presented (6.8 vs 1.4% after LIP inactivation;
2; p < 0.05) (Fig. 5).
These results indicate that the status of a single flashed target in
the context of a double-target task is different from that of a similar
target in the context of a single-target task such as visually or
memory-guided saccades, where the percentage of error trials on
contralesional side is unaffected by LIP inactivation (Table
1).
View larger version (12K):
[in this window]
[in a new window]
|
Figure 5.
Omissions on single-target trials intermingled
with double-target presentations. Horizontal bars show
the percentage of single-target trials on which the monkeys failed to
respond. White bars correspond to control data;
black bars correspond to data after LIP inactivation.
*p < 0.05.
|
|
Results obtained after muscimol injections in VIP or saline injections
in LIP were indistinguishable from those on no injection control
experiments (2; p > 0.05).
Target selection impairment during visual search
In the visual search task, the monkeys, by means of saccades, had
to look for a target presented among several nontarget distractors. Two
search conditions were investigated: in the feature search, the
distractors shared no feature with the target, although in the
conjunction search, the distractors shared either its color or its
shape, or neither of them.
Performance in the feature search task showed no contralesional
effect of LIP inactivation in either monkey on individual inactivation
experiments or on pooled data (target location × inactivation
interaction; p > 0.05). This task was performed during four separate inactivation experiments in monkey M and two experiments in monkey A. The overall search time was reduced in monkey M (171.0 vs
188.2 msec in control; inactivation main effect:
F(1,864) = 11.8; p < 0.001) and nonsignificantly increased in monkey A (240.6 vs 223.4 msec
in control; inactivation main effect: p > 0.05). This
was a rather easy task, with a single saccade sufficient to acquire the
target on 85-95% of the trials.
In contrast, search time was systematically increased in the
conjunction condition. On pooled data analysis, we found that for
monkey M, the overall mean search time was 288.3 msec after inactivation as compared with 226.8 msec in control. For monkey A,
search time rose from 361.5 msec to 534.5 msec. In both monkeys, search
time increased significantly as a function of the number of items,
independent of the inactivation condition (monkey M: F(2,902) = 34.9, p < 0.01; monkey A: F(2,678) = 17, p < 0.0001). More importantly, the effects of muscimol
were highly specific to the target location. In monkey M, there was a
selective effect of inactivation for contralesional targets
(F(1,902) = 10.7; p < 0.001) and a significant inactivation × number of items
interaction (F(2,902) = 7.9;
p < 0.001). Post hoc pairwise comparisons
(Student-Newman-Keuls; p < 0.05 corrected) showed
that the increase in search time was significant for 8 and 16 items,
but not 4 items (Fig. 6). For ipsilesional targets, no significant inactivation or inactivation × number of items interaction effects were found. In monkey A, search
time increased after LIP inactivation for contralesional targets
(inactivation: F(1,678) = 141;
p = 0.0002), regardless of the number of items in the
display (no inactivation × number of items interaction). No
significant effect of inactivation was observed on performance for
ipsilesional targets. These results were obtained during five and four
inactivation experiments in monkey M and monkey A, respectively.
Effects observed on individual inactivation experiments mirrored the
above pooled results, despite the fact that the data samples were
relatively small because of the large number of conditions. In monkey
M, significantly longer contralesional search time was observed for 16 items on all inactivation experiments and in three of five experiments
for 8 items. In monkey A, the contralesional increase in search time
failed to reach significance in only one of the four experiments.
View larger version (26K):
[in this window]
[in a new window]
|
Figure 6.
Visual search performance. Search time is shown as
a function of display size for contralesional (A)
and ipsilesional (B) targets. Search time for a
target defined by a conjunction of color (red vs orange) and form
(circle vs square) is defined as the interval between the search
pattern onset and the start of the saccade landing on the target
(bar height is mean search time; error bar indicates
SE). White bars correspond to control data; black
bars correspond to data after LIP inactivation.
Asterisk indicates corrected p < 0.05.
|
|
Because the number of saccades allowed to acquire the target was
unconstrained, we could examine the oculomotor search strategy adopted
by the monkeys in terms of where the eyes landed before arriving on the
target. Most of the errant saccades were directed toward ipsilesional
distractors. This is illustrated in Figure 7 with single trial examples from monkey
M, in which the initial saccades were both right-sided regardless of
target location. This monkey showed a contralesional side bias in
control experiments that was reversed after LIP inactivation, with
intermediate saccades now landing more often ipsilesionally (Fig.
8A)
(p < 0.0001;
2). In monkey A, a pronounced
ipsilesional bias was already present during control experiments, and
LIP inactivation did not exacerbate this tendency. Inspection of the
type of distractors visited indicates that saccades landed
preferentially on the ones having either the same shape or the same
color as the target, with monkey A in particular showing a natural
preference for same color over same shape distractors (Fig.
8B). There was no significant influence of LIP
inactivation on the distribution of saccades among the various types of
distractors in either monkey.
View larger version (15K):
[in this window]
[in a new window]
|
Figure 7.
Single-trial examples of visual search patterns
from monkey M during LIP inactivation. The small dots
represent eye position sampled every 4 msec; large dots
represent the search stimuli, and the circle represents
the location of the target. The contralesional field is on the
left.
|
|
View larger version (24K):
[in this window]
[in a new window]
|
Figure 8.
Characteristics of saccades to distractors.
A, Proportion of saccades directed to contralesional
(white bars) and ipsilesional (gray
bars) distractors. B, Proportion of saccades
directed to same-shape (white bars), same-color
(gray bars), and opposite (i.e., different shape
and color; black bars) distractors.
*p < 0.05.
|
|
The drawback of allowing multiple saccades is that it is not possible
to determine the extent to which longer visual search time reflects
inefficient processing of contralesional stimuli or a bias to make eye
movements toward the ipsilesional field. The contribution of the latter
factor is less of an issue on trials during which monkeys started
searching directly within the hemifield containing the target. A
separate analysis conducted on these trials showed only that search
time for contralesional targets is still significantly prolonged in
both monkeys (351.4 vs 276.1 msec for monkey A, p < 0.001; 234.8 vs 217.4 msec in control for monkey M, p < 0.05). A supplementary task was designed for monkey M, whose search
strategy showed a strong ipsilesional bias; in this task the entire
conjunction search display was confined to a single visual hemifield.
The task was performed by the monkey on two separate inactivation
experiments. The pooled results shown in Figure
9 indicate that LIP inactivation
increased search time for the target embedded in a contralesional array
(inactivation main effect: F(1,857) = 9.75; p = 0.0019; no inactivation × number of
items interaction) but had no effect on performance on the ipsilesional
array. The same pattern of results was obtained on each inactivation
experiment when analyzed individually. It is worth noting that during
this task, the monkey never made saccades to the empty hemifield,
whether ipsilesional or contralesional; eye movements were restricted
to the regions of space containing objects.
View larger version (20K):
[in this window]
[in a new window]
|
Figure 9.
Visual search performance for monkey M when all
items are placed within the same hemifield. Search time for a target
defined by a conjunction of color (yellow vs green) and form (diamond
vs square) is defined as the interval between the search pattern onset
and the start of the saccade landing on the target (bar
height is mean search time; error bar indicates SE). Spatial
layout of items is represented above each display size for the
contralesional (A) and ipsilesional
(B) sides. The contralesional field is on the
left. White bars correspond to control
data; black bars correspond to data after LIP
inactivation. Asterisk indicates corrected
p < 0.05.
|
|
The effects of muscimol inactivation in VIP and sham injections of
saline in LIP were tested on the conjunction search task with a
circular array, and performance did not differ from that of the
no-injection control experiments.
| |
DISCUSSION |
The main result of the present study is that
muscimol-induced inactivation of LIP impairs saccade target selection,
whereas saccade programming and execution per se remain unaffected. The absence of oculomotor impairments may seem surprising because LIP has
been described as a "parietal eye field" (Andersen et al., 1992)
and because a previous inactivation study showed latency and accuracy
deficits on memory-guided saccades (Li et al., 1999). Different
interpretations can be proposed to resolve this apparent contradiction,
in terms of differences in either the degree or topography of
inactivation. The first explanation suggests that a common neural
substrate exists in LIP for saccade programming and target selection
and that selection can be impaired even with a moderate level of
inactivation, whereas saccadic deficits only emerge at a higher level
of inactivation. The second interpretation implies segregated
subsystems within LIP for these two functions. Neither possibility can
be excluded given the differences in injection protocols used in the
two studies. Li et al. (1999) made principally a unique injection at a
high concentration of muscimol, whereas we made multiple smaller
injections at a lower concentration. Because the effects observed by
these authors were admittedly subtle, slight variations in behavioral
protocols used to assess memory-guided saccade performance might also
account for some of the discordant findings. Li et al. (1999) tested
their monkeys in total darkness, whereas in our study a moderate level
of background illumination was always maintained by the video
projection system. The absence of a visual reference frame in total
darkness, which requires a greater reliance on extra-retinal (eye
position) cues, might provide a more sensitive test of saccadic
performance. Although it is not possible at this stage to decide
between these different explanations, it is an interesting observation
on its own that target selection deficits can be observed in the
absence of any changes in saccade accuracy and onset latency.
Importantly, the effect of LIP inactivation on saccade performance does
not follow a simple correlation with overall task difficulty, as
assessed by the percentage of error trials (Table 1).
Extinction
After LIP inactivation, when presented with two possible targets,
monkeys directed their saccades almost exclusively toward the
ipsilesional one. The issue that needs to be addressed, and to which
our data do not speak directly, is the origin of this ipsilateral bias.
In human subjects, visual extinction is generally assessed through
verbal report and interpreted in terms of perceptual awareness
(Karnath, 1988; Di Pellegrino and De Renzi, 1995). The task used in the
present study measured a preferred motoric choice, and therefore does
not allow us to distinguish whether LIP inactivation induced
principally a detection deficit or an ipsilateral motor decision bias.
The latter interpretation would imply that both targets are detected
but that some kind of critical triggering threshold is reached earlier
for saccades directed ipsilaterally rather than contralaterally.
Intuitively, if signals related to ipsilateral and contralateral
saccades were processed independently and the main effect of LIP
inactivation would be to dampen the buildup of excitation for
contralesional saccades, one would expect abnormally long latencies for
contralateral saccades even in the absence of ipsilateral competition.
The fact that we did not observe this in either of our monkeys and that
deficits emerged only in the context of bilateral targets would suggest
rather that left and right saccade signals do not build up
independently and there is some kind of competitive interaction between
the two sides. Again, the critical site for this competition,
attentional or decisional, remains unclear.
Asynchronous targets have been used to study extinction-like effects in
humans in tasks involving temporal order judgment or saccadic choice.
Rorden et al. (1997) found that in parietal patients with visual
extinction, the contralesional stimulus has to lead the ipsilesional
one by 200 msec to be reported as having appeared first, as opposed to
<25 msec in normal subjects. Much more subtle effects have been
observed on saccadic choice, but the population of patients tested in
this second study no longer showed extinction and had normal temporal
order judgments (Ro et al., 2001). A 50 msec target onset asynchrony
was sufficient to produce an equal probability of left and right
saccades. Thus, despite the differences between the tasks used, the
effects of LIP inactivation that we obtained (on the order of 180 msec)
appear closer to those found in patients with extinction than in
patients with parietal lesions but no extinction.
The effects of LIP inactivation can also be contrasted with those of
FEF lesions. Schiller and Chou (1998) reported a 116 msec target onset
asynchrony for balanced choice, suggesting that the FEF is involved in
saccade target selection. However, one important difference is that in
their study, the proportion of contraversive saccades always approached
100%, whereas after LIP inactivation contralateral saccade probability
remained low, even with target onset asynchronies of 280 msec, which
are much larger than the monkeys' normal saccade latencies.
Furthermore, we found a large proportion of errors on interleaved
single contralateral saccade trials. Because such omissions were
observed only in this task and not during the memory-guided saccade
task, it suggests that after LIP inactivation, the overall task context
created a "virtual" competition between the two sides even on
single target trials. It is not clear whether the differences in the
magnitude of the effects of FEF and LIP lesions are attributable to the fact that Schiller and Chou (1998) made nonreversible lesions and
tested the animals in a chronic stage rather than in an acute stage as
in the present study, or whether this reveal a genuine difference in
the contribution of the two regions to saccade target selection.
Visual search
Visual search also involves competing stimuli, but in contrast
with the above task, irrelevant visual information has to be filtered
out to localize a single designated target among distractors. In a
visual search display, when potential distractors are homogeneous and
compete weakly with the designated target, search time is brief and
independent of the number of distractors. LIP inactivation has no
effect on search time in this so-called "pop-out" or "parallel" visual search (Treisman and Gelade, 1980). However, with many stimuli
in the display possessing some attributes of the target (e.g., its
color or its shape) and competing strongly with one another, the focus
of visual attention and, as in the present study, the eyes will shift
from one location to the next until the stimulus with the proper
conjunction of attributes is found. Our results reveal an important
role of LIP in this serial search process, but the nature of this role
needs to be identified more precisely. Clearly, we observed an
ipsilesionally biased oculomotor strategy in one of the two monkeys.
Whether this bias has motor or attentional origin is open to debate.
The differences in search time between the contralesional and
ispilesional fields remained present even when the oculomotor bias was
factored out (by looking only at trials in which search was initiated
toward the hemifield of the target). Furthermore, in the monkey showing
the strongest ipsilateral bias, the contralesional impairment remained
when the visual competition was confined to a single hemifield.
Altogether, these results suggest the implication of an attentional
component to the target selection deficit in the contralesional
hemifield. Interestingly, in the FEF, where neuronal responses during
search tasks have been related to target selection, it has been shown that the visual selection process can be dissociated from saccadic response selection in the activity of visually responsive neurons (Thompson et al., 1996; Murthy et al., 2001). This suggests that LIP
may participate in parallel with the FEF in both covert and overt
orienting during visual search.
In conclusion, muscimol inactivation of LIP produces deficits in
saccadic target selection, consistent with the hypothesis that LIP
represents a salience map of potential eye movement targets in the
contralateral visual field. These deficits are specific to LIP because
inactivation of a neighboring parietal region, VIP, did not produce any
effects in the tasks that we investigated. Our results appear in
agreement with human brain imaging experiments suggesting that the
intraparietal region is activated more strongly during conjunction
search than during single-feature search (Corbetta et al., 1995). Also,
patients with parietal lobe lesions show deficits in conjunction but
not in feature search (Eglin et al., 1989; Friedman-Hill et al., 1995);
however, these studies tested covert visual search procedure. Further
work will be needed to test whether the contribution of LIP to the
target selection is dedicated to a specific effector system, e.g.,
saccade versus reaching, and whether it is also involved in covert
attentional processing.
| |
FOOTNOTES |
Received June 3, 2002; revised Sept. 6, 2002; accepted Sept. 6, 2002.
This work was supported by the French Foundation for Medical Research
and the Centre National de la Recherche Scientifique. We thank Eric
Rouiller for providing support with the histological analysis.
Correspondence should be addressed to Jean-René Duhamel, Institut
des Sciences Cognitives, 67 Boulevard Pinel, 69675 Bron Cedex,
France. E-mail: jrd{at}isc.cnrs.fr.
| |
REFERENCES |
-
Andersen RA,
Asanuma C,
Essik G,
Siegel RM
(1990)
Cortico-cortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobule.
J Comp Neurol
296:65-113[Web of Science][Medline].
-
Andersen RA,
Brotchie PR,
Mazzoni P
(1992)
Evidence for the lateral intraparietal area as the parietal eye field.
Curr Opin Neurobiol
2:840-846[Medline].
-
Barash S,
Bracewell RM,
Fogassi L,
Gnadt JW,
Andersen RA
(1991a)
Saccade-related activity in the lateral intraparietal area. I. Temporal properties: comparison with area 7a.
J Neurophysiol
66:1095-1108[Abstract/Free Full Text].
-
Barash S,
Bracewell RM,
Fogassi L,
Gnadt JW,
Andersen RA
(1991b)
Saccade-related activity in the lateral intraparietal area. II. Spatial properties.
J Neurophysiol
66:1109-1124[Abstract/Free Full Text].
-
Ben Hamed S,
Duhamel J-R,
Bremmer F,
Graf W
(2002)
Visual receptive field modulation in the lateral intraparietal area during attentive fixation and free gaze.
Cereb Cortex
12:234-245[Abstract/Free Full Text].
-
Bichot NP,
Schall JD
(1999)
Saccade target selection in macaque during feature and conjunction visual search.
Vis Neurosci
16:81-89[Web of Science][Medline].
-
Blatt GJ,
Andersen RA,
Stoner GR
(1990)
Visual receptive field organization and cortico-cortical connections of the intraparietal area (area LIP) in the macaque.
J Comp Neurol
299:421-445[Web of Science][Medline].
-
Bullier J,
Schall JD,
Morel A
(1996)
Functional streams in occipito-frontal connections in the monkey.
Behav Brain Res
76:89-97[Web of Science][Medline].
-
Colby CL,
Duhamel J-R,
Goldberg ME
(1996)
Visual, presaccadic and cognitive activation of single neurons in monkey lateral intraparietal area.
J Neurophysiol
76:2841-2842[Abstract/Free Full Text].
-
Corbetta M,
Shulman GL,
Miezin FM,
Petersen FE
(1995)
Superior parietal cortex activation during spatial attention shifts and visual feature conjunction.
Science
270:802-805[Abstract/Free Full Text].
-
Dias EC,
Segraves MA
(1999)
Muscimol-induced inactivation of monkey frontal eye field: effects on visually and memory-guided saccades.
J Neurophysiol
81:2191-2214[Abstract/Free Full Text].
-
Di Pellegrino G,
De Renzi E
(1995)
An experimental investigation on the nature of extinction.
Neuropsychologia
33:153-170[Web of Science][Medline].
-
Duhamel J-R,
Bremmer F,
Ben Hamed S,
Werner G
(1997)
Spatial invariance of visual receptive fields in parietal cortex neurons.
Nature
389:845-848[Medline].
-
Duhamel J-R,
Colby CL,
Goldberg ME
(1998)
Ventral intraparietal area of the macaque: congruent visual and somatic response properties.
J Neurophysiol
79:126-136[Abstract/Free Full Text].
-
Eglin M,
Robertson LC,
Knight RT
(1989)
Visual search performance in the neglect syndrome.
J Cognit Neurosci
4:372-381.
-
Felleman DJ,
Van Essen DC
(1991)
Distributed hierarchical processing in the primate cerebral cortex.
Cereb Cortex
1:1-47[Abstract/Free Full Text].
-
Friedman-Hill SR,
Robertson LC,
Treisman A
(1995)
Parietal contributions to visual feature binding: evidence from a patient with bilateral lesions.
Science
269:853-855[Abstract/Free Full Text].
-
Goldberg ME,
Bisley J,
Powell KD,
Gottlieb J,
Kusunoki M
(2002)
The role of the lateral intraparietal area of the monkey in the generation of saccades and visuospatial attention.
Ann NY Acad Sci
956:205-215[Web of Science][Medline].
-
Gottlieb JP,
Kusunoki M,
Goldberg ME
(1998)
The representation of visual salience in monkey parietal cortex.
Nature
391:481-484[Medline].
-
Hays AV,
Richmond BJ,
Optican LM
(1982)
A UNIX-based multiple-process system for real-time data acquisition and control.
WESCON Conf Proc
2:1-10.
-
Judge SJ,
Richmond BJ,
Chu FC
(1980)
Implantation of magnetic search coils for measurements of eye position: an improved method.
Vision Res
20:535-538[Web of Science][Medline].
-
Karnath H-O
(1988)
Deficits of attention in acute and recovered visual hemi-neglect.
Neuropsychologia
26:27-43[Web of Science][Medline].
-
Kusunoki M,
Gottlieb J,
Goldberg ME
(2000)
The lateral intraparietal area as a salience map: the representation of abrupt onset, stimulus motion, and task relevance.
Vision Res
40:1459-1468[Web of Science][Medline].
-
Li C-SR,
Mazzoni P,
Andersen RA
(1999)
Effect of reversible inactivation of macaque lateral intraparietal area on visual and memory saccades.
J Neurophysiol
81:1827-1838[Abstract/Free Full Text].
-
Lynch JC,
McLaren JW
(1989)
Deficit of visual attention and saccadic eye movements after lesions of parietooccipital cortex in monkey.
J Neurophysiol
61:74-90[Abstract/Free Full Text].
-
Lynch JC,
Graybiel AM,
Lobeck LJ
(1985)
The differential projection of two cytoarchitectonic subregions of the inferior parietal lobule of macaque upon the deep layers of the superior colliculus.
J Comp Neurol
235:241-254[Web of Science][Medline].
-
Malpeli JG
(1999)
Reversible inactivation of subcortical sites by drug injection.
J Neurosci Methods
86:119-128[Web of Science][Medline].
-
Martin JH,
Ghez C
(1999)
Pharmacological inactivation in the analysis of the central control of movement.
J Neurosci Methods
86:145-159[Web of Science][Medline].
-
Mazzoni P,
Bracewell RM,
Barash S,
Andersen RA
(1996)
Motor intention activity in the macaque's lateral intraparietal area. I. Dissociation of motor plan from sensory memory.
J Neurophysiol
75:1233-1241[Abstract/Free Full Text].
-
Murthy A,
Thompson KG,
Schall JD
(2001)
Dynamic dissociation of visual selection from saccade programming in frontal eye field.
J Neurophysiol
86:2634-2637[Abstract/Free Full Text].
-
Ro T,
Rorden C,
Driver J,
Rafal R
(2001)
Ipsilesional biases in saccades but not perception after lesions of the human inferior parietal lobule.
J Cognit Neurosci
13:920-929[Web of Science][Medline].
-
Rorden C,
Mattingley JB,
Karnath H-O,
Driver J
(1997)
Visual extinction and prior entry: impaired perception of temporal order with intact motion perception after unilateral parietal damage.
Neuropsychologia
35:421-433[Web of Science][Medline].
-
Schiller PH,
Chou I
(1998)
The effects of frontal eye field and dorsomedial frontal cortex lesions on visually guided eye movements.
Nat Neurosci
1:248-253[Web of Science][Medline].
-
Snyder LH,
Batista AP,
Andersen RA
(1998)
Change in motor plan, without a change in the spatial locus of attention, modulates activity in posterior parietal cortex.
J Neurophysiol
79:2814-2819[Abstract/Free Full Text].
-
Thompson KG,
Hanes DP,
Bichot NP,
Schall JD
(1996)
Perceptual and motor processing stages identified in the activity of macaque frontal eye field neurons during visual search.
J Neurophysiol
76:4040-4055[Abstract/Free Full Text].
-
Treisman AM,
Gelade G
(1980)
A feature-integration theory of attention.
Cognit Psychol
12:97-136[Web of Science][Medline].
Copyright © 2002 Society for Neuroscience 0270-6474/02/22229877-08$05.00/0
This article has been cited by other articles:
|
|
|
|
 
P. F. Balan and J. Gottlieb
Functional Significance of Nonspatial Information in Monkey Lateral Intraparietal Area
J. Neurosci.,
June 24, 2009;
29(25):
8166 - 8176.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
D. J. Freedman and J. A. Assad
Distinct Encoding of Spatial and Nonspatial Visual Information in Parietal Cortex
J. Neurosci.,
April 29, 2009;
29(17):
5671 - 5680.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
T. Ogawa and H. Komatsu
Condition-Dependent and Condition-Independent Target Selection in the Macaque Posterior Parietal Cortex
J Neurophysiol,
February 1, 2009;
101(2):
721 - 736.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Campos, B. Breznen, and R. A. Andersen
Separate Representations of Target and Timing Cue Locations in the Supplementary Eye Fields
J Neurophysiol,
January 1, 2009;
101(1):
448 - 459.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. A. Thompson and D. Y. P. Henriques
Updating Visual Memory Across Eye Movements for Ocular and Arm Motor Control
J Neurophysiol,
November 1, 2008;
100(5):
2507 - 2514.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
E. L. Keller, K.-M. Lee, S.-W. Park, and J. A. Hill
Effect of Inactivation of the Cortical Frontal Eye Field on Saccades Generated in a Choice Response Paradigm
J Neurophysiol,
November 1, 2008;
100(5):
2726 - 2737.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Molenberghs, C. R. Gillebert, R. Peeters, and R. Vandenberghe
Convergence between Lesion-Symptom Mapping and Functional Magnetic Resonance Imaging of Spatially Selective Attention in the Intact Brain
J. Neurosci.,
March 26, 2008;
28(13):
3359 - 3373.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
P. Molenberghs, M. M. Mesulam, R. Peeters, and R. R. C. Vandenberghe
Remapping Attentional Priorities: Differential Contribution of Superior Parietal Lobule and Intraparietal Sulcus
Cereb Cortex,
November 1, 2007;
17(11):
2703 - 2712.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
N. W. D. Thomas and M. Pare
Temporal Processing of Saccade Targets in Parietal Cortex Area LIP During Visual Search
J Neurophysiol,
January 1, 2007;
97(1):
942 - 947.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Oristaglio, D. M. Schneider, P. F. Balan, and J. Gottlieb
Integration of Visuospatial and Effector Information during Symbolically Cued Limb Movements in Monkey Lateral Intraparietal Area.
J. Neurosci.,
August 9, 2006;
26(32):
8310 - 8319.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. E. Ipata, A. L. Gee, M. E. Goldberg, and J. W. Bisley
Activity in the lateral intraparietal area predicts the goal and latency of saccades in a free-viewing visual search task.
J. Neurosci.,
April 5, 2006;
26(14):
3656 - 3661.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. W. Bisley and M. E. Goldberg
Neural Correlates of Attention and Distractibility in the Lateral Intraparietal Area
J Neurophysiol,
March 1, 2006;
95(3):
1696 - 1717.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H.-O. Karnath and M. Dieterich
Spatial neglect--a vestibular disorder?
Brain,
February 1, 2006;
129(2):
293 - 305.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
J. Gottlieb, M. Kusunoki, and M. E. Goldberg
Simultaneous Representation of Saccade Targets and Visual Onsets in Monkey Lateral Intraparietal Area
Cereb Cortex,
August 1, 2005;
15(8):
1198 - 1206.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
M. Raffi and R. M. Siegel
Functional Architecture of Spatial Attention in the Parietal Cortex of the Behaving Monkey
J. Neurosci.,
May 25, 2005;
25(21):
5171 - 5186.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Battaglia-Mayer, M. Mascaro, E. Brunamonti, and R. Caminiti
The Over-representation of Contralateral Space in Parietal Cortex: A Positive Image of Directional Motor Components of Neglect?
Cereb Cortex,
May 1, 2005;
15(5):
514 - 525.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. J. Krauzlis
The Control of Voluntary Eye Movements: New Perspectives
Neuroscientist,
April 1, 2005;
11(2):
124 - 137.
[Abstract]
[PDF]
|
|
|
|
|
|
|
Y. E. Cohen, I. S. Cohen, and G. W. Gifford III
Modulation of LIP Activity by Predictive Auditory and Visual Cues
Cereb Cortex,
December 1, 2004;
14(12):
1287 - 1301.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. J. Leigh and C. Kennard
Using saccades as a research tool in the clinical neurosciences
Brain,
March 1, 2004;
127(3):
460 - 477.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
H. Scherberger, M. A. Goodale, and R. A. Andersen
Target Selection for Reaching and Saccades Share a Similar Behavioral Reference Frame in the Macaque
J Neurophysiol,
March 1, 2003;
89(3):
1456 - 1466.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
TOP
ABSTRACT
INTRODUCTION
